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THE VERTEBRATE EYE

AND ITS ADAPTIVE RADIATION

GORDON LYNN WALLS

Research Associate in Ophthalmology,
Wayne University College of Medicine

HAFNER PUBLISHING COMPANY

New York London

1963

reprinted by arrangement with
The Cranbrook Institute of Science

Printed and Published by

Hafner Publishing Company

31 East 10th Street

New York 3, New York

Library of Congress Catalog Card Number 63-17545

(§) copyright 1942

The Cranbrook Institute of Science

Bloomfield Hills, Michigan

All rights reserved. This book, or parts thereof, may
not be published in any form without the written
permission of the publishers.

PREFACE

The stmctural patterns of vertebrate eyes have been undergoing
intelligent scrutiny for about a century and a half. In that time, and
more and more rapidly toward the present, men have been learning
much about the functional meanings of those patterns, and their roles
in the lives of the animals which have produced them. It has seemed
to me that it is time an attempt was made to interpret comparative
ocular biology as a whole to those who want to know what the eye is
all about, but are repelled by the pedantic terminology of anatomy
texts, the mathematics of physiological optics, the scatteredness of the
ecological literature, and the German language. In this book, I have
made such an attempt.

I have chosen the term 'adaptive radiation' for the subtitle of this
work deliberately. It was coined by Henry Fairfield Osborn to describe
the manner in which animal groups have become diversified in pouring
themselves into a number of environmental molds which were made
available to them more or less simultaneously. It is a little unusual to
speak of the adaptive radiation of an organ; but I can think of no
better way to express what the vertebrate eye has done in modifying its
pattern to fit itself for the many different kinds of performance de-
manded of it by its adaptively-radiated owners.

The investigation of anatomy for its own sake is pretty well defunct.
The study of structures in relation to their employment by the animal
has hardly begun. When I started writing this book, I had never heard
of the late Hans Boker; but, in discussing the eyes of vertebrates in
terms of adaptation to environment, I believe I have followed the prin-
ciples of his 'comparative biological anatomy', which have so revivified
the study of anatomy in recent years.

If the comparative ophthalmologists of the world should ever hold
a convention, the first resolution they would pass would say: "Every-
thing in the vertebrate eye means something." Except for the brain,
there is no other organ in the body of which that can be said. It does
not matter in the least whether a liver has three lobes or four, or
whether the tip of the heart points north or south, or whether a hand
has five fingers or six, or whether a kidney is long and narrow or short
and wide. But if we should make comparable changes in the makeup of

PREFACE

a vertebrate eye, we should quite destroy its usefulness. Man can make
optical instruments only from such materials as brass and glass. Nature
has succeeded with only such things as leather and water and jelly; but
the resulting instrument is so delicately balanced that it will tolerate no
tampering.

And yet, vertebrate eyes are not all alike — far from it. Each is a
cluster of harmonious parts, and the changes which have converted one
type of eye into another, through evolution, have necessarily involved
most of its parts. When one feature has had to be altered for some
primary ecological reason, this alteration has in turn called for con-
current secondary alterations of other structures, with the whole complex
remaining harmonious and workable at all times. Of course, many eyes
contain little odds and ends of structures which have no function. But
in every such case, one can be sure that the structure in question did not
arise in its present form, but is a vestige of a once important part which
is no longer needed, or whose task has come to be done better by some-
thing else in the eye. When such remnants are in the way — and they
usually are — the eye gets rid of them promptly, which may add greatly
to the difficulty of determining how the ocular pattern of a given group
was ever derived from that of a known ancestor. Fortunately, however,
there are few such gaps; and it is now possible to tell a well-connected
story of the evolution of almost any particular vertebrate eye.

This book will be of particular benefit to zoologists and ecologists,
medical and veterinary ophthalmologists, and comparative psychologists.
But since none of these people speak the others' languages, I have been
able to assume no more scientific knowledge on the reader's part than the
contents of the usual elementary course in biology. The book should
therefore be entirely clear to any college student or graduate, and to any
amateur naturalist — 'trained' or not. As each unusual term has been
introduced, I have either defined it there and then or else placed it in the
glossary. The reader will find that the difficulty of the reading fluctuates,
which is inevitable in view of the varying weightiness of the material.
Some things about the eye and its workings are intricate, but I must
disclaim all responsibility for that — there are some subjects, such as
astrophysics and thermodynamics, which no writer could possibly 'pop-
ularize'. The reader will also soon note that my mode of expression is
strongly tainted with teleology. I do not expect this to mislead anyone —
it is merely an economy device, for it saves many words to say simply that
an animal has produced this feature or that to fill such-and-such a need.

PREFACE

The material of the book is progressive, though this may not seem
to be indicated by the table of contents. I could not explain everything
at once, but I have so arranged matters that a given discussion will be
perfectly lucid if the reader has not skipped much before it. I hope,
naively of course, that anyone who reads in the book at all will read
the whole of it. It is not designed as a reference book, in which to
'look up' small points from time to time. Rather, it has been written
in the style of a text-book, though for a course which has yet to be
given in any American university. The book is not documented, i.e.
loaded up with specific citations for every point of fact and reasoning
which has originated outside of my own studies. The average reader
will not miss them; and the earnest student who reads the book, and
is led thereby to want to do research in its field, will have to devour all
of the required reading listed in the bibliography anyway. He — and
the established investigator in the field — will readily know which of my
pronouncements to blame upon me alone. If not, he is free to write to
me for specific bibliographic assistance, which I shall gladly furnish
within the limitations of my time and ability.

Part I has been called 'basic' because it incorporates the first bodies
of information which the reader should have if he knows little or nothing
about the eye to begin with — even if he intends to skip straight to
Chapter 17 to find out what the pecten means. It is strongly urged that
every reader, even the ophthalmologist, read all of Part I before attempt-
ing to appreciate other chapters. In it, the human eye and human vision
have been used to acquaint the reader thoroughly with one sample eye
and its workings. The all-important retina is discussed in general terms.
The origins of the eye, ontogenetic and phylogenetic, are explained; and
the elementary facts of vertebrate inter-relationships are set forth so that
the non-zoological reader will understand the necessary taxonomic allu-
sions in Part II and the discussions of relationships and derivations
in Part III.

Part II is the ecological body of the work. Here are gathered to-
gether, unoier the banners of various environmental factors, the evolu-
tionary responses of the vertebrate eye to those factors. In these chapters,
at some risk of cluttering, I have included many cross-references to
ensure that the reader who insists on dabbling will not miss information
pertinent to the satisfaction of his momentary curiosity. Some matters
are expounded in more detail than others, somewhat in proportion to
the interest I have found them to arouse — the subject of animal color

PREFACE

vision, for example, is treated at particular length because no questions
are so often asked of the comparative ophthalmologist as those under
this aegis. Part II is an exposition of fundamental ideas rather than a
compendium of both explicable and at-present-useless facts. Because of
its ecological viewpoint, whole great fields find no place in it (or else-
where in this book) — ocular biochemistry, retinal photo-electrics, clinical
veterinary ophthalmology, most of physiological optics, and so on.
These chapters are intended to stimulate as well as to inform, and both
here and in Part III there is emphasis upon the more conspicuous of the
unsolved problems which await new students.

Part III traces the history of the eye, group by group, from the lowest
living vertebrates to the highest. Here, place has been made for those
features which are of importance to the eye itself as a living thing, but
are not discemibly concerned in its performance in relation to the special
environment of its owner. The emphasis in these synoptic chapters is on
the morphology of the eye, the evolution of that morphology, and the
bearing of it upon the problems of vertebrate phylogeny. The animal as
a whole explains much about its eye, and in turn the eye can often
explain much about the animal. Thus, the structural plan of the snake
eye, its possible mode of origin, and the significance of this for the
evolutionary history of the snakes, are all interconnected matters. The
reader will find numerous sub-indices in Part III which will enable him
to round up quickly all the information about his favorite group which
has been given earlier in the book, and is omitted here to avoid dupli-
cation and waste of space.

The illustrations have been kept as simple as possible, considering the
intricacies of the subject. Many are original, several of them — quite be-
yond my ability to make — beautifully drawn by the Misses Sylvia Hag-
yard and Gladys Larsen. Many others have been borrowed photograph-
ically from the journals, with or without changes (which are noted in
the legends) , and relabelled in accordance with a uniform scheme. Here,
much of the burden of work fell upon Albert Schlorff, without whose
expert photographic assistance I should have been quite helpless. I must
also acknowledge with gratitude the kindness of Viktor Franz in per-
mitting the free use of illustrations from his work. Figures 4, 5, and 41d
are by courtesy of William Bloom and the W. B. Saunders Company,
publishers of his 'Maximow's Text-Book of Histology'. Figures 6a and
16 are modified from Adler's 'Clinical Physiology of the Eye', by per-
mission of The MacMillan Company, publishers.

PREFACE

A great number of my friends have helped materially to make this
book possible, by criticizing portions of the manuscript relating to their
specialties, by furnishing specimens, information, or technical assistance;
and in other ways. I could not omit to mention some of them by name :
Ermine C. Case, Alfred Cowan, Elizabeth Crosby, Brian Curtis, Walter
F. Grether, Parker Heath, Selig Hecht, Arlington C. Krause, George
E. Lathrop, Wade H, Marshall, George A. Moore, Kevin J. O'Day,
Erich Sachs, John F. Shepard, Alec Skolnick, Gabriel Steiner, Francis
B. Sumner, Samuel A. Talbot, and Burton D, Thuma. During the
writing, generous financial support was forthcoming from the Wayne
University College of Medicine and from the Jennie Grogan Mendelson
Memorial Fund for Ophthalmology. During the actual making of the
book, the expert and sympathetic guidance of William L. Wood,
director of the Cranbrook Press, has been invaluable.

I am particularly obligated to the curators of the Museum of Zoology
of the University of Michigan and the Cranbrook Institute of Science
who read the entire text and straightened my kinks in their especial
realms: Carl L. Hubbs (fishes), Helen T, Gaige (amphibians and
reptiles) , Josselyn Van Tyne (birds) , and Robert T, Hatt (mammals) .

Finally, I am most deeply indebted of all to Director Hatt and the
Trustees of the Institute for their invitation to write the book as one of
their series of Bulletins, and for their generosity in the allowance of
space and illustrations. As is so usual with such books, the problem has
been to know how much to leave out. My trepidations in this connection
have led, during the writing, to several upward revisions of the expected
size of the work. I have felt as though I were behaving rather like the
camel which at first asked only to warm his nose within the Arab's tent,
and finished by crowding out the owner. My conscience will be easier
if most of my readers are glad that the book was not smaller.

G. L. W.
Detroit, Michigan
May, 1942

TABLE OF CONTENTS
Part I— Basic

Chapter Page

1. LIGHT AND ITS PERCEPTION 1

2. A TYPICAL VERTEBRATE EYE: THE HUMAN 6

A. Structures and their Functions 6

The Eye a 'Camera', 6 — The Fibrous Tunic, 7 — The Intra-
Ocular Fluids, 12— The Uveal Tract, 13— The Pupil, 17

— The Lens and Zonule, 19.

B. Optics and Accommodation 22

Refraction, 22 — Action of a Convex Lens, 2^ — Refractive
Errors of the Eye, 26 — Dioptrics of the Normal Eye, 29 —
Accommodation, 30.

C. The Ocular Adnexa 36

The Oculomotor Muscles, 36— The Lids, 38 — The Lac-
rimal System, 41.

3. THE VERTEBRATE RETINA 42

A. Histology and Physiology 42

The Pigment Epithelium, 42 — The Visual-Cell Layer, 45

— The Bipolar Layer, 46 — The Ganglion Layer, 47 —
Miiller Fibers, 48 — Neuroglia, 48 — Horizontal and Ama-
crine Cells, 49 — Nutrition of the Retina, 50 — The Optic
Nerve, 51.

B. Types of Visual Cells 52

General Types — Rods versus Cones, 52 — Single Cones, 53
— Rods, 57 — Homology of Rods and Cones, 57 — Green
Rods, 58— Double Cones, 58 — Twin Cones, 60 — Ophidian
Double Cones, 61 — Double Rods, 62.

C. The Duplicity Theory 64

History, 64 — Sensitivity versus Acuity, 65 — Retinal Fac-
tors in Acuity, 65 — Retinal Factors in Sensitivity, 68 —
Evidence for Duplicity of Vision, 71.

4. THE VISUAL PROCESS 74

A. ScoTOPic Vision 74

Rhodopsin, 74 — Dark Adaptation, 76 — Rod Vision, 79.

TABLE OF CONTENTS

B. Photopic Vision 81

Cone Vision, 81 — Color, 81 — Saturation, 84 — Brightness
and the Purkinje Phenomenon, 87 — Trichromatic Vision,
88 — Central Events in Trichromatic Vision, 91 — Color
Blindness, 96 — Photochemistry of Color Vision, 100.

5. THE GENESIS OF THE VERTEBRATE EYE . . .104

A. Embryological 104

Formation of the Optic Cup, 104 — Differentiation of the
Retina, 108— The Lens, 109— The Hyaloid Circulation,

113 — The Vitreous, 113 — The Vascular and Fibrous
Tunics, 114 — Lids and Glands, 117 — -Variations in Non-
Mammals, 117.

B. Evolutionary 119

The Eye a 'Part of the Brain', 119 — Early Theories, 120 —
Balfour's Theory, 122 — The Placode Theory, 125 — Bo-
veri's Theory, 125 — Studnicka's Theory, 126 — Origin of
the Retina, 128— Origin of the Lens, 129.

6. ELEMENTS OF VERTEBRATE PHYLOGENY . . .134

Part II — Ecologic

Chapter ^ Page

7. ADAPTATIONS TO ARHYTHMIC ACTIVITY . . 143

A. The Twenty-Four-Hour Habit and the Eye . . 143

B. Retinal Photomechanical Changes . . .145

Pigment Migration, 146 — ^Visual-Cell Movements, 147 —
Significance and Distribution, 149 — Immediate Causation,
151.

C. Pupil Mobility 153

Functions of the Pupil, 153 — Pupillary versus Retinal
Adaptation, 154 — Comparative Survey of the Two Meth-
ods, 158.

D. DuPLiaTY and Transmutation 163

8. ADAPTATIONS TO DIURNAL ACTIVITY .169

A. DiuRNALiTY AND THE Eye 169

Diumality and Sharp Vision, 169 — Diurnality, Acuity,

and Food, 169— The Eye as a Whole, 171.

B. The Diurnal Retina 175

Cone: Rod and Receptor: Conductor Ratios, 175 — Minimiz-
ation of the Physiological Scotoma, 178.

TABLE OF CONTENTS

C. Are^ Centrales and Foveje 181

The Area Centralis, 181 — The Fovea, 182 — Distribution,
184.

D. Intra-Ocular Color-Filters 191

Types and Distribution, 191 — The Color- Vision Theory,

192 — Yellow Filters and Chromatic Aberration, 193 —
Other Values, 195— Red Filters and the Rayleigh Effect,
197— Value of Red Oil-Droplets in Birds, 197— Value of
Red Oil-Droplets in Turtles, 197 — Phylogeny and Chem-
istry of the Intra-Ocular Filters, 199.

9. ADAPTATIONS TO NOCTURNAL ACTIVITY . . 206

A. Nocturnality and the Eye 206

Noctumality and Crude Vision, 206 — Advantages and
Limitations, 208 — Lightless Habitats and their Conquest,

209— Tne Eye as a Whole, 210— Tubular' Eyes, 212—
Spherical Lenses, 213 — Broad Comeae, 214.

B. The Nocturnal Retina 215

Rod: Cone Ratios, 215 — Pure- Rod Animals, 216 — Sum-
mation, 216.

C. The Slit Pupil 217

Value of the Slit Form, 218 — -Distribution and Meanings
of Pupil Shapes, 219.

D. The Tapetum Lucidum 228

Value and Basis of Eyeshine, 229 — The Tapetum Fibro-

sum, 231 — The Tapetum Cellulosum, 233 — Guanin and
the Argentea, 235 — Guanin in Retinal Tapeta, 236 — Other
Retinal Tapeta, 238 — Guanin in Chorioidal Tapeta, 238 —
Phylogeny and Relative Efficiency of Tapeta, 243— The
Tapetum and Visual Acuity, 245.

10. ADAPTATIONS TO SPACE AND MOTION . . .247
A. Accommodation and its Substitutes .... 247
Dependence of Apparent Distance upon Size, 247 — The
Why of Accommodation, 249— Devices Which Make
Accommodation Unnecessary, 253 — Vertebrate Methods
of Accommodation, 257 — Lampreys, 258 — Elasmobranchs,
260— Teleosts, 260--Other Fishes, 263— Matthiessen's
Ratio, 2&\ — Optical Elimination of the Cornea, 2M — Con-
sequences of Lens Movement, 265 — Amphibians, 265 —
Role of the Vitreous in Ichthyopsidan Accommodation, 268
— Sauropsidan Muscles of Accommodation, 269 — Scleral
Ossicles in Sauropsida, 270 — Accommodation in Saurop-
sida (Except Snakes), 275 — Special Features in Birds and
Lizards, 279— Snakes, 282— Mammals, 283.

TABLE OF CONTENTS

B. Visual Angles and Fields 288

Visual Angles, 289 — Position of the Eyes in the Head,
290 — Extent of the Binocular Field, 291 — Devices for
Enlarging the Binocular Field, 299.

C. Eye Movements and the Fovea 300

Kinds of Eye Movements, 300 — Fishes, 303 — Amphibians,
305— Reptiles, 305— Birds, and the Visual Trident, 307—
Mammals, 310.

D. Depth- and Solidity-Perception 313

Clues to Depth and Distance, 313 — Stereopsis in Man,

315 — The Optic Chiasma in Man and Other Vertebrates,
319 — Supposed Value of Partial Decussation, 320 — The
Case for Singleness in Animals, 323 — The Evolution of
Binocular Vision, 326 — The Nature and Basis of Fusion,
331 — The Strange Fate of the Median Eyes, 338 — Sub-
stitutes for Binocular Stereopsis, 341.

E. Movement-Perception 342

Detection versus Saliency, 343 — Grades of Movement, 345
— The Relativity of Movement-Perception, 347 — Motor
Factors in Movement-Detection, 348 — Sensory Factors in
Movement-Detection, 349 — Adaptation, and Center versus
Periphery, 352 — Stroboscopic Movement versus Real Move-
ment, 356 — Stroboscopic Vision in Animals, 362 — Men-
ner's Theory of the Pecten, 365 — Multiple Optic Pap-
illa, 367.

11. ADAPTATIONS TO MEDIA AND SUBSTRATES . . 368

A. Aquatic Vision 368

Definition, 368 — Effect of Water upon the Plan of the

Eye, 369 — Origin of Intra-Ocular Fluids, 371 — Effects of
Water upon Light, 373 — Looking Through the Surface,
377 — Streamlining of the Eyeball, 379 — 'Adipose Lids',
381— Bottom Fishes, 384 — Cave Fishes, 387— Parasitic
Fishes, 390 — Deep-Sea Fishes, 391 — Deep-Sea Larval Eyes,
403 — The Common Eel, 405 — Aquatic Amphibia, 407 —
Sirenians^CC^Whales, 410— Adaptation to Water Pres-
sure?, 415.

B. Aerial Vision 417

Changes in Dioptrics, 417— New Extra-Ocular Structures,
418 — Adnexa in Amphibia, 418 — The Third Lid and the
Fate of the Retractor, 419 — Adnexa in Sphenodon, 420 —
Crocodilians, 421 — Turtles, 422 — Lizards, 423 — Snakes,
424 — Birds, 424 — Mammals, 425 — Inter-Relations of
Globe and Adnexa, 427 — Peculiar Status of the Elasmo-
branchs, 428.

TABLE OF CONTENTS

C. AiR-AND- Water Vision 429

The Main Problem, 429 — Amphibious Vision in Teleosts,

431 — Amphibians and Crocodilians, 436 — Turtles, 436 —
Amphibious Squamates, 438 — Amphibious Birds, 438 —
Amphibious Mammals, 442.

D. The Spectacle 449

Injurious Substrates, 449 — Types of Spectacles, 449 — Pri-
mary Spectacles and the History of the Cornea and Con-
junctiva, 449 — Secondary Spectacles, 453 — Tertiary Spec-
tacles in Reptiles, 454 — Tertiary Spectacles in Fishes, 459.

12. ADAPTATIONS TO PHOTIC QUALITY . . . .462

A. Color Vision in Animals 462

The Limits of the Spectrum, 462 — Value and Origin of

Color Vision — 462 — Evidence for Color Vision, 465 — A
Sample Ideal Procedure for Investigation, 467 — Fishes,
472— Amphibians, 490— Reptiles, 494— Birds, 497— Mam-
mals, 504 — Phylogeny of Color Vision, 518 — Locus of
Color Vision, 521.

B. Dermal Color-Changes 523

Modes of Color Change, 524 — 'Physiological' and 'Morph-
ological' Chromatophoral Changes, 526 — Control Through
the Eye, 527^ — Physiological Color Changes in Teleosts,
528 — Mode of Control in Teleosts, 529 — Response to
Albedo, 530 — Morphological Color Changes in Teleosts,
532 — Color Changes in Amphibians, 535 — Dermal Changes
in Lower Fishes, and 'Diurnal Rhythms', 537 — Color
Changes in Reptiles, 538.

C. Coloration of the Eye 543

Basis of Iris Colors, 543— Possible Significance, 543 —
Conspicuousness of the Eye, 544 — Concealment of the
Eye?, 544 — Concealment of the Pupil?, 548— Sexual and
Temporal Differences, 549.

Part III — Synoptic

Chapter ^ ^ Page

13. CYCLOSTOMES 555

A. Lampreys 555

The Eye as a Whole, 555— The Retina, 560.

B. Hags 562

14. HIGHER FISHES 563

A. Elasmobranchs 563

The Eye as a Whole, 563— The Retina, 568.

TABLE OF CONTENTS

B. Chondrosteans 569

The Eye as a Whole, 569— The Retina, 572.

C HOLOSTEANS AND TeLEOSTS 573

Holosteans, 573 — The Holostean Retina, 576 — Teleosts,
576— The Teleost Retina, 584.
D. Cladistians and Dipnoans . . . . . . 588

Cladistians, 589 — Dipnoans, 589 — The Dipnoan Retina,
590.

15. AMPHIBIANS 592

A. Anurans 593

The Eye as a Whole, 593— The Retina, 598.

B. Urodeles 600

The Eye as a Whole, 601 — The Retina, 603 — Comparison
with Fishes, 604.

C. C^CILIANS 605

16. REPTILES *..... 607

A. Chelonians 608

The Eye as a Whole, 609— The Retina, 611.

B. Crocodilians 613

The Eye as a Whole, 613— The Retina, 615.

C. Sphenodon 616

The Eye as a Whole, 617— The Retina, 620.

D. Squamates 622

Lizards, 622 — The Lacertilian Retina, 625— Snakes, 627 — ■

The History of the Snake Eye, 632 — The Ophidian Ret-
ina, 636.

17. BIRDS 641

The Eye as a Whole, 641 — The Pecten, and its Analogues
in Other Vertebrates, 648— The Retina, 659.

18. MAMMALS 663

A. Monotremes and Marsupials 664

The Monotreme Eye, 664 — The Monotreme Retina, 669 —

The Marsupial Eye, 671 — The Marsupial Retina, 674.

B. Placentals 675

The Eye as a Whole, 676— The Retina, 684— The Early
History of the Placentalian Eye, 686.

BIBLIOGRAPHY 693

INDEX AND GLOSSARY 721

xiv

Part I -Basic

Chapter 1
LIGHT AND ITS PERCEPTION

The principal means by which most animals are made aware of their
surroundings, and changes in these surroundings, is the reflection or
emission of light toward them by external objects and the reception of
this light by special organs which we term photoreceptors. The more
complicated of these photoreceptors are called eyes, though it is not
complexity, as such, which governs the applicability of that special term.
We say that the function of the eye is vision, but since all photoreception
is not vision and not all photoreceptors are eyes, we must consider these
broader and narrower terms before delving into our subject proper —
the structure and variations of vertebrate eyes and their relation to the
ways of life of their possessors.

Light may best be defined, for our purposes here, as a rhythmic eman-
ation of energy whose rhythm-frequency or pitch falls within definite
limits, outside of which are the higher or lower frequencies of radio,
cosmic, X-, and other rays. Visible light thus forms a circumscribed
band of frequencies to which the eye happens to be sensitive and which,
compared with all forms of radiant energy in general, is like a single
octave toward the high-pitched end of the scale of a piano (see Table I) .
It contains only a small fraction of the total amount of energy given off
by the sun, and sunlight in turn forms only a portion of the 'grand
spectrum' of radiant energy. Like other forms of radiant energy, light
in its ultimate units can vary in but simple ways — in speed, in frequency,
and in intensity. But natural lights and illuminations are complex mix-
tures of these variations, and make possible the infinite variety of nature's
pictures, varying in tone or shading (owing to combinations of inten-
sities) and in color or hue (owing to combinations of frequencies) ,

We have been discussing light as an objective physical entity; but, just
as there would be no sound if a tree were to fall with no one to hear it,
so also there would be no light in the physiological sense if there were no
photoreceptor upon which it impinged. In this other sense light is a
sensation, an experience in consciousness. Like other such experiences,
it may be evoked by a limited number of causes (other than actual

2 LIGHT AND ITS PERCEPTION

physical light) . The qualities of a light-sensation bear only a close, not
an absolute, relationship to the objective attributes of a physical light
which produces it. Thus, different colors may be seen under special cir-
cumstances when the corresponding different frequencies of light are
not being steadily presented to the eye at all, or the same color may
result from totally different mixtures of frequencies. Two lights with the
same energy-content may appear different in brightness while two others,
equally bright, may differ greatly in actual physical intensity. Color and
brightness are thus subjective correlates of the objective frequency and
intensity. The former can be perceived but not measured, while the latter
can be measured with inanimate instruments but cannot be perceived
with the eye.

A sobering array of optical illusions may be seen by the reader in any
good reference work on psychology, and will serve to teach, still more
emphatically, the lesson that: "Our eyes do not see; but we see with our
eyes." Photoreception is one thing — it may be conscious, the reception
of the external stimulus of light upon the sill of the "window of the
soul" — or it may lead reflexly to quite unconscious activities such as the
change of the size of the pupil, the aiming of the eyes, the blinking of
the lids when the eye is about to be struck by something, and so on.

Vision is something more. It is the complex and sometimes deceptive
product of the interaction of the simple information which travels along
the optic nerve and the manipulations, as yet unfathomable, which this
information undergoes in the brain before it is presented to the con-
sciousness for action or other disposal.

A photoreceptor may be constituted by a single part of a one-celled
animal; by one of a number of similar, scattered, photosensory cells in
an invertebrate's skin; by a patch of cells closely aggregated into a plate,
or lining a pit; or by an ocellus or eye (Fig. 1). This last term is best
reserved for those photoreceptors in which there is a light-sensitive layer
of cells upon which accessory parts converge the light rays received from
environmental objects. An eye, then, ordinarily contains at least a photo-
sensory epithelium or retina, and a lens. An image may however be
formed upon the retina by a pinhole (as in the chambered nautilus)
instead of by a lens; or, the lens in a given type of eye may be employed
to concentrate the light in order that the eye may work in dimmer illum-
inations, instead of to form an image so that the mind may have a picture.
Finally, a number of 'concentrator' units may be congregated so that a
mosaic image can be built up in the consciousness itself, and it is upon

OBJECTIVE AND SUBJECTIVE LIGHT 3

this plan that the 'compound' eyes of many arthropods are constructed.
Vertebrate eyes are all built upon one fundamental plan. With the
exception of those which have degenerated because their owners live
underground, or in the perpetual night of caves or the depths of the
ocean, they are provided with a retina and with a lens whose optical
properties are such that it forms an image upon the retina. The lenses of
the median eyes which some reptiles possess on the top of the head are
probably often of the concentrator type; but those of the lateral, or
ordinary, eyes are nearly always eikonogenic — that is, image-forming.

c n^

Fig. 1 — Various photoreceptors.

a, intracellular type in a one-celled animal, Pouchetia cornuta. b, scattered photosensory
cells in the skin of an earthworm, c, pit-like visual organ of a limpet, Patella, d, pinhole-
camera type of eye in the chambered nautilus, e, ocellus of a scorpion, Euscorpius, with
concentrating lens, f, eye of a snail, Murex. g, image-forming eye of a squid, Loligo.
h, eye of vertebrate.

c- cuticle; e- epithelium; /- lens; n- nerve fibers; p- pupil; r- retina; s- secreted material.

Before we pass to a consideration of the detailed structure and work-
ings of a standard vertebrate eye, it needs to be further emphasized that
vision, seeing, is a phenomenon of the mind plus the eye and not of the
eye alone. It would probably not stagger any reader of this book to be
asked to believe that a worm may react to a light-stimulus without having
a sensation or consciousness of light. Vertebrate vision as we ourselves
experience it, however, is more than just photoreception. Vertebrate
visual mechanisms, from fish to mammal, are so nicely constructed that
so far as the eyes themselves are concerned, they may in many cases send

LIGHT AND ITS PERCEPTION

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VISION VERSUS PHOT ORECEPT ION 5

to the central nervous system all of the information that human brains
receive from human eyes. That does not mean at all, however, that the
same use and value is ever made and obtained from that information.

Many vertebrates with perfectly good eyes, as complex as our own,
may not see anything. In explanation of this perhaps surprising state-
ment, it may be enough to point out that the portion of the brain in
which human visual impulses terminate and are integrated — in which,
in other words, vision seems to reside — is not present in the brains of
fishes at all. A fish may have a knowing look in his eye as he passes up
one kind of fly and avidly seizes another, but we have no right whatever
to assume that he sees either fly, or indeed anything else. It is quite
possible that he is acting, like the worm, only reflexly and without con-
scious accompaniments to patterns of shade and hue which, given a
brain capable of the analysis ours can perform, would be mental pictures
to him as they are to us.

When therefore, elsewhere in this book, such questions are raised as :
"Do dogs see colors?" and "Can fishes tell a square from a triangle?"
the reader must visualize 'see' and 'tell' in tell-tale quotation marks, and
bear with the writer if he seems to lapse into anthropocentrism and to
attribute conscious visual acts to animals whose dim minds we cannot
read. It is easiest to compare the visual potentialities of one ocular
mechanism with those of another as though behind each there lay a brain
like that of man; but it is hoped that without further frequent reminder,
the reader will forever remember this :

Human vision, so valuable and so kaleidoscopic, is the product of a
complex brain teamed with a relatively simple eye; and when we some-
times encounter more complex eyes (which are always connected with
simpler brains) we must not assume that they afford their owners any-
thing so informative of the environment as does the vision we experience.
"Nothing is in the mind which is not first in the senses" — but the sense-
organs, and particularly the eye, may offer the mind much more than
the latter can assimilate.

Chapter 2

A TYPICAL VERTEBRATE EYE: THE HUMAN

(A) Structures and their Functions

The human eye will serve admirably as an introduction to vertebrate
ocular morphology and physiology, for it is fairly well generalized and
presents no bizarre features. In the ensuing discussion, fine structural
and terminological details will be given only where they are important
for an understanding of the workings of the eye. Any detailed descrip-

y /////////////////////////A

V///////////////////////77,

Fig. 2 — Comparison of eye and camera.

Parts which correspond in function bear similar numbers. /- retina = film, on curved track;
2a- cornea = front element of lens; 2h- crystalline lens = rear element of lens; j- iris :z dia-
phragm between lens elements; 4- pigment of chorioid coat = flat black paint; 5- eyelids =
roller-blind shutter.

tion of the human retina will be omitted here, since a general treatment
of the vertebrate retina is given in Chapter 3. The reader who wishes to
learn the histology of the human eye for its own sake will of course study
actual preparations and a textbook of microscopic anatomy.

The Eye a 'Camera' — It is almost a cUche to say that the eye is built
like a camera (Fig. 2) . In each there is a sensitive screen (retina = film
or plate) on which an inverted image is formed by a lens (corneas-
crystalline lens = lens). One device (lids = shutter) can exclude light,
which when admitted by it is regulated in amount by a variable aperture
(pupil = diaphragm aperture). The interior is darkened (chorioid pig-
ment = dead black paint) so that internal reflections will not blur or

THE EYE A 'CAMERA'

multiply the image. Lastly, the whole apparatus can be set to take
equally sharp pictures at different distances (accommodation = substi-
tuting one lens for another in the camera, or varying distance between
lens and film).

posterior chamber
limbal zone.

conjunctiva
canal of Sc hie mm
ciliary muscle

sclera
chorioid'

lamina cribrosa

Fig. 3 — Horizontal section of right human eye. x 4. Modified from Salzmann.

On the left, the section contains a cihary process behind which the zonule fibers are partly
concealed; on the right, the section has passed between two ciliary processes and the full
extent of the zonule fibers can be seen. The limbal zone (transition between cornea and
sclera) is stippled to emphasize that it is broader internally than externally.

The Fibrous Tunic — The outer case of the living camera is formed
by the fibrous tunic, consisting of the sclera and the cornea, the latter
seemingly a transparent anterior continuation of the sclerotic coat which

8 A TYPICAL VERTEBRATE EYE: THE HUMAN

is more sharply curved than the latter (Fig. 3). A substantial portion of
the thickness of the cornea represents the skin of the head, which during
evolution became affixed to the eyeball, leaving loose places, to permit
eye movements, up underneath the eyelids where it merges with their
linings to join the ordinary outer skin at the lid margins. Only some of
the inner layers of tissue in the cornea represent a clear window in the
original, ancestral, fibrous capsule. As a matter of fact, the sclera itself

Fig. -I — Fibrous and vascular tunics of the human eyeball, x 135.
Modified from Maximow and Bloom, after Schaffer.

a, sclera and chorioid.

a- artery; c- choriocapillaris layer of chorioid; Iv- lamina vitrea; s- sclera; v- vein; vl- vascular,
pigmented layers of chorioid.

b, cornea.

b- Bowman's membrane; d- Descemet's membrane; e- epithelium; m- mesothelium; p- sub-
stantia propria.

is almost as transparent as the cornea in many of the lower vertebrates.
The 'white' of the human eye is differentiated from the clear cornea not
because the latter has become transparent secondarily, but rather because
the sclera has become clouded. What has happened in evolution also
takes place in individual development, and the clear parts of the em-
bryonic eye are clear from the start and remain so — they do not become

THE FIBROUS TUNIC 9

SO. Despite this easily ascertained fact, many speculations have been
made as to what factor is responsible for the transparency of the cornea
and the lens. The really interesting question is, what makes the other
tissues of the developing embryo become opaque.

The sclera (Fig. 4a, s) is composed of tough, inelastic, tendinous tissue
organized in ribbon-like bundles of microscopic fibers which are felted
together in such a way that the whole tissue is about equally strong in all
directions — to resist the intraocular pressure, equal of course in all direc-
tions, without allowing the eyeball to change its shape. The flat fiber-
bundles are of unknown length, for their ends cannot be found; but each
seems to arise somewhere behind the rim of the cornea, runs parallel
thereto for a space, then courses backward around the eye and forward
again in a wide loop — not, however, following a great circle of the ocular
sphere. The tissue of the sclera contains very few cells. It consists chiefly
of the lifeless fibers, and its rate of living (metabolism) is so low that
it requires no direct blood supply. Nearly all of the blood vessels to be
seen in sections of the sclera are merely passing through it on their way
into or out of the chorioid coat.

The layers of fibers in the cornea (Fig. 4b) are not so much felted
as in the sclera, but run more nearly parallel with less interchange of
fibers between layers. The cells between them are consequently more
definitely organized into layers also; but they are scattered very far apart
in a given layer. The substance of the healthy cornea is quite devoid of
blood vessels, which would interfere with transparency. At the same
time, it is so firm that the diffusion of liquids through it is much im-
peded. Its living cells, the corneal corpuscles, therefore join hands by
means of long, delicate threads of living protoplasm along which nutri-
ments and wastes may be transported to and from the blood vessels
surrounding the margin of the cornea. The avascularity of the cornea,
and evaporation from its surface, make it several degrees cooler than the
body as a whole, and the metabolism of the corneal cells is adjusted to
the lower temperature.

The change in the character of the tissue, as one passes from the sclera
into the cornea, is a gradual one and the wide region of transition noted
marks the limbus (rim) of the cornea. A flange of scleral substance, the
scleral roll, (Fig. 5, sr) overlaps the edge of the cornea on its inner sur-
face so that the illusion of the cornea being set in the sclera, like a watch-
crystal in its bezel, is created. The two portions of the fibrous tunic are
not actually at all easily separable, but the limbus is the weakest region

A TYPICAL VERTEBRATE EYE: THE HUMAN

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THE FIBROUS TUNIC 11

in the fibrous tunic. It is at the Umbus that an isolated eyeball will
rupture, if it is squeezed until it bursts.

The outer surface of the fibrous mass (substantia propria) of the
cornea is covered by a stratified epithelium which is much like that lining
the mouth, and lacks the dead, homy outer layers which are present on
the general epidermis of the body. This corneal epithelium (Fig. 4b, e;
Fig. 5, ce) is continuous, at the limbus, with the thicker and less regular
epithelium of the conjunctiva (Fig. 5, ec). The conjunctiva (Fig. 5, co)
represents head skin which at the margins of the upper and lower eyelids
is doubled back on itself up underneath them to form their linings, and
is continuous over the front of the eyeball, with which it is fused to form
the 'conjunctiva fixa' — the loose folds in the culs-de-sac up under the
lids being the 'conjunctiva libera'. The connective-tissue dermis of the
conjunctiva fixa can hardly be distinguished from the loose connective
tissue which clings to the sclera; but at any rate it stops at the limbus
and only the epidermis appears to continue over the cornea.

Actually the dermis belonging to the corneal-epithelium part of the
conjunctiva is represented by some of the outermost layers of the sub-
stantia propria — no one can say just how many, in the case of the human
eye. The very outermost layer, just beneath the epithelium, is devoid of
cells and stains a little differently. It is known as Bowman's membrane
(Fig. 4b, b) ; but it scarcely deserves recognition and in the lower animals
cannot ordinarily be made out at all as a distinct part of the substantia
propria.

The corneal epithelium is richly supplied with pain-sensory nerve end-
ings and apparently with no others, and is remarkable for the speed with
which it can grow to repair or replace itself if injured. There is some
reason to think that it is normally nourished from entirely outside the
body — from the tears, which contain appreciable amounts of nutrient
substances.

The inner surface of the cornea is lined by a thin pavement of cells
usually called the endothelium of the cornea. (It more properly deserves
to be considered a portion of the mesothelium of the anterior chamber,
however, since it is continuous with the anterior covering of the iris and
the term 'endothelium' is outmoded as applying to mesodermal epithelia
generally). Between the substantia propria and the mesothelium, and
secreted by the latter as its basement membrane, is the thin, homo-
geneous, elastic 'membrane of Descemet' (Fig. 4b, d).

12 A TYPICAL VERTEBRATE EYE: THE HUMAN

It needs to be made clear at this point that the adjective 'elastic',
wherever it is appUed to an ocular structure, means 'springy' rather than
'easily stretched' — thus Descemet's membrane, the lens capsule, the
zonule fibers and so forth are elastic in the sense of a celluloid strip,
not of a rubber cord.

The Intra-Ocular Fluids — The fibrous tunic is normally kept dis-
tended to the point of rigidity by the pressure of fluid secreted within
the eye. This fluid, the aqueous humor, is continuously produced at a
slow rate and drained out of the eyeball into the blood stream by a
complex arrangement which is so regulated that the intra-ocular pressure
remains roughly constant at about 25 millimeters of mercury. Half of
this internal pressure is created by the external pressure of the extra-
ocular muscles and if both these and the blood-vessels leading to the eye
are severed, the mtra-ocular pressure falls to about 10 millimeters of
mercury. Overproduction of aqueous humor or any chemical, mechan-
ical, or pathological upset in the drainage system will lead to a painful
rise in pressure, the condition being known as glaucoma. If the pressure
is unrelieved, it clouds the cornea and injures the retina, and the end
result is blindness.

The greater portion of the intra-ocular fluid, occupying the large
chamber in the back of the eye, is rendered gelatinous by the addition
to it of proteins secreted during development by the retina. This mass
of gelated aqueous is called the vitreous (= glassy) body, or vitreous
humor (Fig, 3; Fig. 5, r). It is relatively permanent and in the fully
grown eye it is fixed in amount, so that any portion of it which is lost
through a wound is replaced only by watery aqueous humor. It is mostly
to the unmodified aqueous, in the front of the eye, that fresh fluid is
constantly added; and it is with the liquid aqueous that the pressure-
regulatory drainage mechanism — the canal of Schlemm (Fig. 3; Fig 5,
sc) communicates in an indirect way.

So far as the human eye itself is concerned, there is no powerful
reason why the material which fills the chambers of the eye should be
of two kinds — liquid anteriorly and semi-solid posteriorly. But in the
forebears of the fishes, which invented the vertebrate eye, the material
near the cornea had to be kept fluid so that the lens could be readily
moved in accommodating the focus of the eye to different distances,
and the lens would have dropped back into the globe if there were
only liquid behind it. In the higher vertebrates, the lens is not changed

HUMORS; UVEAL TRACT 13

in position but only slightly altered in shape, and it is held firmly in
place by ligaments which the lower fishes lacked; but the differentiation
in consistency of the intra-ocular media has never been abandoned. This
is probably fortunate, as otherwise, in animals above the fishes, the evolu-
tion of a muscular iris and mobile pupil might have been inhibited.

The Uveal Tract — The layer of the eyeball wall next inside the fibrous
tunic, clinging closely to the sclera but swinging inward away from it at
the sclero-corneal junction, is the uveal tract or uvea. The part of the
uvea which is attached to the sclera is a thin, deeply pigmented layer
consisting mostly of blood vessels, with connective tissue binding them
into a membrane. It is called the chorioid coat (Fig. 3; Fig. 4a). The
pigmentation of the chorioid prevents internal reflections and keeps light
from getting through the wall of the eyeball indiscriminately, and the
rich vascularity of the tissue is concerned with the nutrition of the highly
metabolic retina.

Against the inner surface of the uveal tract, throughout its extent,
lies the retina (Fig. 3). Where it is in contact with the chorioid, the
retina is thick (pars optica) and is sensitive to light. The anterior por-
tions of the uveal tract are lined with a thin, insensitive continuation of
the retina (pars caeca), which thus really terminates at the rim of the
pupillary aperture.

The sensory part of the retina has the form of a cup whose lip, the
'ora terminalis' (Fig. 3; Fig. 5, oO, is an important landmark inside the
eyeball. From the ora forward, both retina and uvea are profoundly
modified. The chorioid, at that point, thickens and ceases to be so
heavily pigmented and vascularized. The thickened region forms, in a
sagittal section, a slender triangle with its narrow angle aimed pos-
teriorly to merge into the chorioid. This thickened zone of the uvea is
called the ciliary body (Figs. 3 and 5), and it is characterized by the
presence of many involuntary muscle fibers and, on its inner surface
anteriorly, a large number (70-80) of radially arranged fin-like struc-
tures, the ciliary processes. Each ciliary process (Fig. 3; Fig. 6c; Fig. 7g)
is essentially a fold of non-sensory retina covering both sides of a flat
sheet of small blood vessels. Retina and uvea thus intimately cooperate
to form the ciliary processes. The anterior part of the ciliary body which
bears them is termed the corona ciliaris. At the posterior ends of the
processes they diminish in height and fade down to the level of the val-
leys between them. This leaves, between the hind ends of the processes

14 A TYPICAL VERTEBRATE EYE: THE HUMAN

and the ora terminalis, a fairly smooth posterior region in the ciliary
body, called the orbiculus ciliaris (Fig. 3 ; Fig. 5, oc; Figs. 6c, 7g, cor, orb) .
Inasmuch as it is from the blind epithelial part of the retina covering
the ciliary body that the aqueous humor is given off, the ciliary processes
and the less conspicuous secondary folds between them are best inter-
preted as a device for greatly increasing the secretory surface for the

MiS

spca
spcv

Fig. 6 — Vascular structures of the human eye.

a, vascular plan of the eye, showing veins in black, arteries clear. Modified from Adler,
after Leber.

dcv- anterior ciliary vessels; cc- choriocapillaris; crv- central retinal vessels; c/- canal of
Schlemm; ey- episcleral vessels; Ipca- long posterior ciliary artery; mc- major circle of iris;
pcy- posterior conjunaival vessels; rca- recurrent chorioidal artery; rv- retinal vessels; spca-
short posterior ciliary artery; spcv- short posterior ciliary vein; yep- vessels of ciliary process;
y'l- vessels of iris; yns- vessels of optic nerve and sheath; yy, yy- vorticose veins.

b, surface view of portion of choriocapillaris from fundus, x 65. Redrawn from Salzmann.
The black spots mark the junaions, with the capillary net, of small connecting arteries and veins.

c, surface view, from inner side, of portion of ciliary body. After Franz.

c- cornea; ch- ciliary body; cor- corona ciliaris; cp- ciliary processes; /, /- minor folds; ;'- iris;
orh- orbiculus ciliaris; r- retina; s- sclera.

production of aqueous. This was probably not their primary function
when they were originally evolved, however, as will be seen later when
the method of accommodation in the reptiles is explained. Over the cili-
ary body, the blind pars ciliaris retinae consists of a double layer of tall
cells, the ciliary epithelium (Fig. 7g, ce, ce). The outermost of these
layers is pigmented and is a simple continuation of a similar pigmented
layer which, further posteriorly, lies between the chorioid and the sensory

THE UVEAL TRACT

a V abl pbl

Fig. 7 — The iris.

a, radial section of human iris, x 24. a- artery; at/- anterior border layer; c- crypt; «e- iris
epithelium (= pigmented posterior layer of iridic retina); ma- major circle (circular artery in
ciliary body); wj- minor circle (anastamosis of radial vessels); phi- posterior border layer
(= dilatator pupillee, = myoid lamina of anterior epithelial layer of iridic retina); pz.- pupil-
lary zone (remainder of iris constitutes ciliary zone); s- connective-tissue stroma; sm-
sphincter muscle; v- vein.

b, =the small rectangle in a, enlarged to show the heavily pigmented posterior epithelium
and the lightly pigmented 'spindle cells' of the anterior epithelial layer, whose muscular
portions merge into a sheet to form the dilatator. Partly after Salzmann.

c, a spindle cell from the anterior retinal layer of the iris of a rhesus monkey, showing the
epithelioid cell-body and the partial differentiation of the base of the cell into a muscle
fiber, which is shown in its contracted condition. Redrawn, modified, after Hotta. d, same
as c, relaxed, e, same as c, but stretched (as when sphincter contracts).

f, diagram of vascular plan of mammalian iris, showing veins in black, arteries clear.
cp- capillary plexus of pupillary zone (devoted particularly to the sphinaer muscle); Ipca,
Ipcd- long posterior ciliary arteries; ma- major circle; wi- minor circle.

g, diagram showing distribution of pigment (stippling) in the retinal portion of the iris, as
compared with that in the ciliary epithelium and in the region of the sensory retina.
ce, ce- ciliary epithelium; cor- corona ciliaris; cp- ciliary process; ie- iris epithelium; o- era
termmalis of sensory retma; orb- orbiculus ciliaris; pbl,sc- piosterior border layer ( = dila-
tator) and spindle cells; pe- pigment epithelium of sensory retina; s- sclera; sm- sphincter
muscle; sr- sensory retina; u, u- uvea.

16 A TYPICAL VERTEBRATE EYE: THE HUMAN

part of the retina throughout their extents. The innermost of the two
layers of the ciliary epithelium is unpigmented and is a forward con-
tinuation of the sensory retina, which drops sharply in thickness at the
ora terminalis (Fig. 3; Fig. 7g).

At the anterior end of the ciliary body the uveal tract bends sharply
inward, away from the fibrous tunic, to form the iris (Figs. 3, 5, and 7).
This structure is an opaque disc of tissue with a hole, the pupil, in its
center. It is not flat, but bulged slightly forward by the lens which lies
behind it, so that the iris forms a low truncated cone when seen in profile.
The periphery of the iris is anchored to the inner aspect of the limbus
corneas by a connective-tissue meshwork, this region being known as the
iris- or filtration-angle (Fig. 5, mt, fa). It is important that this crevice
between iris and cornea remain wide, and not be squeezed shut or
blocked by material of any kind. This would lead to glaucoma, for the
only important exit-pathway for excess fluid, the canal of Schlemm (Fig.
3; Fig. 5, sc), lies shallowly embedded in the fibrous tunic at the iris
angle, separated from the aqueous only by a thin layer of the meshwork
tissue.

In the iris, the uvea and retina are even more intimately associated
than in any part of the ciliary body. On the posterior surface of the iris
— that is, the surface directed toward the lens and the vitreous — the
relations of the pigmented and unpigmented layers of the double retinal
epithelium (here called the pars iridica retinae) are reversed; for here
it is the innermost or posterior layer, nearer the lens, which is pigmented.
The anterior or outer layer, toward the cornea, contains little or no pig-
ment (Fig. 7g). In blue eyes, the brown pigment of the retinal backing
of the iris is the only pigment the iris contains — the blue color of the iris
being caused by optical trickery similar to that which makes veins, con-
taining dark red blood, appear blue when seen through white skin. In
brown and black irides, there is more or less pigment also in the uveal
connective-tissue stroma of the iris (Fig. 5, is; Fig. 7a, s), which is much
like the chorioid in construction. Inasmuch as the usual color of the
mammalian iris is brown, and the human blue eye represents a failure to
develop stromal pigment, the blue eye may properly be considered an
abnormality — a developmental anomaly — despite its common occurrence.
This viewpoint is strengthened by the fact that blue eyes are recessive to
the darker colors in heredity. The reader is not advised, however, to
refer slightingly to the azure orbs of his inamorata! Perfect albinos
(which perhaps never occur in the human species) of course lack even

THE PUPIL 17

the retinal pigment, hence have pink irides owing to the easy visibihty
of the numerous blood vessels of the iris.

The Pupil — The function of the iris is to 'stop down' the lens (Fig. 2)
— to prevent the light coming in through the peripheral zone of the
cornea from passing through the edge of the lens and reaching the retina.
Only the central part of the lens is optically good, and within certain
limits the image on the retina will be sharper, the smaller the aperture
in the iris. At the same time, the image will be less bright with a smaller
pupil, and in a given illumination might not be intense enough to affect
the retina unless the pupil could be opened more widely. A wide dila-
tation of the pupil affects the illumination of the image more than its
area or the size of the visual field it subtends; but this increase in image
brightness entails a sacrifice of the clarity of the picture, owing to the
optical imperfection of the lens periphery which is brought into play.
The regulation of the size of the pupil, in sympathy with the vari-
ations in the sensitivity of the retina and the external illumination, is
accomplished by contractile elements in the iris. Some of these are full-
fledged involuntary muscle cells, indistinguishable from those of the
abdominal organs, and are organized into a ring-shaped 'sphincter
pupillje' embedded in the iris stroma and closely surrounding the pupil
{sm in Figs. 5, 7a, 7g). Contraction of this muscle reduces the diameter
of the pupillary circle, though of course there is an obvious minimum
below which it cannot be further reduced; so, a circular pupil like that of
man cannot be closed entirely. The antagonist of the sphincter is a com-
plex consisting of the elasticity of the tissue and the radial blood vessels
(Fig. 7f) of the iris (which are straightened out when the sphincter con-
tracts and which tend to return to an undulant resting shape) together
with the active contractility of the 'dilatator pupillae'. This latter (Fig.
7a, pbl; Fig. 7b-e) is not a true muscle, but a myoid lamina developed
from the anterior face of the pars iridica retinae : the sparsely pigmented
cells of the anterior layer of this epithelium have each a long spindle-
shaped portion containing contractile fibrillae and lying with its long axis
at right angles to that of the cell body, which is attached to the middle of
the spindle (Fig. 7b-e) . These spindles thus form a layer which appar-
ently lies alongside the anterior layer of epithelium (Fig. 7a, pbl) in the
pars iridica retinae, but is really a part of that epithelium (Fig. 7g) . The
spindles may even be fused with each other in a syncitial fashion, though
this point is uncertain. Their myofibrillae run radially in the iris, so that

18 A TYPICAL VERTEBRATE EYE: THE HUMAN

their contraction opens up the pupillary aperture, throwing the body of
the iris into concentric folds or contraction furrows. The dilatator, being
only a part of an epithelial layer, contains no nuclei and no blood vessels,
nor any connective tissue forming septa within it or a sheath outside it.
The sphincter shows all of these features, however.

Both sphincter and dilatator are derived embryologically from the
anterior layer of the double epithelial pars iridica retinae which is, em-
bryologically, the zone of the optic cup nearest its lip. The cells which
become sphincter muscle fibers separate completely from the epithelium
late in fetal life, and the epithelium exhibits a gap underneath them (Fig.
7a, g) ; but the dilatator cells remain permanently, so to say, in a half-
way stage of conversion from epithelium into muscle. As a rare anomaly
in man, even this development may fail and there may be no trace of a
dilatator, the pupil then remaining strongly contracted throughout life
('microcoria'). Wherever among the lower animals the dilatator is lack-
ing (the pupil then being opened by the elasticity of the iris tissue alone,
upon relaxation of the sphincter) the spindle cells of the anterior layer
of the pars iridica retinae remain wholly epithelial, like the cells of the
posterior layer, and fail to lose their pigmentation during development as
do the elements which produce dilatator fibers in other animals and man.

The sphincter and dilatator have very different nerve supplies from
the autonomic system, and respond very differently to pharmacological
agents and to substances which duplicate or imitate the natural chemical
intermediators between nerve and muscle. They are involved in a num-
ber of reflexes. The fundamental one is the contraction of the pupil to
protect the retina from dazzlement when the external illumination is
suddenly increased. As the retina adapts to the new illumination (by
reducing its sensitivity) the pupil slowly reopens. Other reflexes include
the 'consensual' contraction of the pupil of a covered eye when the other
eye is illuminated, its dilatation in emotional states or when the skin of
the neck is pinched, its contraction when the eyes converge and accommo-
date for nearby objects, etc. The last-mentioned of these reactions is not
a true reflex, but the result of co-innervation of the sphincter pupillae
and the muscles of accommodation, the common nerve also running
with that which supplies the convergence-muscle, the internal rectus. The
complexity of some of the pupil reflexes is only realized when an attempt
is made to analyze their neurological basis in cases where the reflexes
have been lost or altered, due to traumatic or pathological lesions in the
central nervous system.

THE LENS AND ZONULE 19

The Lens and Zonule — The crystalline lens is a glassy, cushion-
shaped body which lies behind the iris (Figs. 3 and 5). It is supported
from behind by the vitreous body and from the front, to some extent,
by the iris. The slightly conical form of the iris is entirely owed to the
light pressure of the lens against it. If the lens is removed, as in an oper-
ation for cataract, the iris thereafter hangs loosely and trembles when-
ever the eye moves.

The chief support of the lens is given by a great number of firm
threads which, like so many guy-ropes, run from the rim of the lens to
the ciliary body. Collectively, these threads form the suspensory liga-
ment or zonule of Zinn (Fig. 3; Fig. 5, ^/). Each zonule fiber arises from
the surface of the ciliary epithelium, runs forward between two adjacent
ciliary processes, and sweeps around toward the lens equator to fuse with
the capsule of the lens. The largest number of fibers insert on the an-
terior face of the lens near the equator, a rather smaller number on the
posterior face, also near the equator; and scattered fibers insert at the
equator everywhere between these anterior and posterior sheets of fibers
('anterior and posterior leaves of the zonule'). Some atypical fibers cross
each other between the zonule leaves, and others run from one ciliary
process to the next and do not join to the lens at all. A little behind
the posterior zonule leaf (which is bowed to fit its curvature) lies the
anterior membranous surface of the vitreous, which is joined to the pos-
terior lens capsule along a narrow ring (Egger's line; Fig. 5, el) but is
free of the posterior lens surface in its center, creating the fluid-filled
'retrolental space' (Fig. 3; Fig. 5, rs). Between the anterior hyaloid mem-
brane of the vitreous and the posterior leaf of the zonule is the flattened
annular 'canal of Petit'. Between the leaves of the zonule is the space
called the 'canal of Hannover' — though of course it is not a true canal
since the fibers in each leaf of the zonule do not form an intact mem-
brane, but rather a grille. Between the anterior leaf and the back of the
iris lies the posterior chamber sensu stricto (Fig. 5, pes), although the
term 'posterior chamber' is properly enough used to embrace collectively
all of the aqueous-filled spaces behind the iris.

Newly-formed aqueous, poured into the posterior chamber by the
ciliary epithelium, can get into the anterior chamber (between iris and
cornea) only by infiltrating between the zonule fibers and then passing
between lens and iris and through the pupil. If, in an inflammation of
the iris, the whole pupil margin adheres to the lens capsule, the aqueous

20 A TYPICAL VERTEBRATE EYE: THE HUMAN

accumulates in the posterior chamber and bulges the iris forward, this
being one of the many possible causes of glaucoma.

The body of the lens, released from its capsule in the fresh condition,
is a glutinous, almost inelastic mass which gives no hint of its true
histological structure. This is best disclosed by crushing a lens which has
been hardened in formalin or alcohol, when it is seen that the lens is
composed of innumerable layers, like the coats of an onion, each layer
in turn being made up of fine fibers. An individual lens fiber in a given
layer runs from an anterior point, near the axis of the lens, circumfer-
entially around to a point in the posterior half of the lens — again near
the axis. No fibers could each have both ends exactly on the lens axis,
or the lens would be greatly elongated, pointed anteriorly and poster-
iorly, and would then be quite unsuited to its optical function. Fibers
running in one radius or meridian of the lens meet fibers in the diamet-
rically opposite meridian, end-to-end, along radial planes called 'lens
sutures' (see Chapter 5, section A; Figs. 40, 41, pp. 110-1). These suture
planes necessarily branch more and more elaborately as the lens body
grows by the addition of new layers of fibers at its surface, in order to
accommodate the increase in number of fibers in each layer over the
smaller number in the next innermost, slightly older layer, A given lens
fiber tends to lie along the convex curvature of a fiber in the next inner-
most layer of fibers, and along the concave curvature of one in the next
outermost layer. Radial lamellae of fibers are thus built up so that the
lens, besides having an 'onion' aspect, can also be thought of as being
built like an orange with many hundreds of segments. Since the diameter
of a single fiber is quite constant, the number of fibers per layer in-
creases as the lens grows, and the number of radial lamellae perforce
increases from time to time so that a maximum can be counted at the sur-
face, fewer and fewer farther and farther in toward the center of the lens.

The lens is contained in an unbroken, homogeneous, elastic envelope,
the lens capsule. The capsule is not uniform in thickness everywhere but
has definite thickened zones at particular locations, whose importance
will be explained in connection with accommodation. Covering the an-
terior half of the lens, to and slightly beyond the equator, is a single
layer of cuboidal cells, the lens epithelium (Fig. 5, le). This layer lies
just beneath the capsule. It is of no importance optically, but is all-im-
portant for the growth of the lens. It is believed to secrete the capsule
or at least to be more efficient in this than the lens fibers which have
their sides against the posterior half of the capsule, for the anterior por-

THE LENS AND ZONULE 21

tion of the capsule is thicker than the posterior in most animals. This
is, however, open to interpretation as a positive adaptation rather than
a mere accident of difference in secretory capacity, for as will be seen
later, accommodation is facilitated by a thick anterior capsule but would
be indifferent toward an equally thick posterior capsule.

The lens epithelium is the source of all of the myriads of lens fibers
excepting a very small ball of them at the center of the lens, which are
formed directly from the posterior wall of the embryonic lens vesicle —
a bubble of tissue which forms as a pit in the skin of the head, from
which it closes off and pinches free to sink down into the optic cup. If
the lens epithelium could be isolated intact, it would be like a thin,
shallow bowl composed of tiny tiles. We must imagine this bowl to be
growing constantly by the multiplication of its tiles, with those at the
edge of the bowl elongating into rods which, as they get longer and
longer, each slide one end along the inner surface of the bowl toward
its center, the other end growing in the opposite direction and curving
toward a point in space above the center of the bowl. It is in this fashion
that each new layer of lens fibers is added over the preceding one (Figs.
40 and 41), by the conversion of the epithelial cells at the equator of
the lens into long, curved threads which are hexagonal in cross-section
so as to fit against one another without intervening space, just as do the
cells of the epithelium itself. Any given cell in the epithelium of a grow-
ing lens is thus moved steadily toward the lens equator by the mitotic
expansion of the epithelium, and, upon finding itself eventually at the
rim of the epithelial bowl, proceeds to convert itself into a lens fiber.

The lens is very prone to opacify, thus giving rise to 'cataract', in re-
sponse to any of a number of causes; but it is normally optically empty —
that is, completely transparent and with no obvious signs of its elab-
orate internal structure. With special lighting arrangements, as with the
ophthalmologist's slit-lamp, it is possible to see several concentric sur-
faces within the lens, analogous to growth-rings in a tree trunk. These
mark periods in life — the same in all of us — at which the optical density
of the new-forming lens fibers is changed abruptly to a lower value than
that of the previously formed layers of fibers. Thus the optical density of
the lens — its effectiveness in slowing the speed of light and hence its
focusing power — decreases in several distinct steps from center to sur-
face. In a given region, however, the density of the fibers and of '"he
scant fluid between them is so nearly identical that the surfaces of the

22 A TYPICAL VERTEBRATE EYE: THE HUMAN

fibers reflect no light and consequently are invisible in the living lens.
The fibrous structure of the lens simply disappears as does a glass bead
when dropped into a vial of oil of the same optical density as the glass.

(B) Optics and Accommodation

Refraction — The property of substances which is called their 'optical
density' has been alluded to above. The higher the optical density of a
material, the slower light is able to travel through it. Light travels fastest
through a vacuum and very nearly as fast through air, so that for prac-
tical purposes the speed of light in air is taken as the maximum. This
speed divided by the speed of light in a given substance gives a figure

°-°°' : i i i : ! i : :

\ .-mM

b ijiiiiin

\ ^ :::::::::

°%°o°°„°° %°i" ■■■■'■■ -Open ground
soldiers > vyheat :
open ground :::::::::

dspkremeft Q^ '. ': : ^°° ; -'o
:::::::: .\ o ° o '

\ o °

a l::!:::::

c ;:;;;;;;; \\°:

Fig. 8 — An analogy for the refractive bending of light rays by a glass plate (see text).

which is called the 'index of refraction' of that substance referred to air
as a standard.

The effect of the optical density of a substance is to produce a bend-
ing of a beam of light which enters that substance at an angle, having
previously traversed a substance of different optical density. The amount
of the bend in the light-beam will depend upon the difference in optical
density of the two substances and upon the angle at which the beam
approaches their interface. The direction of bending will depend upon
whether the second substance traversed has a higher or lower density,
or index of refraction, than the first.

This bending of light rays when they pass through boundary surfaces
is called 'refraction'. Its basis may be best understood if we use an old

REFRACTION 23

favorite analogy for our light-beam and our pair of optically different
substances. Suppose a platoon of soldiers to be marching over bare
ground toward the edge of a wheat-field, which is at an angle to their
line of march (Fig. 8). The ranks of soldiers now represent successive
wave-fronts in a light-beam, and their files represent the individual light
rays in the beam. Obviously the soldiers cannot march as fast through
the dense wheat as over open ground, so that the latter may represent
air, and the wheat-field a piece of glass of high optical density.

As the first soldiers in the front rank start into the wheat, they are
slowed up, but those at the other end of the front rank are still able to

A

A -0- -^

f

Fig. 9 — Step-by-step explanation of the focusing of parallel rays by a convex lens.

a, displacement of ray by tilted plane-parallel plate (compare Fig. 8). b, bending of ray
by prismatic plate, c, approximation of parallel rays without convergence, by pair of tilted
plane-parallel plates, d, convergence of parallel rays by pair of prismatic plates, e, inde-
pendent foci of pairs of parallel rays, through action of prisms placed base-to-base,
■f, coincidence of foci when slope of prism faces is decreased toward their bases, g, single
focus of all parallel rays, resulting when process in f is fully carried out, yielding a
smoothly-curved lens.

march rapidly since they have not yet reached the wheat (Fig. 8a).
Consequently the front rank is swung around as if hinged at one end,
and by the time the whole of the rank is in the wheat, it has taken a
new direction of march which is of course followed by each rank in the
whole platoon (Fig, 8b). Upon emerging from the wheat-field on
the other side (Fig. 8c), the process is reversed and the platoon's line
of march becomes parallel to its original one, displaced laterally a dis-
tance which depends upon the width of the wheat-field and the difficulty
of marching through it.

24 A TYPICAL VERTEBRATE EYE: THE HUMAN

If the soldiers had encountered the wheat head on instead of at an
angle, their line of march would not have been tilted. But their ranks
would have been closed up, and while moving through the wheat each
soldier would have been treading on the heels of the man in front of him.
Strictly speaking, this would be refraction also, for the same decrease in
wavelength occurs when the angle of incidence is other than 90° —
refraction is most accurately defined in terms not of any bending of
the light rays, but of their change in speed and wavelength. Thus it
actually takes place when light meets a surface at right angles; but since
no visible change then occurs, the existence of the phenomenon is more
or less ignored.

Substituting now our beam of light and piece of glass for the soldiers
and the wheat-field, we can understand why the angle at which the light
meets the glass is so important in determining the direction the beam
will take through the glass. If the angle be changed, the new direction
will change. If a perpendicular be drawn to the surface of the glass, then
the beam of light on entering the glass from air will be bent toward the
perpendicular; and upon escaping from the glass into air again it will be
bent away from a perpendicular at the point of escape, the two bends in
the beam being equal if the two surfaces of the glass are parallel.

Action of a Convex Lens — We are now ready to understand how a
lens brings rays of light to a focus (study Fig. 9) . If a beam of parallel
rays of light strikes a convex lens, each ray in the beam will make an
angle with a tangent to the lens at the point where the ray strikes it, and
the angle will vary with the distance of the ray from the central ray of
the beam, which we will suppose to pass through the center of curvature
of the lens surface. The farther a ray is from the axial (central) ray,
the greater the angle it makes with a radius of the lens at its point of
contact with the latter, and the greater the angle of bending, toward
the radius, through which it will be refracted by the glass of the lens
(Fig. 9g).

Thus, the outermost rays of the beam are bent the most, rays lying
closer and closer to the axial ray are bent less and less, and the axial
ray is not bent at all. All the rays thus converge beyond the lens and
if the shape of the lens surface is just right, they may be made to con-
verge at a single point. This point, or 'focus', will be at a fixed distance
from the lens, and that distance can be varied only in two possible ways
— by making the lens variable in curvature or by exchanging it for a

ACTION OF A CONVEX LENS 25

different one. About the only variable lenses in the world are those in
living vertebrate eyes.

A lens forms an 'image' of an object, the distance of the image from
the lens being fixed as long as the distance of the object from the lens
is constant. We can best grasp how the image is formed if we think of
it as being made up of a large number of points, each corresponding to
a point on the object (Fig. 10). The light reflected from each point on
the object — its two end-points, say, as in Figure 10 — travels in straight
lines away from that point in all possible directions unless the object
happens to have a mirror-like surface. We can be sure of this, for we
can walk around an object and see it, from any direction, by means of

I

^ / 1 \ ^ vl/

Fig. 10 — Formation of an image by a lens.

Of the rays emanating in all dirertions from each point on the objert, those intercepted by
the lens are brought to a focus, thus generating a point in the image. Each image-point lies
on the opposite side of the lens axis from the corresponding object point; hence the image
is inverted.

the light coming in that direction from the object to our eyes. All of the
rays from an object-point which happen to be intercepted by a lens are
brought to a point focus beyond the lens at a particular, fixed distance.
If the object-point lies below the axis of the lens, however, the light from
it will be focused at an image-point above the axis and vice versa.
Hence, when we consider all the image-points formed by the focusing
of all the light from each of the object-points, we understand how the
image is built up. We also see why it hangs in space at a fixed distance
from the lens, is smaller than the object, and is inverted. We can now
see the image if we catch it on a screen at the image-distance from the

26

A TYPICAL VERTEBRATE EYE: THE HUMAN

lens. If we move the screen toward or away from the lens the image will
immediately become blurred because the object-points will be represented
on the screen not by sharp image-points, but by patches of light of the
same shape as the lens ('blur' or 'confusion' circles, where the lens is
round) which overlap each other.

If the screen now remains stationary at the proper distance, and the
object moves toward or away from the lens, the image will focus behind
or in front of the screen (Fig. 11), and the picture on the latter will
again be composed of hazy blur circles. With the object in this new
position, its image can now be made to fall on the screen only if the lens
is shifted in position or altered in curvature. Both of these methods are
used, in different kinds of vertebrate eyes, to keep the image sharp on

Fig. 11 — Relation of objea-distance to image-distance. After Kahn.

Only the B is sharply imaged on the screen, on which the A and C are represented by blurs.
The sharp images of the A and C hang in space as shown, and can be placed on the station-
ary screen only by moving the lens, or by substituting another lens of different strength.

the retinal screen when the object varies in distance from the eye. These
adjustments comprise what is called 'accommodation'.

Refractive Errors of the Eye — In the human eye there are several
curved surfaces at which refraction takes place, the end result being the
production of an image on the retina. There is also an elaborate arrange-
ment for changing the curvature of one of these surfaces so that the
image can be moved slightly forward or backward in the eye. This
mechanism of accommodation comes into play when we shift our gaze
from a distant to a nearby object, or when we watch an object which is
moving toward or away from us. As an object approaches, its image
recedes behind the retina and must be pulled forward. As an object goes
away from us, its image moves forward into the vitreous and must be
pressed back onto the retina in order to be seen sharply. In many persons
the eyeball is abnormally short (Fig. 12, top diagrams), so that the

REFRACTIVE ERRORS OF THE EYE

27

accommodation process, unaided by convex spectacles, is inadequate to
pull the image forward onto the retina and the sharp picture lies behind
the eye (hypermetropia or far-sightedness). In others, the eyeball is ab-
normally elongated (Fig, 12, bottom diagrams) and the image lies so
far forward in the vitreous (except when the object is very close to the
eye) that concave spectacles are required to move the focus of the lens
backward and place the image on the retina (myopia or near-sightedness) .

Object At Great Distance; Object At Walking Distance: Object At Reading Distance

15

o o^

tr
H o

tr —

receptive (visual-cell) layer
rays focus behind eye

some accommodation

much accommodation

rays focus in receptive layer

rays focus in receptive layer

no accommodation

some accommodation

2 —

rays focus at inner surface
of receptive layer

rays focus at outer surface
of receptive layer

rays focus in receptive layer

no accommodation

little or no accommodation

9r

rays focus in front
receptive layer

rays
of t

rays still focus in front
of receptive layer

rays focus in receptive layer

Fig. 12 — Spherical refractive errors of the eye.

Shows the extent of accommodation required, and the location of the images, in hyper-
metropic or far-sighted eyes (top row), normal eyes (middle row), and myopic or near-
sighted eyes (bottom row).

A third refractive error to which the human eye is prone is 'astigmatism',
a condition in which the retinal image of a point is not a point but a
line, owing to one of the refracting surfaces (almost always the cornea)
being partly cylindrical as well as spherical in its curvature (Fig. 13).
This results in a blurring of objective lines running in certain directions.
The error is easily corrected, when it is regular as indeed it usually is,
by the appropriate counteracting cylindrical curvature formed on the

28 A TYPICAL VERTEBRATE EYE: THE HUMAN

spectacle lens. As we shall see later, all three of these conditions which
for the human eye are 'errors', are perfectly normal and desirable situ-
ations in the eyes of various vertebrates whose visual requirements differ
greatly from our own.

Fig. 13 — Astigmatism.

a, a square piece of normal cornea whose radius of curvature, r, is the same in all meridians,
images a point p as a point on the screen s. In any other position the screen would intercept
a blur-square.

b, a piece of cornea whose radius of curvature in one direction, /, exceeds its radius of
curvature in another direction, r, is said to be astigmatic. It images a point p as a line
(horizontal in this instance) ih on a screen s placed in its first focal plane, and also as a
line at right angles to the first (the linear vertical image iv) on a screen /' placed in its
second focal plane. The most compact image of p is the 'figure of least confusion', flc, on the
screen /; but this image is a blur-square — the point p is nowhere imaged as a point, as in a.

c, the same piece of astigmatic cornea as in b sharply images the horizontal limbs of a cross
on the screen s, places a blurred cross on the screen /, and sharply images the vertical limbs
of the cross on the screen s". The whole of the objea cannot be sharply imaged at any one
distance from the astigmatic refracting structure.

DIOPTRICS OF THE NORMAL EYE 29

Dioptrics of the Normal Eye — As light enters the eyeball it first
encounters the tissue of the cornea, then in succession the aqueous
humor, the lens, the vitreous humor and the transparent retina on whose
posterior, outer surface the sensory rod and cone cells lie. These trans-
parent structures and substances, exclusive of the retina, are known col-
lectively as the dioptric media. When a light ray comes through the air
into the cornea at one side of the latter's center, it is bent sharply toward
the antero-posterior axis of the eyeball. Upon leaving the cornea and
entering the aqueous humor, the ray is bent again but only very slightly
since the corneal tissue and the aqueous have nearly the same optical
density. The refractive index of the cornea is 1.376, and that of the
aqueous is 1.336, which is about the same as that of water.

Now upon entering the lens, the ray is bent further, again toward the
axis of the eye. The index of refraction of the lens can be taken as 1.42.
Actually, the values for the lens are 1.406 at the center, 1.386 at the
surface, but because of its zoned structure the lens behaves as would a
homogenous body whose index was actually higher than that of any part
of the lens. This figure, 1.42, for the effective index of the lens, does
not exceed the index of the aqueous (1.336) by as much as the latter
value exceeds the index of air (l.OO). This, together with the fact that
the anterior surface of the lens is not as sharply curved as the cornea,
is responsible for the fact — often overlooked — that the cornea does most
of the job of placing the image on the retina. In the optically normal
eye the lens acts like the fine adjustment of a microscope — it adjusts the
position of the image only in a minor way. Some highly myopic persons,
in fact, see clearly without spectacles after the lens has been removed
because of cataract — with the lens in the eye, they have too much focus-
ing power, the focal length of the cornea alone being equal to the
length of their abnormally elongated eyeballs.

Upon travelling through the posterior surface of the lens into the
vitreous humor, our light ray for the first time passes from a medium
of higher density into one of lower density — the vitreous having the
same index as the aqueous. If it were passing through a convex surface,
it would be bent away from the axis of the eye; but since it is here
travelling through a concave surface it is still further converged toward
the axis. In fact, since both surfaces of the lens are in contact with media
whose refractive indices are the same, and the posterior surface of the
lens is more sharply curved than the anterior, the posterior face is the
more important of the two in the static refraction of the eye.

30 A TYPICAL VERTEBRATE EYE: THE HUMAN

The ray now travels to the retina, having crossed the optic axis of the
eye so that it strikes the retina on the opposite side of the axis to the
one on which it entered the cornea. The retinal image of an object is
consequently inverted and much smaller than the object, as is true of
the image of any simple convex lens, as we have seen. The refractive
index of the human retinal tissue, which in life is optically empty, is not
known; but it may be of considerable importance in connection with the
physiology of the fovea (Chapter 8, Section C) . There are indications
that it is higher than that of the vitreous and may approach that of the lens.

It should be borne in mind that it is the difference in refractive index
on the two sides of a boundary surface which, together with the sharp-
ness of curvature of that surface and the direction of curvature (whether
convex or concave), determines the extent of convergence or divergence
of light rays passing through it. The absolute values of the refractive
indices are of no consequence. Hence since the anterior surface of the
cornea is an interface between two very different media (air and tissue)
it is the most important refractive surface in the dioptric media. The
posterior surface of the lens is next in importance, the anterior surface
of the lens least effective (when the eye is not accommodating), and
the posterior surface of the cornea can be ignored entirely.

It is the anterior surface of the lens, however, which in the human eye
is alone modified in curvature in the act of accommodation — hence for
this process, that surface is of paramount importance. We are now pre-
pared to examine the mechanism by which human accommodation is
accomplished.

Accommodation — In the first place the reason for accommodation,
and the extent of the process, need to be clearly understood. The curva-
tures of the refractive surfaces of the ideal human eye and the refractive
indices of ordinary air and of the dioptric media are such that when the
eye is at rest — that is, exercising no muscular effort to accommodate
for nearby objects — objects at the horizon are in focus upon the
back surface of the transparent retina. The seeing-cells, the rods and
cones, stand on this surface like the bristles of a brush. Their length is
appreciable, and since a light ray which helps to form the image strikes
the retina perpendicular to its surface and thus passes axially through a
visual cell, it follows that the optical image may lie anywhere along the
length of the visual elements and still form the same photochemical
image, and be as sharply 'seen' in the form of a cerebral or mental image.

ACCOMMODATION

31

There is thus a certain leeway which the focus of the optical image
may have without its becoming blurred in the consciousness. This lee-
way is in fact so great that without any change in the dioptric structures
of the eye, an object can approach from the horizon to a distance of
about twenty feet* without its image moving back far enough to get out
of the visual-cell layer and into the insensitive chorioid. The image in
the eye is so very small compared with the object that since the move-
ment of the image, either laterally or forward and backward, is minified
to a high degree, the movements of the image over the surface of the
retina (especially through its thickness) are almost microscopic. Conse-

Fig. 14 — The mechanism of human accommodation.

The left half of the diagram shows the structures in relaxation. The thickness of the lens
capsule has been exaggerated one hundred times to bring out its local variations. On the
right, accommodation; by reference to the angular scales, the movements of the various parts
can be discerned. Note that the contraction of both the radial and circumferential portions
of the ciliary muscle has stretched forward the smooth orbicular region of the ciliary body
(to which most of the zonule fibers attach) and has bunched up the coronal region (bearing
the ciliary processes, whose profiles are indicated by the dotted lines). The relaxation of the
zonule fibers has permitted the elastic lens capsule to mold a bulge of sharpened curvature
on the anterior surface of the lens. Note also that the sphinrter muscle of the iris has
contracted, closing down the pupil in its 'accommodation reflex'.

quently, the object may recede from twenty feet to infinity without its
image coming forward more than the length of the rods and cones —
a small fraction of a millimeter (see Fig. 19, p. 43).

Within twenty feet, however, the refracting power of the media must
somehow be increased to keep the image in the visual-cell layer of the
retina. In the human, the anterior surface of the lens is sharpened in

*It is really a bit more, but so variable that for the didactic purposes of this book, twenty
feet is arbitrarily taken as standard.

32 A TYPICAL VERTEBRATE EYE: THE HUMAN

curvature to accomplish this (Fig. 14), and the structures most involved
are the lens capsule, the zonule fibers, and the muscle cells in the ciliary
body. The latter must contract to focus the eye for nearby objects, relax
partially for more distant objects up to twenty feet away, and relax com-
pletely for objects beyond twenty feet. This is why it is restful to the
eyes to gaze out of a window at distant objects for a few moments
occasionally, when doing close work of any kind.

The ciliary muscle fibers are formed into two muscles which blend
with each other and are really only one, since one mass of fibers is de-
rived from the other in the embryo and the two masses have a common
nerve supply and act together, having the same effect upon accommo-
dation in spite of their great difference in orientation within the ciliary
body.

The 'radial' or 'meridional' fibers, as seen in a sagittal section of the
eye, are arranged fanwise, the small end of the mass being fastened
at the scleral roll and the other end being frayed out and distributed
along the whole ciliary body, most of the fibers ending along its inner
surface (Fig. 3; Fig. 5, mb). When this radial muscle (of Briicke) con-
tracts, the effect is a stretching of the flat orbiculus region of the ciliary
body so that its anterior border moves forward — the ora terminalis being
fixed. The corona ciliaris, that portion of the ciliary body bearing the
ciliary processes, is telescoped, its posterior border moving forward but its
anterior attachment at the iris angle remaining fixed. The result of this
forward movement of the region of junction between corona and orb-
iculus is a relaxation of the taut guy-wires of the lens, the zonule fibers.
These are normally in a state of considerable tension when the ciliary
muscle is not contracted; for, as the eyeball grows, before and after
birth, its diameter increases proportionately faster than that of the lens.
Hence the suspensory-ligament fibers, once they have grown out from
the ciliary epithelium and attained connection with the young lens cap-
sule, are placed under constantly increasing lengthwise stress which is
not entirely removed by any compensatory increase in length on their
part. This brings about a slow broadening and flattening of the growing
lens and a permanent state of tension in the suspensory ligament, which
can be relieved only by the contraction of the ciliary muscle.

A portion of the ciliary muscle fibers, the number being often greater
in far-sighted eyes and less in near-sighted ones (where they may even
be entirely lacking) are organized into a ring-like muscle (of Mixller),
analogous to the sphincter pupillae. Although the fibers in Miiller's muscle

ACCOMMODATION 33

(Fig. 5, mm) are thus at right angles to those of the radial (Briicke's)
muscle, the two muscle masses are in no way antagonistic in their action
as are the sphincter and dilatator pupillae. The contraction of Miiller's
muscle heaves the ciliary processes inward toward the axis of the eyeball
and thus substantially supplements the action of Briicke's muscle in
letting up the tension in the zonule fibers. In fact, the muscle of Miiller
is much the more efficient of the two, since no component of its direction
of contraction is wasted in uselessly pulling any part of the ciliary body
forward in the eye. It is only the inward component of the action of the
diagonally-placed Briicke's muscle which is very useful. It is significant
that in far-sighted (hypermetropic) eyes, which must constantly make
extra accommodatory effort (Fig. 12), it is Miiller's muscle — not
Brucke's — which becomes hypertrophied if spectacles are not worn.

To understand what happens to the lens when the zonule is relaxed,
we must recall the nature of the lens capsule and consider its structure
in a little more detail. The capsule is a firm, elastic membrane. If a
cut is made in it, the edges of the cut will tend to roll outward — thus
it is clear that the capsule is normally exerting pressure on the lens
fibers. If the capsule were equally thick throughout and the lens fibers
were plastic enough, the elasticity of the capsule would tend to mold
the lens into a ball if the flattening effect of the tensed zonule fibers
were to be eliminated by cutting them.

Actually, however, the capsule varies greatly in thickness in different
parts and consequently varies locally in the force which its elasticity can
exert upon the lens capsule (Fig. 14). Fincham, who has revised and
modernized the F^elmholtz theory of human accommodation, has care-
fully studied the properties of the capsule and of the decapsulated lens.
Without its capsule, the body of the lens slowly takes on the flattened
form characteristic of the intact lens in situ in the resting eye. Hence
the bulged form of the lens in accommodation is brought about by the
capsule's assertion, upon it, of a molding force more than strong enough
to overcome the tendency of the lens body to flatten. Cutting the zonule
fibers allows the capsule to mold the lens into the same shape it has in
accommodation. The relaxation of the ciliary muscle allows the tensed
zonule fibers to effect a 'physiological decapsulation' of the lens, by pulling
so hard upon the equator of the capsule that the latter 's elasticity is ren-
dered ineffectual, and the lens body assumes the same flattened form
which it takes when removed from its capsule. The contraction of the
ciliary muscle, on the other hand, eliminates the pull of the zonule fibers

34 A TYPICAL VERTEBRATE EYE: THE HUMAN

just as if the latter had been severed and the lens entirely isolated. We
may express these antagonisms and cooperations as a series of equations :

Lens - capsule = lens in situ + relaxed ciliary muscles (no accom.) ;

Lens + capsule - zonule = lens in situ + contracted ciliary muscles;

Lens + capsule - accommodation = lens - capsule;

Lens + capsule + zonule + accommodation = lens + capsule — zonule;
and so on.

The thinnest portion of the lens capsule is a large central area of its
posterior part. This is surrounded by a greatly thickened band which
lies fairly close to the equator. The equatorial region itself is again thin.
On the anterior surface is another thickened zone which lies a little
farther from the equator than the posterior thickening and leaves a
smaller thin central area than occurs on the posterior capsule. This
central thin area of the anterior capsule is also slightly thicker than the
posterior central thin area (Fig. 14).

Ordinarily all of the light used for vision passes only through the
anterior and posterior central thinnings of the capsule — the pupil does
not dilate widely enough to expose the periphery of the lens to incoming
light. The posterior surface of the lens fits the vitreous body so closely,
with incompressible fluid in the retrolental space between the two, that
it cannot change its curvature materially during accommodation. The
anterior leaf of the zonule is probably relaxed more completely than the
weaker posterior leaf at a given stage of accommodation, and the net
result is that only the anterior lens surface is free to deform when the
zonule is relaxed by the contraction of the ciUary muscles. The anterior
zone of thickening in the capsule then proceeds to reduce its diameter
and is stiff enough to force the thin central area of the capsule to form
a bulge, into which the body of the lens is molded. This sharpening of
the curvature of the useful portion of the anterior lens surface increases
the refracting power of the eye and holds the image forward on the
retina in spite of the approach of the object within the 'commencement
point' of accommodation — that is, within the critical twenty-foot distance.

The amount of accommodation which is being exerted at any one
time, and the total amount of which the individual is capable, can be
conveniently expressed in the same units used for designating the focus-
ing power of a lens. The unit in question — the diopter — is not really a
unit at all, for it has a sliding value. The strength of a lens in diopters
is the reciprocal of its focal length in meters. That is, a one-diopter lens
focuses parallel rays at a point one meter away, and a two-diopter lens

ACCOMMODATION 35

focuses at one-half meter, a five diopter lens at one-fifth of a meter, and
so on. The emmetropic eye (Fig. 12, middle row of diagrams) focuses
parallel rays on its receptive layer when it is not accommodating. If now
a one-diopter lens is added, like a spectacle, in front of the relaxed eye,
an object one meter away will be imaged on the retina. A four-diopter
spectacle will enable the non-accommodating eye to image sharply an
object only a quarter of a meter distant. So, we may say that the amount
of accommodation being exerted by an emmetropic eye is four diopters
when, without a spectacle, it images an object at one-fourth of a meter.

-near point at 2

near point at reading distance
^near point at arnn's length
^^^^^^^j-near point at 13'

50 60 70

Age In Years

Fig. 15- — Decrease of human accommodation with age, owing to the progressive hardening
of the body of the lens. Plotted from data of Donders on emmetropic subjects.

By accommodating to a certain extent — four diopters' worth — the focus-
ing power of the crystalline lens has been increased by four diopters over
its strength when at rest; for, this amount of accommodation can take
the place of a four-diopter spectacle placed before the non-accommo-
dating eye.

The range of accommodation — that is, the greatest increase in the
focusing power of the lens — which a person can produce is unfortunately
not a fixed quantity (Fig. 15). Almost as inevitable as death and taxes
is a decrease in that range, with age, to such an extent that the indi-
vidual (unless substantially myopic to begin with) becomes unable to

36 A TYPICAL VERTEBRATE EYE: THE HUMAN

image objects as close as one holds a book to read, and must adopt
spectacles whether he has ever needed them before or not. This phenom-
enon is called presbyopia (literally, old sight), and most of us enter
its realm sometime in our forties. The decrease in accommodating
power is not caused by any weakening of the ciliary muscle, but by a
perfectly normal, progressive hardening of the lens. The ciliary muscle
tries as hard as ever in the presbyopic years — but its force, be it remem-
bered, is not the one which molds the lens. The actual molding force,
the elasticity of the lens capsule, is really quite weak at best, and becomes
wholly inadequate to its task when the body of the lens reaches a certain
stage of firmness. The hardening of the lens is so gradual, however, that
few of us live so long that our graph of the process (Fig. 15) reaches the
line of zero accommodation. When this does happen, the once emme-
tropic eye is still emmetropic — still focuses parallel rays upon its retina;
but its 'near point' (the nearest point at which an object can be sharply
imaged) has moved away from the eye until it is twenty feet away, at the
point where the eye formerly commenced to accommodate for approach-
ing objects.

(C) The Ocular Adnexa

The major anatomical structures which fall under the above heading
are the oculomotor muscles, the lids, and the lacrimal apparatus.

The eyeball lies, cushioned by fat, in a pyramidal cavity in the skull,
the bony orbit. The angle at the apex of the orbit is about 45°, and the
center-lines of the two orbits also make an angle of about 45 . This
brings the mesial walls of the orbits approximately parallel; but for the
axes of the eyeballs to be parallel it is necessary for them to make 22^/2
angles with the axes of the orbits.

The Oculomotor Muscles — Back at the apex of the orbit is the small
aperture by which the optic nerve enters the skull, and close to this
point are the origins of four of the six muscles which rotate the eyeball
(Fig. 16). These are the straight muscles or 'recti'^ — superior, inferior,
medial (internal, nasal) and lateral (external, temporal). They form
the 'muscle cone' around the nerve and diverge toward the equator of
the eyeball. Here they pass through the connective-tissue capsule (of
Tenon) which forms a jacket over the sclera, loosely connected to the
episcleral tissue, and which is a portion of an elaborate system of con-
nective-tissue membranes or fascia in the orbit, one of whose fortunate

THE OCULOMOTOR MUSCLES 37

functions is to bar conjunctival infections from the orbit where they
might do great damage to the eye and the brain.

Becoming tendinous on passing through Tenon's capsule, the inser-
tions of the muscles fuse with the tissue of the sclera. Since the fascial
sheaths of the muscles are continuous with Tenon's capsule, it is possible
to dissect a diseased eye out of the capsule, and by sewing a ball into
the latter, provide a stump for an artificial eye which will move in har-
mony with the good eye of the other side.

Fig. 16 — Oculomotor muscles of man, as seen from above in a dissected head.

On the left, a portion of the superior oblique has been cut away to reveal the inferior
oblique; on the right, the superior rectus has been removed to permit a view of the inferior
rectus. Modified from Adler.

io- inferior oblique; ir- inferior rectus; /r- lateral (external) reaus; mr- medial (internal)
rectus; n- optic nerve; p- pulley through which tendon of superior oblique passes; so- tendin-
ous portion of superior oblique; sr- superior rectus.

Two Other muscles (Figs. 16 and 17) meet the superior and inferior
surfaces of the eyeball obliquely from the nasal side of the anterior part
of the orbit, where one of them, the 'inferior oblique' muscle, is attached.
The other, 'superior oblique', has however greatly lengthened phylogen-
etically and its origin has moved back toward that of the recti. Its side-
wise attack upon the eyeball was preserved throughout the backward
migration of its origin by the development of a tough ring or pulley,
through which it passes. The pulley formed at the old sub-mammalian
site of attachment of the muscle on the anterior nasal orbital wall. As
an anomaly, the muscle may atavistically end here, or a normal superior

38 A TYPICAL VERTEBRATE EYE: THE HUMAN

oblique may be accompanied between the eyeball and the pulley by an
extra muscular slip which has a common insertion with it upon the eye-
ball. An additional and interesting atavism in an occasional human is a
'retractor bulbi' muscle, which in other mammals serves to hold the eye-
ball tightly back in the orbit regardless of the relaxations and contrac-
tions of the eye-rotating muscles. It ordinarily has four parts in mammals,
alternating with the recti and originating with them at the apex of the
orbit. The anomalous human retractor bulbi may exhibit this complete
arrangement. The two oblique muscles, approaching the eyeball from the
nasal side, might seem to give the muscular apparatus extra power for
converging the two eyes — convergent movements being more frequent
than any others — but since they do not pass in front of the center of
rotation of the eye, their chief actions are to tilt the eyeball upward and
downward. Their original purpose was, however, very different (p. 303).
The six normal muscles are supplied by three different cranial nerves,
one of which cares for four of them. Their bilaterally cooperative actions
and the elaborate central-nervous control thereof are beyond the scope
of this elementary description.

The Lids — The eyelids are essentially folds of skin, which were devel-
oped by land animals primarily for cleaning and moistening the cornea,
and which incidentally protect the eye from small foreign objects such
as insects, wind-blown sand, and the like. The cornea of an aquatic
animal is kept clean and succulent by the water itself, through which
no natural particle can travel with sufficient velocity to injure or embed
in the cornea. It is a mistake to suppose that the chief purpose of the
lids is to protect the eye — from blows, and so on; for they are no real
protection against such insults. That function, in man, is taken care of
by the supraorbital ridges of the skull which overhang the orbits and
bear the eyebrows, whose purpose appears to be to divert sweat from
the eyes.

The opening between the lids, which reveals a portion of the eyeball,
is the 'palpebral fissure'. Its temporal and nasal angles are respectively
the (sharper) outer and (broader) inner 'canthi'. In the inner canthus
can be seen the plica semilunaris, a crescentic fold of conjunctiva which
is a vestige of a third, sidewise-sweeping eyelid present in many animals,
the nictitating membrane. Neither the special muscles nor the special
gland (Harder's) of the third eyelid are present, even as vestiges, in
man. Overlying the base of the plica is a pink mass, the caruncle, which
is really a bit of the margin of the lower lid which becomes isolated

THE LIDS

39

• r C S " « S-2

-c 2 ^ v2i c c a,
i2 0-5 i.£-§ a3

M-5-

> 'C '

40 A TYPICAL VERTEBRATE EYE: THE HUMAN

therefrom in the embryo and sometimes bears eyelashes and their assoc-
iated glands as evidence of its true nature.

Near the inner canthus on each Ud margin is a pore raised on an
eminence. These 'punctae lacrimaha' are exits for the tear fluid which
accumulates in a pool, the lacus lacrimalis, at the inner canthus.

The human upper lid (Fig. 18) does most of the work in closing the
eye, though in most vertebrates it is the lower which moves the more.
A continuous sphincter muscle surrounds the palpebral fissure and is
much flattened and very broad where it courses through the two lids
between their outer dermal and inner conjunctival surfaces. The oppo-
nents of this 'orbicularis oculi' muscle are thin muscles running down
into the upper lid and up into the lower. The more important of these
is the levator muscle of the upper lid, which works with the superior
rectus of which it is a derivative. Thus, when the eyeball is turned up-
ward the lid automatically rises. When the levator is paralyzed, as
sometimes occurs in diseases of the nervous system, the individual has
a sleepy look owing to the unsightly drooping of the lid; but the oph-
thalmic surgeon cleverly corrects this by fastening the inside of the lid
to the superior rectus itself.

Between the muscle-sheets of the lids and their conjunctival linings
lie firm plates, one in each lid — the tarsi. Each tarsus is composed of
dense connective tissue and is curved to fit the surface of the eyeball.
Their presence insures a smooth sliding of the lids and obviates any
tendency of the latter to roll up when in action. Embedded in each
tarsus is a row of elongated (Meibomian) glands which open by a series
of apertures behind the lid margin. They represent an additional row of
eyelashes which have disappeared in evolution, leaving their glands
behind them. The sebaceous secretion of these, together with that of
smaller glands (of Zeis) associated with the lashes which are scattered
along the edges of the lids, maintains a film of oily emulsion over the
layer of tear fluid and holds the latter firmly and smoothly against the
eyeball. The tears can spill over onto the cheeks only when they so
accumulate that their weight breaks the retaining film.

The periodic blinking of the lids is ordinarily involuntary and un-
conscious. The rate of blinking varies, but each blink occupies %o of a
second. Its chief values are in moistening and cleaning the cornea and
in pumping the tear fluid out of the lacus lacrimalis — though this is an
incidental function of the lid muscles rather than of the lids themselves.
One might expect the drying of the cornea to initiate the blinking reflex,

THE LACRIMAL SYSTEM 41

but numerous experiments have shown that this is not the case. Though
many factors have been tested for their effect or lack of effect upon the
acceleration or inhibition of the rhythmical blinking of the lids, the im-
mediate cause of it remains quite unknown.

The Lacrimal System — The tear fluid, which can be thought of as
the land animal's substitute for an ocean, is produced continuously in
small amounts (less than 1 cc. per day in the absence of irritation) by
the lacrimal gland. This compound tubular gland lies against the su-
perior temporal quadrant of the eyeball in the anterior part of the orbit,
propped forward by the orbital fat (Fig. 17). Its dozen ducts open
mostly far up under the upper lid. Like the lids themselves, the entire
lacrimal apparatus is lacking in fishes, where it is not needed, and is
much reduced in those aquatic forms which have had terrestrial ancestry.
The tears are mixed with mucus secreted by scattered cells in the con-
junctiva, and most of this fluid is disposed of by evaporation. Any
excess, upon irritation of the eye or in mild emotional states, drains
through the two punctae — chiefly the lower — into a pair of canaliculi
which converge and enter the 'lacrimal sac'. This is a dilatation of the
upper end of the lacrimal duct, a membranous canal which runs vertically
downward, through the bony substance of the skull, to empty into the
nasal cavity. This connection leads to our being able to taste the salty
tears in the back of the mouth when we weep. There are a number of
so-called valves in the tear-drainage system, and its action is rather com-
plicated; but the essential factor in emptying the lacus is a pumping
action by the orbicularis oculi upon the adjacent lacrimal sac. This
makes it possible to conceal emotion and sometimes to forestall weeping
(the spilling of excessive tear fluid onto the cheeks) by rapid blinking.
The primary use of the tears is to clean and wet the cornea. Their
overproduction upon irritation is often entirely effective in washing away
the source of irritation. The fluid contains enough sugar and protein
to be of value in the nutrition of the corneal epithelium, which is able
to absorb proteins. There is some evidence that it is the sole source of
that nutrition. Moreover, the tears are bactericidal to a not unimportant
extent due to the presence in them of a special antiseptic ferment, 'lyso-
zyme'. The most conspicuous thing about the lacrimal system, however,
— psychical (emotional) weeping — is strictly peculiar to the human
animal and to some species of bears, and serves no physiological pur-
pose whatever. It§ value is wholly psychological and economic — as every
woman knows!

Chapter 3

THE VERTEBRATE RETINA

(A) Histology and Physiology

The sensory retina of any vertebrate consists essentially of four layers
of cells. One of these, the pigment epithelium, is not immediately con-
cerned with the process of photoreception. The other three layers com-
prise the retina proper, which lies against the pigment epithelium but is
rarely connected with the latter by any continuity of material.

The Pigment Epithelium — The pigment epithelium of the retina
(Fig. 19) is firmly joined to the inner surface of the chorioid coat.
Each cell in the epithelium is like a six-sided tile and the cells are set
in a regular mosaic with only a thin layer of cement between their
contiguous sides. The base of the cell, toward the chorioid, is also
covered by cement which the cell secretes, so that an unbroken layer
of this cement lies between the pigment epithelium and the chorioid.
The innermost layer of the chorioid is an extremely thin elastic sheet
which, together with the cuticular cement layer between it and the bodies
of the pigment cells, comprises the 'glass membrane' (lamina vitrea).
The whole of the thickness of this really double membrane is often
assigned to the chorioid — or, by some, even to the pigment epithelium,
which clings much more tightly to the chorioid than to the retina proper
when an attempt is made to peel the layers of the eyeball wall apart.
The pigment epithelium belongs to the retina physiologically and embry-
ologically, however, if not anatomically. It is nowhere continuous with
the chorioid, whereas, as we have seen (see Fig. 7g, p. 15) it is contin-
uous at the pupil margin with the anterior prolongation of the sensory
retina.

The free surface of the pigment cell usually bears a number of pro-
cesses which may be few and heavy (even single) or numerous and
filamentous, like a tuft of microscopic hairs (Fig. 20). The granules of
pigment, which consist of a colorless matrix impregnated with a light
brown form of melanin called 'fuscin', are of two sorts — round ones
tending to occupy the cuboidal base of the cell around the nucleus, and
spindle-shaped ones filling the processes and often migrating in and out

42

THE PIGMENT EPITHELIUM

43

of the latter in bright and dim Hght. Pigment may be entirely lacking
over a large area of the epithelium where this lies against an especially
modified area of chorioid (Chapter 9, section D).

* lamina vllrea
** pigment epithelium

receptor layei

'" >c»>v^ "^^m." ^-extllmrmem^.^
^ '^^J^ outernuclear

•^^'i^- ^'\'^"

X'-^-lJ' \ outer plexi-
!*?V rr *^ ^1 form layer

'i^^c\^^'^li T

^r«4^ ^^^■^m.'nner nuclear

inner plexi-
form layer

L^

) ganglion layer ^

nerve fibers

■^'iRtrllmrmemb:

Fig. 19 — The human retina.

At the left, a vertical seaion through the retina in the nasal fundus, as it appears in ordin-
ary histological preparations (fixation in Kolmer's fluid; nitrocellulose embedding; Mallory's
triple stain, Heidenhain's hematoxylin and phloxine). x 500. (Note cross-section of capillary
in inner nuclear layer).

At the right, a 'wiring diagram' of the retina showing examples of its principal elements,
as revealed in material impregnated with silver by the methods of Golgi. Based largely upon
the work of Polyak.

a- amacrine cell (diffuse type); b,b- bipolar cells (ordinary, 'midget' type); c,c- cones;
cb- 'centrifugal' bipolar, believed by Polyak to conduct outward through the retina rather
than inward; db- diffuse bipolar, connecting with many visual cells — chiefly rods; g, g-
ganglion cells (ordinary, 'midget' type); h- horizontal cell — its dendrites connecting only
with cones and its axon with both rods and cones at some distance from the cell-body;
m- Miiller fiber — its ends forming the limiting membranes and its substance serving to
insulate the nervous elements from each other except at synapses; pg- 'parasol' ganglion
cell (one of several giant types, conneaing with many bipolars) ; r, r- rods.

THE VERTEBRATE RETINA

Anterior to the ora terminalis the pigment epithelium passes over the
cihary body as the outermost of the two layers of the ciliary epithelium
and is almost unchanged except for an increase in the height of its
cells and the disappearance of all processes together with the spindle
form of pigment granule. Its continuation on the back of the iris is

Fig. 20 — Pigment-epithelial cells, x 500.

The horizontal line beneath each drawing shows the position of the external limiting mem-
brane. A portion of the lamina vitrea is shown as a heavy black line. Spaces occupied by
cones are marked c; those filled by rods are marked r.

a, group of cells from an unstained, flat mount of human pigment epithelium, as seen from
the chorioid side. Through the clearings formed by the nuclei, some of the elongated pig-
ment granules in the distal part of the cell can be seen.

b, two human pigment cells from the nasal periphery, in vertical sertion. One cell is opposite
a cone, and bears a delicate tubular process which ensheathes the cone outer segment {cf.
Fig. 19). The other cell is opposite only rods, and is devoid of processes.

c, pigment cell of a mouse opossum, Marmosa mexicana, showing the paucity of retinal
pigment charaaeristic of many strongly nocturnal animals.

d, pigment cell of an African lungfish, Protopterus eethiopicus, showing a mass of fila-
mentous pigment-laden processes markedly differentiated from the body of the cell.

e, pigment cell of goldfish, Carassius auratus, light-adapted. The two or three heavy proc-
esses contain relatively little migratory pigment (in rod-like granules) in their tips {cf. Fig.
62, p. 146; Fig. 94, p. 237).

almost devoid of pigment in those animals in which it has produced
a dilatator pupillas (Fig. 7, p. 15). At the edge of the pupil the layer of
cells doubles back upon itself and continues, now heavily pigmented, to
the periphery of the iris as the latter's most posterior layer of tissue.
There its pigmentation disappears and a clear epithelium proceeds over

THE VISUAL CELL-LAYER 45

the ciliary body, as the innemiost of the two layers of the ciliary epi-
thelium, to the ora terminalis. At this point the simple epithelium sud-
denly becomes stratified and complex to form the sensory retina.

Travelling thus forward to the pupil in the pigment epithelium and
backward again into the sensory retina proper, we are easily able to see
that the entire retinal coat of the eye reaches to the pupil margin and
forms a two-layered cup. The two major layers — pigment epithelium
and retina proper — develop directly from the two layers of the embry-
onic optic cup, which arises as a bubble of tissue on the side of the
brain, becoming constricted off therefrom and deeply indented on the
side toward the skin. This indentation gives the vesicle an outer and an
inner layer and an opening, aimed toward the surface of the head, into
which the lens is received after its separation from the skin (see Fig. 38,
p. 106). Thereafter the opening becomes (relatively) smaller, and per-
sists as the pupil.

The Visual-Cell Ltayer— Standing on the external surface of the
retina proper, and constituting its receptive layer, are the rods and cones
(Fig. 19). These elongated cells thus point away from the light, which
must pass through the remainder of the retina to reach them (hence the
complete transparency of this tissue as contrasted with the brain, which
has a similar histological organization). Their tips are pressed against
the pigment cells or are even buried in deep indentations in them, or
between their processes when such are present. The processes in turn
may reach nearly to the bases of the rods and cones so that they are
deeply interdigitated with the latter. Though there is seldom a conti-
nuity of substance, the dovetailing of the sets of processes and visual
cells is so intimate and firm that one or the other is often torn in two
if the retina and chorioid are forcibly separated. In other cases the
absence of all pigment-cell processes may make a separation very easy,
and only the optic nerve, the fusion of the two layers of the optic cup
at the ora terminalis, and the pressure of the vitreous then hold the
retina firmly and smoothly in place.

At the level of the bases of the rods and cones the retina has its ex-
ternal limiting membrane (briefly, the 'limitans') which may be likened
to a piece of wire screening through each hole of which a rod or cone
projects. The visual cells are a tight fit for the holes and are thus kept
perpendicular to the membrane and prevented from getting out of line
by any sliding lengthwise past each other. In some retinas, delicate hair-
like processes from the outer surface of the membrane itself form so-

46 THE VERTEBRATE RETINA

called fiber-baskets, fused with the surfaces of the bases of the visual
ceils and anchoring them very firmly in place.

On the inner side of the limitans lie the nuclei of the rods and cones.
The diameters of these are ordinarily much greater than those of the
cytoplasmic parts which protrude outward through the limitans. This
results in the nuclei piling up into several rows (forming the 'outer
nuclear layer') the number of which in a given retina will be roughly
equal to the quotient of the square of the diameter of the nucleus divided
by the square of the diameter of the predominant type of visual cell.
Cones are usually so plump at their bases that there is room for their
nuclei to lie up against the limitans or even above it; but a rod nucleus
may lie far below its rod, being connected with the latter by a slender
thread which winds its way up among the intervening rows of nuclei.

The Bipolar Layer — From each visual-cell nucleus a short thread-like
*foot-piece' travels inward (toward the vitreous) until it clears the other
visual-cell nuclei, and then expands into a terminus which may be either
smoothly rounded, or branched like a bird's foot (Figs. 19, 22, 23, 24).
This is related, as in a handclasp, to a similar arborization at the outer
end of a 'bipolar' neuron, whose cell body lies deeper in the retina
toward the vitreous. A bipolar dendrite may embrace several or a great
many visual-cell termini, so that the number of bipolar cells in a retina
is always less than the number of visual cells. The branched process of
the bipolar cell which joins to the visual cells, and the similar process
from the bipolar cell-body which travels in the opposite direction (to-
ward the vitreous) are however much more slender than the cell-body.
The bipolar nuclei are consequently piled up in several layers like those
of the visual cells, and this second band of nuclei forms the 'inner nu-
clear layer' of the retina (Fig. 19). In this layer, along with the nuclei
of bipolar cells, are a (usually) smaller number of nuclei belonging to
several types of cells which will be mentioned later.

Some of the bipolar cells each connect with but one cone. Such are
the numerous 'midget bipolars' of the primate retina (Fig, 19, b). Other,
'diffuse' bipolars (Fig. 19, db) of several types may each embrace a great
number of rods, and some cones as well. In many retinae there are diffuse
bipolars which connect only with rods, or only with cones; but such
elements appear to be lacking in man.

The inner nuclear layer is separated from the outer nuclear layer by
a feltwork of the delicate nerve fibers which make the connections

BIPOLAR AND GANGLION LAYERS 47

between visual cells and bipolars. This is the 'outer plexiform layer'.
An 'inner plexiform layer' also occurs on the vitread side of the inner
nuclear layer, and has a similar significance. In it lie the synaptic junc-
tions between bipolar cells and the innermost of the three masses of cells
concerned with the projection of the image to the brain — the 'ganglion
layer'.

The Ganglion Layer — The cells of this layer (Fig. 19) have either
small or large bodies and simple or elaborate dendrites which reach up
into the inner plexiform layer to meet the termini of the bipolars. Each
ganglion cell gives off a slender axon process which courses along the
inner surface of the retina, next to the vitreous. All of these fibers, from

Fig. 21 — The optic chiasma.

a, of man, showing partial decussation of optic nerve fibers.

b, of bird, showing total decussation; in some vertebrates (i.e., most fishes) the nerves are
not thus plaited — but whether the fibers are interwoven or not, they all decussate in non-

mammals.

c- chiasma; n- optic nerve;

retina; /- optic tract, which enters brain.

all over the sensory retina, converge at one place in the 'fundus' (back)
of the eye and there turn parallel to each other and pass outward
through the retina, chorioid and sclera in a compact bundle as the optic
nerve, which travels toward the brain (Fig. 21).

A ganglion cell may gather in the axons of several bipolars (Fig. 19,
pg) , just as one of the latter in turn often connects not with one visual
cell but with several. This has been called the 'inward convergence' of
the visual cells upon optic nerve fibers, or 'summation'. The impulses
which travel down several visual-cell foot-pieces are summated in their
efforts to stimulate a single bipolar cell, and numbers of bipolar nerve-
impulses are in turn gathered into single ganglion cells and optic nerve

48 THE VERTEBRATE RETINA

fibers. This phenomenon of summation is of the utmost importance in
the physiology of the retina, and will be discussed again when certain
other concepts have been introduced.

The three kinds of retinal elements so far mentioned — visual, bipolar,
and ganglion cells — are those concerned in the simple, straightforward,
projective pathway of the visual impulse to the brain. There are four
other types of cells which remain to be described: Miiller fibers, neu-
roglial cells, horizontal cells, and amacrine cells.

Miiller Fibers — Miiller fibers may be likened to rivets which run
through the whole thickness of the retina proper and bind its layers
together (Fig. 19, m). Their outer ends form the external limitans and
their inner ends are expanded into trumpets or pyramids whose bases,
against the vitreous, are six-sided and are fitted together as an unbroken
mosaic, the internal limiting membrane of the retina. This is not a true,
isolable membrane but simply the inner surface of the retina. The vitre-
ous which touches the internal limitans may be a little tougher than the
rest, like the skin on a cornstarch pudding; but it is still part of the
vitreous — there is no distinct layer at the retino-vitreal interface which be-
longs to neither structure. The retina and vitreous are simply in contact.
The nucleus of a Miiller fiber lies about half-way through the thick-
ness of the inner nuclear layer and is very easily identified by its elon-
gated oval form. The boundary surface of a Miiller fiber, however,
cannot be made out at all unless the cell is isolated by the procedure
of macerating the retina; for the Miiller fibers have irregular expansions
and cavities in them, and occupy a surprising amount of the total volume
of the retina. If we imagine building a model of the retina by using wires
for the nerve fibers in it, and large glass beads for their nuclei, we could
then represent the whole population of Miiller fibers best by filling in all
the empty space with wax or some such substance. All of the nuclei in
the retina sit in pockets in the Miiller fibers, which at the levels of the
nuclear layers form a sort of sponge-work. Every nerve-fiber is likewise
insulated from every other by a film of intervening Miiller-fiber sub-
stance; and only at the synaptic handclasps between nerve-fiber ends is
there opportunity for separate nerve cells actually to come in direct con-
tact.

Neuroglia — The neuroglial cells of the retina are small and not num-
erous. They are like one of the chief types of glial elements in the brain
and spinal cord. While glial cells are abundant and im.portant in serving

SUSTENTATIVE AND INTEGRATIVE CELLS 49

as the connective-tissue of the central nervous system, their place is taken
in the retina by the Miiller fibers, which do the same job even better and
other jobs in addition. We may fairly consider the glial cells of the
retina to be meaningless, and present only because of their inheritance
from the brain wall of which the retina is, after all, a part. Occasionally
they seem to resent their idleness and become altogether too busy, gener-
ating a 'glioma' — a particularly disastrous type of tumor whose presence
calls for the immediate removal of the eye to prevent a fatal involve-
ment of the brain by way of the optic nerve.

Horizontal and Amacrine Cells — Although the Miiller fibers and
neuroglial cells are certainly not impulse-conducting elements, the 'hori-
zontal cells' are under suspicion of performing some sort of integration
of the retina. If we think of the visual^bipolar->ganglion-cell chain as
running vertically through the retina, then the amacrines and horizontal
cells do their work in a horizontal direction. The horizontals have their
cell-bodies among those at the outer surface of the inner nuclear layer
(Fig. 19, h). In lower vertebrates the horizontal cells are chunky and
epithelioid, or ropy and anucleate, and seem only to have a supporting
function like the Miiller fibers. In higher vertebrates, however, they more
often have many spider-leg processes running in the outer plexiform
layer. Thus they may give the appearance of nerve cells and very prob-
ably do conduct laterally, tying up one area of the retina with another
just as regions of the cerebral cortex are interconnected by association
fibers. Those of mammals (Fig. 19, h) are certainly conductive, and in
man have their stubby dendrites connected with cones and their long
axons connected with distant rods and cones.

The 'amacrine' cells ordinarily have this same horizontally integrative
function. Their exact action and its effects upon subjective visual phe-
nomena are about the biggest remaining mystery in the physiology of
the retina. Their nuclei tend to lie in the inner half of the inner nuclear
layer and each gives off a single process which passes vitread and then
branches more or less, the branches being short or very long (Fig. 19, a).
The amacrines seem to associate the bipolar^ganglion-cell synapses, per-
forming for the inner plexiform layer the same function that the con-
ductive types of horizontal cells do for the outer.

The action of these two types of cells would appear to be detrimental
to the preservation of the pattern of the retinal image during its 'wire-
photo' transmission to the brain in the form of nerve-impulses. If all the

50 THE VERTEBRATE RETINA

amacrines were carrying impulses at once, the result would certainly be
a hopeless garbling of the projective transmission and a blurring of the
cerebral picture of the external visual field. One would, then, expect to
find amacrines very few or even lacking in the retinae of those animals
whose vision is keenest and whose ability to discriminate fine-detailed
patterns is greatest. Yet it is in just such animals that the amacrines are
most abundant. In the birds, for example, they may even outnumber the
bipolar neurons. Obviously, only a few can be in action at any one time,
and they make of the retina an elaborate switchboard in which now one,
now another conduction may be enhanced or inhibited.

In primates, some of the elements formerly believed to be 'amacrine'
(hterally, 'lacking an axon') have recently been found to possess axons
after all. If their axons and dendrites have indeed been correctly iden-
tified (and the identifications are so far on a purely morphological basis) ,
then such elements are really bipolars of a peculiar sort — they conduct
toward the receptor layer. Such a supposed 'centrifugal' bipolar is shown
in Figure 19 (cb). Their discoverer, Polyak, thinks that they serve to
alter the state of activity of the visual cells. What this may mean, trans-
lated into terms of visual physiology and visual psychology, is not clear.
It seems as likely that the centrifugal bipolars intensify (or prolong) the
activity of ordinary bipolars in a given amount or pattern of illumin-
ation, by (so to say) taking excitation from their lower ends and putting
it back in at their tops. Anyone familiar with radio hook-ups (which the
diagram in Fig. 19 rather resembles!) can see how the centrifugal bipolar
may be compared with a tickler coil in a regenerative circuit.

There are many true amacrines in primates, however; and these axon-
less, horizontal integrators are abundant in other vertebrates — partic-
ularly so, in birds (v. s.).

A moment's thought about the mystery of the amacrines suffices to
convince one that the retina is more than just a sense organ which re-
tails to the brain, parrot-fashion, the physical changes in the environ-
ment. The retina is an association center with every bit as complex a
mode of action as the cerebral cortex itself. The elucidation of its switch-
board activities is almost beyond the realm of physiology.

Nutrition of the Retina — The nervous tissue of the retina probably
does not have a high rate of metabolism, but the rods and cones are very
sensitive to any interference with their supplies of materials and oxygen.
These come from the chorioid, which aside from its light-absorbing func-

NUTRITION OF THE RETINA 51

tion is wholly devoted to the nutrition of the visual cells. The turnover
of substances must be very great, for the chorioid is very rich in blood
vessels which indeed comprise most of its bulk in many animals.

Just outside of the lamina vitrea lies a network composed of broad,
flat capillaries. This 'choriocapillaris' reticulum (Fig. 6b, p. 14) is so fine-
meshed that its capillaries total a greater portion of its area than do
the spaces between them. It is with the blood in the choriocapillaris that
the visual cells make their exchanges of supplies and wastes, liaison
being effected by the pigment epithelium which is thus taking in and
giving off materials at both of its surfaces continuously. The retina
often has blood vessels clinging to or embedded in its inner surface, but
these are usually concerned only with the nutrition of the inner layers
of the retina. Even where (as in most mammals) capillary branches of
these vessels invade the retina itself, they almost never reach outward
beyond the inner nuclear layer and obviously belong only to the vitread
portion of the retina. Such a capillary shows in Figure 19.

The choriocapillaris is supplied with blood by a layer of arteries
outside of it in the chorioid, and drains into a layer of large inter-con-
necting veins which lie on the scleral side of these arteries (Figs. 4a, 6a;
pp. 8, 14). The veins converge in the four quadrants of the eyeball to
pour their contents into the four great 'vorticose veins' which conduct
the blood away from the equator of the eye. Other vessels also penetrate
the sclera anteriorly and supply or drain structures other than the retina.
The vessels mentioned above, which supply the inner layers of the retina,
are few and are branches of vessels which enter the eyeball in or along
with the optic nerve. True retinal vessels are present only in the eels and
the mammals — -and not even in all of the latter, some of whose retinas
(e.g., in the rhinoceros) are as completely avascular as those of the lower
vertebrates.

All of the vessels concerned with the eye apart from the retina— and
even including those last mentioned above — do not, taken together, com-
pare in abundance with the rich chorioidal circulation. This latter exists
solely for the benefit of those cells of the whole eye which are most
important, if any are that: the rod and cone visual cells.

The Optic Nerve — The human optic nerve takes a long, slightly
undulant course to the apex of the orbit and there enters the cranium
(Fig. 16, p. 37). It is flexible, and by its length allows enough slack to let
the eye rotate freely. It contains more than a million nerve fibers, most of

52 THE VERTEBRATE RETINA

which transmit visual impulses, though many are centrifugal. It is heavily
ensheathed by tendinous and vascular coats continuous on the one hand
with the sclera and on the other hand with the meningeal coverings of
the brain, and is divided by internal septa, of connective tissue and neu-
roglia, into many fiber-bundles. The central retinal artery and vein join
the nerve at some distance from the eyeball and run through its center
to emerge within the eye at the nerve head, where they branch over the
inner surface of the retina. The optic 'nerve' is called such only for
convenience. It is not a true nerve but, like the retina, an ectopic portion
of the brain itself.

Within the cranium the two optic nerves cross through each other
and continue, as the 'optic tracts', into the brain. The crossing or
'chiasma' is especially complex in man and in all other mammals, for
in them only some of the fibers from each eye cross into the opposite
optic tract, the others going directly into the tract on the same side.
In other vertebrates, the crossing or 'decussation' of the fibers is com-
plete — that is, all of the fibers from each optic nerve enter the opposite
side of the brain (Fig. 21). No special advantage is gained by such an
arrangement — it arose mysteriously along with the numerous similar
decussations in the tracts of the brain, brain stem, and spinal cord; but
there is a special value of partial decussation which will be found ex-
plained in Chapter 10, section D. Even where the decussation is total,
the chiasma is seldom a simple anatomical crossing of one whole optic
nerve over the other. This is indeed the situation in most fishes; but
elsewhere the two nerves are interwoven to a greater or lesser extent
(Fig. 21b).

(B) Types of Visual Cells

General Types— Rods versus Cones — The visual cells of vertebrates
are of two general types which were long ago given the names 'rod' and
'cone' — though with our superior modern knowledge of their phylogen-
etic ramifications and physiological characteristics we might wish that
a more apt pair of names could be substituted for the traditional ones.
In a given retina containing both highly sensitive visual cells (rods)
and relatively insensitive ones (cones) , the high- and low-threshold cells
can always be told apart; but the rod of one retina may resemble struc-
turally the cone of another, or may give evidence of having been recently

OPTIC NERVE; RODS VS. CONES 53

derived from a cone-type in an ancestor of different habits. In an at-
tempt to resolve the confusion resulting from an overemphasis of shape-
differences — which has even led some to deny any distinction between
rods and cones! — the writer several years ago proposed the names
'photocyte' and 'scotocyte' for the two physiological types of visual
cells contrasted in the Duplicity Theory (see next Section). But it is
perhaps too late to bring about any such revolution in the terminology.

Of the two types, there can be no doubt that the cone is the older and
more primitive. This statement however — which is quite contradictory
to any the reader will find in other books — is not to be taken to mean
that cones entirely like those of man were the original vertebrate visual
cells. It is certain, for instance, that the ancestral cell lacked any means
of analyzing colors. It is equally certain that the common ancestor of
present-day rods and cones lacked any such ingenious sensitizing sub-
stance as rhodopsin (see Chapter 4) . With a slender, pointed, stimulable
organelle, the outer segment, derived from a formerly vibratile flagellum
(see Chapter 5, section B) and connecting directly to a simple afferent
neuron, the pro-vertebrate visual cell could not but have been a high-
threshold receptor, which limited the excursions of its owner to the
brightly lighted surface waters.

Rods came later, as a means of extending the period of activity over
a greater portion of the twenty-four hours. They were derived quite
simply from cones by the enlargement of the outer segment and by an
increase in the number of visual cells connected to each nerve cell. It
was not desirable for all of the visual cells to make these changes, for
unless two types were preserved side by side in a nice balance, sensitivity
to dim light could not be increased without too great a sacrifice of re-
solving power. The needs of the animal — whether greater for sensitivity,
or for visual acuity — then determined the proportion of small un-sum-
mated and larger, summated visual cells which would give him optimal
visual capacity. With the invention of the powerfully sensitizing rhod-
opsin by the rod on the one hand, and the differentiation of a photo-
chemical basis for hue-discrimination in the cones on the other hand,
the widely useful duplex retina as we know it today came into being.

Single Cones — Because of the antiquity and priority of the high-thres-
hold cell, we will consider first the cytology of a typical single cone such
as that of the frog (Fig. 22c). The elaborate cytoplasmic portion of this
complex cell protrudes through a lacuna of the external limiting mem-

54

THE VERTEBRATE RETINA

brane, which constricts its base firmly and keeps the nucleus of the cone
on the vitread side. The tapered photosensitive tip of the cell is the
outer segment, the remainder of the cell down to the nucleus being the
inner segment and representing the columnar body of the ancestral epi-
thelioid ependymal cell. In the distal end of the inner segment lies the

( cf

Fig. 22 — Single cones.

1000.

a, of sturgeon, Acipenser fulvescens. b, of goldfish, Carassius auratus; light-adapted {i.e.,
with myoid contraaed — cj. Fig. 62, p. 146; in fishes, the cone nucleus often lies partly or
wholly above the external limiting membrane, as here), c, of leopard frog, Rana pipiens:
dark-adapted {i.e., with myoid elongated — c/. Fig. 64, p. 148). d, of snapping turtle,
Chelydra serpentina, e, of marsh hawk. Circus hitdsonius; from the circumfoveal eminence,
f, of man; from the circumfoveal eminence.

d- oil-droplet, embedded in: e- ellipsoid; /- foot-piece; /- external limiting membrane;

m- myoid; n- nucleus; o- outer segment; p- paraboloid.

ellipsoid, whose shape in the frog cone happens to justify this geomet-
rical name, though this is seldom true. Embedded distally in the ellipsoid
is the oil-droplet, which in some frog cones contains a dissolved yellow
pigment. The stalk-like portion of the inner segment is highly contrac-
tile (Chapter 7, section B) and hence is called the myoid (= muscle-
like). The myoid joins the large, ovoid nucleus in which the chromatin

SINGLE CONES

55

occurs in a reticulum of many small granules. From the region of the
nucleus a short, thick, dendritic 'cone-foot' proceeds vitread to make a
synapse-like junction with a bipolar dendrite.

&

y/

Fig. 23— Rods. X 1000.

a, generalized rod, showing organelles as they might appear if visible in the living cell;
note myeloidal spiral and centrosomic Fiirst fiber in outer segment, diplosome and Kolmer-
Held fiber proceeding therefrom in inner segment, b, rod of Protopterus cethiopicus—
unusual, in that it contains an oil-droplet, implying secondary origin from a cone (c/. Fig.
25). c, rod of goldfish, Carassius auratus; light-adapted (i.e., with myoid elongated — cf.
Figs. 62 and 63). d, common or 'red' (rhodopsin-containing) rod of leopard frog, Rana
pipiens; dark-adapted {i.e., with myoid contraaed — cj. Fig. 64). e, 'green' (Schwalbe's)
rod of Rana pipiens. i, rod of flying squirrel, Glaucomys v. volans; exemplifies the fila-
mentous type characteristic of many strongly nocturnal animals, g, human rod from near
the temporal side of the macula lutea.

d, oil-droplet; e- ellipsoid; /- foot-piece; /- external limiting membrane; m- myoid (the
corresponding portion of the inner segment is non-contractile in e, f, and g); n- nucleus;
o- outer segment; p- paraboloid.

56 THE VERTEBRATE RETINA

Not all single cones are built like those of the frog. The oil-droplet
is lacking in the cones of nearly all living forms lower than the frogs;
but even so there are reasons for thinking the oil-droplet to be a very
primitive visual-cell feature. Such droplets occur in pigment epithelial
cells, which are homologous with the visual cells, and apparently also
(in salamanders) in the type of brain-cell from which the rods and cones
originated. The ellipsoid, which appears to be a light-concentrating
device, is sometimes supplemented by a second dioptric organelle, the
paraboloid, lying proximal to it in the myoid. The paraboloid may have
some very important function other than its incidental optical one.
While the ellipsoid always stains heavily with acid fuchsin, an out-
standing peculiarity of the paraboloid is its usual refusal to take any
stains at all. It is quite likely that some paraboloids are fluid vacuoles —
perhaps sometimes artificial spaces (Figs. 22a, 23b, 24a and b) ; but
many are solid or semisolid (Figs. 2 2d, 25) and keep their shape when
expressed from the living cell.

The cone outer segment may actually be cylindrical when it is so very
slender that it could hardly be expected to taper, as in many lizards and
birds, and even sometimes when there is plenty of room for a more
bulky, conical structure (Fig. 22). The myoid may be quite non-con-
tractile and thus undeserving of that name, as in man; and it may be
permanently greatly elongated, marooning the body of the cone opposite
or even beyond the tips of the rods (flying squirrels, some lampreys and
snakes — see Fig. 69a, p. 167). The nucleus of the frog cone is typical
structurally, but not as regards its position, for cone nuclei almost always
lie in contact with the limitans or even (some fishes) beyond it, on its
scleral surface (Fig. 22a and b).

One of the most noteworthy peculiarities which cones may have is
that presented by the cones of the greater portion of the human retina,
and also by some other placental mammals, the dog and cat for exam-
ple : the cone outer segment is a cylinder enclosed by a tubular process
of the pigment epithelial cell opposite to it, and apparently (though this
is not yet certain) fused at its tip with the pigment cell, actual proto-
plasmic continuity existing between the two (Figs. 19, 20b; pp. 43, 44).
No such arrangement is ever seen in rods, and its obvious advantages for
the facilitation of the nutrition of the cone constitute important evidence
for the cone's having a faster metabolism than the rod — something
which has long been suspected on other grounds.

RODS; HOMOLOGY WITH CONES 57

Rods — One rod would do about as well as another to illustrate rod
structure, for rods do not differ from retina to retina nearly so much
as do cones. The rod (Fig. 23) has the same principal parts as the cone
— outer and inner segments, nucleus, and foot-piece. The outer segment
is almost without exception a perfect cylinder and the inner segment is
often more slender — sometimes, as in bony fishes, much more so.

The rod in man and other mammals is not contractile; so, the term
'myoid' for the undifferentiated part of the inner segment would be a
misnomer. A structure corresponding in microchemical behavior to the
cone ellipsoid is present, though it is probably optically functionless.
Rod nuclei tend to be smaller, more nearly spherical, and with much
larger and fewer masses of chromatin than cone nuclei. The latter hav-
ing preempted positions against the limitans (the cones being the first
visual cells to differentiate in embryonic retinae), the rod nuclei per-
force contact the limitans only between cone nuclei and for the most
part are forced to pile up below it to form the thick outer nuclear layer.

Cones ordinarily vary considerably in different retinal regions, being
more slender and more numerous toward the fundus. Rods are uniform
in concentration everywhere except as this is influenced by the cones —
it is as though the cones had been distributed in the retina first, and
then the spaces between them neatly filled in with as many rods as
would conveniently fit. Rods are ordinarily uniform in diameter through-
out a retina, but their length tends to increase slightly and slowly from
ora to fundus. The center of concentration of cones, or of rods when
they have such a center, does not necessarily lie anywhere near the optic
axis of the eye. Seen 'on the flat', the rod and cone mosaic exhibits a
pattern which in different animals may have the hexagon, the square,
or some other geometrical figure as its unit. These patterns have not
yet been sufficiently studied for them to yield up any ulterior meaning
which they may have.

Homology of Rods and Cones — Cone and rod are homologous part
for part and have many points in common. The outer segments of both
have thin sheaths filled up with a lipid ground-substance in which one
or more closely wound spiral filaments of another lipid material, derived
from mitochondria, are embedded (Fig. 23a). These show faintly or
clearly in large rod outer segments (Figs. 25 and 26), rarely also in
cones; but they are presumably always present. When too heavily
stained, they commonly give an appearance of transverse discs (Figs.

58 THE VERTEBRATE RETINA

22f, 23g). A long filament runs axially or peripherally in the outer seg-
ment of (again, presumably) every visual cell and, just within the inner
segment, is connected with a pair of granules from which a second,
much shorter, filament proceeds down the inner segment for a way
(Fig. 23 a). This filament-and-granule apparatus, collectively, is the cen-
trosome of the cell, whose function in visual physiology, if any, is not
known. Rods may contain paraboloids, or even oil-droplets (Figs. 23b,
25b, c) , though only when the rods have had a peculiar history (Chapter
7, section D). The rod foot-piece may be just like a cone-foot; but in
animals whose rods are very slender and numerous (teleosts, mammals,
and nocturnal birds) it is a slender filament terminating in a highly
specialized, unbranched 'rod end-knob' — apparently to make more com-
pact the connections of many rods to single bipolars (Fig. 19, p. 43).

It is also in such animals that the rod and cone nuclei are most sharply
differentiated as to size, shape, and chromatin distribution. In forms
with fewer, more bulky rods (lampreys, amphibians, many reptiles) the
rod and cone nuclei are indistinguishable on any basis other than pos-
ition, and the foot-pieces may be nearly or quite identical. In connection
with the question whether the rod or the cone is the more primitive cell,
it is significant that when the nuclei and foot-pieces are alike in a retina,
they both resemble the cone structures of retinae in which they differ —
and, cone-type nuclei are more like nuclei in general than are rod-type
nuclei. The heavy, dendritic cone-foot would also appear to be a more
primitive sort of connecting process than the peculiar rod-fiber and its
end-knob. Where they are markedly differentiated, the differences be-
tween rod and cone nuclei have no relationship to physiological differ-
ences which we are able to discern at present.

Green Rods — There is a type of so-called rod, restricted to the am-
phibians, whose very long stalk is but slightly contractile (Fig. 23 e).
It lacks rhodopsin and this, together with the shortness of its outer
segment, would necessarily make it have a relatively high threshold.
Functionally, this 'green rod' (of Schwalbe) is probably more cone-like
than rod-like — its nucleus even lies in the inner part of the outer nuclear
layer, alongside the cone nuclei; but its origin is quite unknown.

Double Cones — Even more mysterious are the 'double cones' — and
the puzzle they present is particularly irritating to the curious inves-
tigator because they are so very widespread among vertebrates. If they
occurred in only one or two animals, we might dismiss them as a curi-

DOUBLE CONES

59

osity. Perhaps if they occurred in the human retina we would before
now have gained some clue to their role in visual processes; but their
functional significance, their exact mode of formation in the developing
retina, and the probable time and manner of their evolutionary origin
have yet to be determined. Next to the amacrine cells, the double cones

Fig. 24 — Double and twin cones, x 1000.

a, double cone of a holostean fish, the bowfin, Amia calva. b, double cone of leopard
frog, Rana pipiens; dark-adapted {i.e., with myoid of chief cone elongated), c, double
cone of western painted turtle, Chrysemys picta marginata. d, double cone of European
grass snake, Matrix natrix. e, twin cone of a teleost fish, the bluegill, Lepomis m.
macrochirus; light-adapted (i.e., with fused myoids contraaed). f, conjugate element (of
Fundulus heteroditus; after Butcher) characteristic of some teleosts; perhaps intermediate
between a and e, perhaps instead a derivative of e.

c- 'clear mass'; d- oil-droplet; e- ellipsoid of chief cone; e'- ellipsoid of accessory cone;

/- foot-piece; g- 'granular mass'; /- external limiting membrane; m- myoid; n- nucleus of

chief; n- nucleus of accessory; o- outer segment of chief; o'- outer segment of accessory;

p- paraboloid.

are physiologically the most obscure elements in any and all retinae.
They have unfortunately not greatly interested visual physiologists,
since the latter have their attention focused upon the human retina, in
which double cones are lacking.

Double cones appear phylogenetically first in the holostean fishes
(Fig. 24a). They occur in amphibians, reptiles, birds, one monotreme
(Ornithorhynchus) and marsupials, but not in any known placental

60 THE VERTEBRATE RETINA

mammals although some of the most primitive of these may prove to
have them when examined. So, most vertebrate groups have double
cones; yet we have no idea what they mean. The most that can be said
is that the number of double cones, relative to the total number of cones,
tends to be high in strongly diurnal animals and low in strongly noc-
turnal ones. As a maximum, double cones may about equal in number
the single cones of the same retina.

The typical double cone (Fig. 24b, c ) consists of two very unlike
cones fused together in the lower myoid region. One member — the chief
cone — is always very much like the single cones in the same retina. The
other, or accessory cone is decidedly different. The ellipsoid is usually
unclear in outline proximally and its material blends with the ground
substance of the inner segment. There is almost never an oil-droplet,
but an enormous paraboloid is almost invariably present. This so dis-
tends the accessory myoid that the myoid of the chief cone is thinned
and curved around the paraboloid region so as to be almost indistin-
guishable proximally. There are two nuclei, and some indications that
the two foot-pieces connect with different bipolars. The two members
of a double cone seem to supplement each other — an organelle which
one lacks, the other possesses; but since everything that may be present
in the two members together may also occur in one single cone, the
segregation of parts in the double cone is without obvious meaning.

Twin Cones — Quite another sort of element is the 'twin cone' (Fig.
24e) found in so many teleost fishes. In this receptor the two members
are identical and are fused throughout the length of the inner segment.
Thus the twinned myoid contracts and elongates as a unit during photo-
mechanical changes, whereas in double cones only the chief member
moves, the accessory having no myoid in the proper sense of the word.
Twin cones are strictly a teleostean monopoly. These fishes being a
terminal group in evolution, it is impossible to believe that ordinary
double cones developed from twin cones; nor is there much reason to
suppose that twin cones were ever double ones of the type described
above. But there are elements in some teleosts which for want of a third
possible name we shall have to call double cones (Fig. 24f ) . They seem
to represent twin cones in which the two ellipsoids and outer segments
have become unequal in size and different in staining properties and
hence, chemico-physical makeup; but the zone of fusion still extends the
whole length of the inner segment so that the two myoids contract and

TWIN CONES; OPHIDIAN DOUBLE CONES 61

lengthen as one. These structures indicate that the makeup of the com-
mon double cone is worth imitating for some reason; and we shall see
shortly that the snakes have also discovered this for themselves. But,
until the distribution of these peculiar elements is better known and has
been related to teleostean taxonomy, there remains the possibility that
some of them are derivatives of holostean double cones (Fig. 24a) which
have never quite equalized their two members, rather than a secondary
departure of twin cones in the direction of double ones.

Like the double cones of other classes, the twin cones of the teleosts
appear to be related to diurnal activity. Wunder has shown that they
are most numerous in surface fishes, less and less common in fishes
which habitually swim at greater and greater depths. Thus they seem
somehow to be associated with vision in bright light, though apparently
not with sharp vision since they are excluded from teleost foveae. More
than that cannot be said about them in the light of present knowledge.

Ophidian Double Cones — The double cones of snakes are quite
unique. Though all lizards have double elements of the standard type
(Fig. 25a), the primitive snakes of the boa family have only single cones
of one kind, together with rods (Fig. 69b, p. 167). In the big central
family of snakes, the Colubridae, the standard retina contains only cones
of three types. One of these (Type A) is a large single cone and is
abundant. Another (Type C) is a small single cone which occurs always
in small numbers and is entirely lacking in the retinae whose resolving
power is highest.

The Type B, double, cone (Fig. 24d) bears no resemblance to double
cones outside the snakes. Its chief member is bulky, and is identical
with the Type A single cone. The accessory is extremely slender and is
fused with the chief cone throughout the length of the inner segment.
The accessory nucleus is often displaced laterally in the outer nuclear
layer; and applied to it is an organelle, the paranuclear body, which
occurs only in ophidian double visual cells. Snake cones have no oil-
droplets or paraboloids, and the ellipsoid usually fails to stain with acid
fuchsin. The inversion of size-relationship of chief and accessory, the
paranuclear body, the absence of a paraboloid, and the extensive fusion
of the inner segments set the ophidian double cone off so sharply from all
others that even if it were present in the Boidae one could feel certain that
it was originated de novo within the snake group, and represents the
second — at least — separate invention of a double cone by vertebrates.

62

THE VERTEBRATE RETINA

Double Rods — Still another kind of visual cell is the double rod. These
were long known in geckoes (a family of nocturnal lizards) and have
recently been found in snakes. The gecko double rod (Fig. 25) was

Fig. 25^Double rods in lizards, and their derivation, x 1000.

a, the two cell-types of the pure-cone retina of the (diurnal) collared lizard, Crotaphytus
collaris; parts as in Figs. 22 and 24. The outer segments are tiny and the oil-droplet is
yellow in life.

b, cell-types of Rivers' night lizard, Xantusia riversiana. The outer segments have become
rod-like but contain no rhodopsin, and the oil-droplets are large and colorless. Morpholog-
ically, these elements are intermediate between cones and rods; physiologically, they are
low-threshold.

c, the cell-types (single and double rods) of the banded gecko, Coleonyx variegatus. The
massive outer segments contain rhodopsin, and the oil-droplets have disappeared.

certainly not derived from a bifurcated single rod, but directly from a
double cone. It is thus closely homologous with the ordinary type
of double cone since it is the latter which occurs in diurnal lizards. The
double rods in certain snakes (Fig. 26) were just as certainly derived
from the peculiar ophidian type of double cone, for they have exactly

DOUBLE RODS

the same structure except for the size and shape of the outer segments.
They contain no rhodopsin, and owe their sensitivity to the large vol-
ume of their outer segments and to their multiple connections to single
nerve cells. The gecko double rod does contain a rhodopsin, indicating
that this substance, like other pigments such as hemoglobin and melanin,
can be evolved repeatedly and was not invented once and for all.

This whole matter of the conversion of one type of visual cell into
another will be discussed at some length later (Chapter 7, section D).
It has a considerable bearing upon the ability of animal species to change
their characteristic behavior with respect to light, and upon the question
of the capacity of animals for discriminating colors (see Chapter 12).

Fig. 26 — Double rods in snakes, and their ancestry.

a, the three cell-types of the pure-cone retina of a diurnal colubrid, the European gcass
snake, Matrix natrix; parts as in Figs. 22b and 24d. Type A is the ordinary single cone;
type B is the double cone, equal in numbers to A; type C is an uncommon single cone with
dark-staining ellipsoid.

b, the homologous rod types of the spotted night snake, Hypsiglena o. ochrorhynchus. In
this genus and in some other colubrids, the ancestral cones have all been converted into rods,
through intermediate conditions shown by such forms as Cemophora, Arizona, Rhinocheilus,
and Trimorphodon. See Figure 68a, p. 166.

Since cones can and do change into rods in evolution — and rods into
cones, as well, though less often — it is not surprising that numerous
halfway stages in such derivations occur in living forms. These are, of
course, grist to the mill of those few who insist that any distinction be-
tween rods and cones is wholly artificial. Naturally, such cells do defy
classification, and will not be considered here as discrete types.

64 THE VERTEBRATE RETINA

(C) The Duplicity Theory

History — In 1866 the great retinologist Max Schultze unobtrusively
announced a conclusion to which he had come after some fifteen years
of investigations in comparative ocular histology. He had been struck
by the correlation between the relative numbers of rods and cones in
various retinae and the habits of their possessors with regard to light.
Nocturnal vertebrates had many rods, and few cones or even none.
Diurnal species had ipany cones, and might even lack rods entirely.
Schultze suggested that the cone is the receptor for photopic (bright-
light) vision and that the rod is the organ of scotopic (dim-light) vision.
To this he added a corollary hypothesis that the cone alone is respon-
sible for color vision; for in dim light colors are no longer discriminable
and the world presents itself only in shades of gray.

This theory passed unnoticed by the physiologists and early psychol-
ogists until, toward the end of the century, the same idea was brought
forward independently by two men who were led to conceive it by differ-
ent lines of evidence, and neither of whom knew much of Schultze's
work. Parinaud, studying human vision in certain pathological condi-
tions, produced his 'theorie des deux retines'. Von Kries, repeating and
extending Schultze's observations on twilight vision, with special refer-
ence to the vision of the retinal center, formulated the 'Duplizitats-
theorie' about as we have it at present.

It is not at all uncommon for psychologists and medical men to say
even today that the Duphcity Theory is ^^only a theory," and to express
considerable doubt as to its vahdity. This ordinarily implies a con-
finement of knowledge to the basis of the theory in human vision. Of
course, if one considers only the known facts of human vision, one can-
not expect to be able legitimately to use very many of them to prove the
very theory which was evolved to explain them. But the comparative-
ophthalmological findings of Schultze and of many zoologists since his
time have built so unshakable a foundation for the theory that its major
tenets may be regarded as proven facts. True, there are prominent
French retinologists who do not believe in it, but their methods of study
are so antiquated that it is hardly surprising that they are unsure of the
distinctness of rods and cones.

It is necessary however to bear in mind that the Duplicity Theory as
we state it nowadays is really two theories in one. It states that the rods
are responsible for the hazy, crude, achromatic (black-gray-white) per-

THE DUPLICITY THEORY 65

cepts of dim light and that the cones yield the sharp, detailed images
and the chromatic (colored) sensations characteristic of bright-light
vision. Actually, the factors which make rod vision unsharp but sensi-
tive, and make cone vision sharp but requiring higher intensities of
illumination, are not the same as those which make rod vision achro-
matic and cone vision chromatic. We may be quite sure that animals with
rod-rich or pure-rod retinae have only diffuse mental pictures and can
see in very weak light, but we have at present no proof that all cones
are hue-discriminatory and that all rods are not. To date, no animal
positively known to have only rods in its retina has been properly tested
for color-vision capacity, and many animals which have plenty of cones
have been shown not to have color vision (see Chapter 12, section A).

Sensitivity versus Acuity — When we say that an animal sees well or
sees poorly, that it can see in the dark or that it is blind in the daytime,
we are loosely jumbling together two aspects of vision which should be
carefully distinguished and thoroughly understood. They are indeed so
very different that they are practically mutually exclusive. These two
aspects are visual sensitivity and visual acuity. By the sensitivity of an
eye we mean its ability to respond to weak stimuli, the capacity it has for
continuing to respond to light as that light is slowly dimmed. By acuity
we mean the ability to continue to see separately and unblurred the
details of the visual object as those details are made smaller and closer
together. Sensitivity involves what the psychologist and physiologist call
'threshold of stimulation'; acuity involves what the physicist and opti-
cian call 'resolving power'.

Both the sensitivity and the acuity of the vision of any vertebrate
depend upon the structure and mode of operation of its entire visual
apparatus, including the gross plan of the eyeball, the characteristics of
the dioptric media, the retina, the cerebral structures involved in vision,
and the mental capacity of the animal. But the structure of the retina
sets ultimate, maximal limits upon both sensitivity and acuity which can-
not be exceeded by any sort of manipulation of other parts of the whole
system. We can therefore understand these two aspects of vision well
enough for the time being, if we examine the retinal basis for each.

Retinal Factors in Acuity—To consider acuity first: if the reader
will carefully compare a newspaper picture with one printed on the
glazed paper of a magazine, he will see that each is composed of dots,
and that the two pictures differ greatly in amount of detail. The news-

66 THE VERTEBRATE RETINA

paper picture is built up of large dots spaced widely, for on such rough
paper any finer dots would make only an inky blur. The magazine
photograph contains many more dots per unit area, and they are much
smaller. We say that the magazine picture is the better resolved of the
two. Similarly, we might take two photographs with the same camera
but using two different kinds of film whose emulsions differed greatly
in fineness of grain. The fine-grained picture could be enlarged much
more than the coarse-grained one without becoming blurry and losing
in detail. The fine-grained emulsion 'resolves' better what it 'sees'.
Again, through a well-corrected microscope lens one can see and count
fine dots, striations and the like which run together under less perfect
lenses — and again, we speak of a difference in resolving power as exist-
ing between the two. As we have seen, retinal images are very small;
but mental images are 'big as life' and the retinal image must stand
enormous enlargement without too much loss of detail, when it is trans-
lated into a mental picture of the visual field of the eye.

The dioptric apparatus of the eye may cast upon the retina an image
which is relatively large or small, hazy or sharp; but the retina in turn
may be crudely or finely built and upon this will depend the possible
maximum perfection of the cerebral image. The resolving power of the
retina is governed by three factors, all of which vary from retina to
retina and the last of which may even vary physiologically from time
to time within a single retina: (a) the slenderness of the visual cells;
ib) their closeness of spacing; and (c) the number connected with one
optic nerve fiber. The first two of these are almost self-evident; for if
the images of two object-points fall upon two separate visual cells, be-
tween which is an unstimulated visual cell, the two object-points may
be resolved; but if the visual cells are so plump or so far apart that the
two object-points are imaged upon two adjacent visual cells, they cannot
be distinguished as two points and will seem the same as a single large
object-point whose image covers the same two adjacent visual cells. In
the one case, we have an analogy for the fine screen through which a
picture is photographed for reproduction on coated paper as a half-tone
electrotype; in the other case, a coarse screen like that used with news-
print.

Factor "c" brings in the concept of summation presented in a pre-
ceding Section. Two object-points, whatever their size or separation, will
be seen as a single blur if their images fall upon visual cells which
connect with the same bipolar, or upon those whose separate bipolars

SENSITIVITY VS. ACUITY 67

connect with the same ganglion cell. Other things being equal, the more
bipolar and ganglion cells in a retina, the higher its resolving power.
Two retinae may be about equal in this regard even when one has many
slender, tightly packed visual cells and the other has fewer, plumper,
more widely spaced ones; for in the first retina there might be many
bipolars but few ganglion cells, or fewer bipolars and more ganglion
cells, and the overall resolving power be no greater than that of the
second retina whose visual cells were scanty and large — provided they
had isolated bipolar and ganglion-cell connections.

When sections of the retina are especially prepared so that its nerve
fibers and their connections are brought out, the retinal foundation for
the visual-acuity tenet of the Duplicity Theory is at once evident. Rods
are always connected in large numbers to single bipolar cells while cones
tend to have more isolated connections (Fig. 19, p. 43). Of the many
forms of bipolars in the human retina, the smallest (midget bipolars of
Polyak) each tend to be connected with a single cone and in turn to an
individual ganglion cell and optic nerve fiber, so that each such cone
has a 'private wire' to the brain; whereas, to extend the telephone anal-
ogy, other cones and especially rods are on the old-fashioned multiple
'party line'.

This great difference in the degree of summation of rods and cones
is the most important single factor in making rod vision diffuse and
cone vision sharp. It is much more than enough to compensate for the
fact that in almost all retinae the rods are more slender than the cones,
which would give the rod-population the higher resolving power if the
degrees of rod- and cone-summation were made equal. Thus the chief
reason for the crude character of rod vision is outside of the rod itself;
and we should so state the Duplicity Theory that it attributes acuity
differences not to the rods and cones themselves but to the entire rod-
vision and cone-vision mechanisms, each including a set of visual cells
and their particular bipolars, ganglion cells, and optic nerve fibers.
Relatively few bipolars connect with both rods and cones and probably
a minority of ganglion cells embrace both rod- and cone-bipolars. Parin-
aud's 'theorie des deux retines' is thus really more expressive of the
facts than is 'Duplicity Theory'. The most recent and accurate esti-
mates of the number of rods and cones in one human retina are : rods,
110,000,000 to 125,000,000; cones, 6,300,000 to 6,800,000 (Osterberg).
There are about 1,000,000 fibers in the human optic nerve, not all of
which are sensory; and in a sizable group of these (the macular bundle)

68 THE VERTEBRATE RETINA

each fiber represents a single, unsummated cone. Obviously, summation
is very great even in the human retina — and the human eye is built,
better than most, for 'sharp' vision!

Another important cause of the haziness of rod vision is the dilatation
of the pupil. To have only the rods in action, the illumination must be
dim — below the threshold of stimulation of the relatively insensitive
cones. The pupil opens to let in more light, which permits the rods to
continue in action but, incidentally, has two unfortunate effects: the
'depth of focus' of the eye is reduced, and the periphery of the lens
comes into play with its detrimental effect upon the quality of the
optical image. There is nothing the retina can do about it, and twi-
light vision here suffers another loss in resolution for which the in-
dividual rods should not be blamed. In animals whose eyes are built for
moonlight, this factor may be negligible or absent since the lens is then
large, and the whole area of its surface exposed by the widened pupil
is probably optically 'good'; but the retinal summation factor is still pres-
ent in such animals, and indeed in far greater degree than in ourselves.

Retinal Factors in Sensitivity — The differences between rod- and
cone-vision with regard to sensitivity are, like the acuity-differences,
caused by three factors. They are not unrelated to the acuity-differences,
and in the case of sensitivity two of the factors reside in the visual cells
themselves and only one is extrinsic. The sensitivity-promoting factors in
the rod mechanism are: (a) the size of the outer segment; (b) the
extent of summation; and (c) rhodopsin.

The business end of a rod or cone is its outer segment. It is in this
part of the cell, nearest the pigment epithelium and thus farthest from
the source of light, that the light effects chemical changes which initiate
the impulse that travels down the length of the cell and, if it is strong
enough, evokes a nerve-impulse in the associated bipolar. By and large,
rod outer segments tend to be long cylinders whereas cone outer seg-
ments are shorter (Figs. 22-26) ; and while these may be as thick through
at their bases as rod outer segments, they taper more or less and may
even be quite pointed at their tips. Hence the names originally applied
to the two types of cells, though the human cone outer segment is now
known not to be at all conical when properlv preserved.

If a geometrical cone and a cylinder have the same area of base and
the same height, the cone then has only one-third of the volume of the
cylinder. Here is an important intrinsic reason why, other things being

SENSITIVITY VS. ACUITY 69

equal, a rod should be more sensitive to light than a cone — several times
as much photosensitive material is traversed by a pencil of light, when
it stimulates a rod, as when it stimulates a cone. Thus in dim light
sufficient chemical change may take place in a rod for an effective im-
pulse to reach the bipolar; but the same amount of light will not lead to
activity in a cone-bipolar alongside. The rod, then, will have the lower
threshold of stimulation — it will take less light to set off its transmission
of an impulse. Rods can lower their thresholds in evolution (thus in-
creasing their sensitivity) by lengthening their outer segments as long
as this does not interfere with the nutrition of the rest of the retina from
the choriocapillaris. Cones could of course also increase their sensitivity
by elongating and by approaching a cylindrical form; but they have not
often done so, except as a part of the process of transmuting into rods.

The second factor influencing sensitivity is the extent of summation.
If several visual cells are hammering at the door of a single bipolar, it
is more likely to be aroused than if a single visual cell has to try to evoke
a bipolar response without aid from others. Nerve cells carry impulses
in obedience to the 'all-or-none law', which means that if a given fiber
conducts an impulse at all, it transmits it at full strength. The visual
cells, however, are not nerve cells (see Chapter 5, section B) and there
is no evidence that their foot-pieces obey the all-or-none law. We are
consequently free to suppose that when even a little light strikes a
rod, something happens photochemically, and that several feeble im-
pulses travelling down several rod foot-pieces and impinging upon one
bipolar dendrite can start an impulse flowing in that bipolar. In the same
weak illumination, a single cone or even a rod would not carry an im-
pulse strong enough to awaken a private bipolar.

Indeed, unless the function of the multiple connections of rods to
bipolars is to promote the sensitivity of the whole rod-mechanism in this
way, the inward convergence of the retina becomes quite meaningless.
Summation tends to destroy visual acuity, and no animal needs or wants
diffuse vision for its own sake — he only tolerates it if he must do so in
order to gain the sensitivity which happens to be more important to him.

Bulky visual cells and extensive summation promote sensitivity, but
it is inevitably at the expense of visual acuity. Sensitivity and resolving
power are thus on the two ends of a see-saw, and whatever sends one up,
sends the other down. This relationship holds as well for extra-retinal
structures as for the retina itself; for the big lenses and wide pupils of
some vertebrates, which produce small bright images and lower the

70

THE VERTEBRATE RETINA

overall ocular threshold, reduce acuity; and in others the flat lens which
produces a broad image, spreading over enormous numbers of visual
cells, thereby increases the resolution but at the same time lowers the
brightness of the image and thus reduces the sensitivity of the eye as
a whole.

By far the most important factor in endowing the rods with their
great sensitivity is the substance which is called Visual purple' or better,
rhodopsin. This is a deep red pigment which is formed slowly but con-
tinuously in the rod outer segment. The greater its concentration there,
the more light is absorbed and the more effective is that light as a stim-
ulus for vision. Since rhodopsin is destroyed by light, it builds up to
higher concentration in dim light or darkness than in bright light. Thus

rods alone

(log) Intensity (log) Intensity

Fig. 27 — Evidence for the Duplicity Theory (see text).

the sensitivity of the rods automatically increases just when it will do
the most good, due to the excess of rhodopsin-formation over destruc-
tion, and decreases when that in turn is desirable, due to the excess of
rhodopsin-destruction over formation, in bright light. Moreover, the em-
ployment of rhodopsin for increasing sensitivity does not entail any
sacrifice of resolving power by the rod-mechanism, and there are few
vertebrates whose rods get along without it.

It is rhodopsin which is largely, perhaps entirely responsible for 'dark
adaptation', the familiar result of which is our ability to see quite well
around us in a theater after a few minutes in our seat, although we may
have had to feel to see whether the seat was empty, when we first came in.

Rhodopsin is entirely absent from cones at all times; and there is per-
haps so little of it in rods when they are brightly illuminated that they
must then fall back upon the intrinsic outer-segment-volume factor and

EVIDENCE FOR DUPLICITY OF VISION 71

the extrinsic summation-difference to retain any lead over the cones in
the matter of sensitivity. But when the rods are working to best advan-
tage, at intensities below the cone threshold, the intrinsic factor of their
rhodopsin content far outweighs the combined effect of the other two.
So important is rhodopsin in this regard, and so deeply involved in the
fundamental chemical events of the visual process itself, that a large part
of the first section of the next chapter will be devoted to this magic
chemical whose effect is: "Now you don't see anything; now you do!"

Evidence for Duplicity of Vision — Essentially, then, the Duplicity
Theory states that the retina contains a sensitivity mechanism and an
acuity mechanism, and identifies these with the rods and cones respec-
tively. If both of these mechanisms are in operation only through a

(log) Intensity Time In Darkness

Fig. 28 — ^Further evidence for the Duplicity Theory (see text).

certain transitional range of intensities, and only one or the other of
them can operate effectively below and above this range, we might ex-
pect that many phases of visual physiology would exhibit differences in
accordance with whether one, both, or the other mechanism were
in action. This is indeed the case. When graphs of various visual physi-
ological processes are plotted, a characteristic 'kink' is always to be seen
in the curve, marking the change-over from predominantly rod- to pre-
dominantly cone-control of the process in question. Moreover, when
such curves are plotted for stimuli restricted to the pure-cone (foveal)
portion of the human retina, or are plotted for animals with cone-sim-
plex retinas, there is no kink— the whole curve resembles the cone portion
of the graph of a rod-and-cone, duplex, retina. And of course pure-rod
retinae yield curves which lack kinks and simulate the below-the-kink
portion, or rod portion, of a duplex retina's graph.

72 THE VERTEBRATE RETINA

The kink is often sharper than we might expect it to be, if it repre-
sents a transition. It is accentuated — that is, the overlap of rod-func-
tioning into the physiological realm of the cones is reduced — by little-
understood phenomena of mutual inhibition of rods and cones. Circum-
stances which favor one of the mechanisms allow it somehow to sup-
press, partially, the activity of the other mechanism. Thus the rods or
cones of a 'pure' retina in some ways exceed in performance their
counterparts in a duplex retina.

When the rate of flashing of an intermittent light is speeded up, a
point is reached at which the successive impressions fuse and the light
appears to burn steadily. This 'critical frequency of fusion for flicker'
has been much studied in man and animals — in the latter by indirect
methods, of course, involving training or the recording of the electrical
discharges from the retina. The critical frequency increases with inten-
sity (strictly, with the logarithm of intensity — = Ferry-Porter law) . At
an intensity of 0.25lux— the cone threshold — the critical-frequency
curve of a duplex retina such as the human shows a kink (Fig. 27).
When colored lights are used, the effect of color on the critical frequency
begins to manifest itself only above the cone threshold, as would be
expected. With red light, there is no kink— the rods being insensitive to
deep red, however intense. Only the cone part of the flicker-fusion curve
is obtained from foveal stimulation; and, the farther peripherally the
area stimulated, the closer the whole curve simulates that part due to
the rods alone. A pure-cone retina, such as that of a turtle, gives a kink-
less curve. The pure-rod gecko has also been found to give a homogen-
eous curve — though the curve is that characteristic of cones, which
seems surprising until one takes into account the fact that the geckoes'
rods were secondarily derived from cones (see Fig. 25) .

Another visual phenomenon which plots a kinked curve is the thresh-
old of intensity discrimination. By this is meant the proportion by which
a light must be increased in intensity in order for it to be seen to have
brightened. The initial intensity being designated "I", the increment is
"dl". The curve of "I/dl" plotted against "I" (Fig. 27) shows a change
of slope, or kink, at the cone-threshold intensity. With only foveal
stimulation there is again no kink; nor is the rod part of the curve, or
any kink, obtained with red light.

Perfectly familiar to all is the increase of visual acuity with intensity
— so very commonly do we speak of a light as being "not bright enough
to read by." Less apparent is the existence of a kink in this relationship

EVIDENCE FOR DUPLICITY OF VISION 73

as well, with acuity rising more rapidly above the cone threshold than
below it in most animals (Fig. 28). If we knew very accurately this
relationship for pure-rod and pure-cone animals, we would expect to
find their curves of acuity-versus-intensity to be kinkless.

As a final illustration of the difference in behavior of rods and cones,
we shall consider the rate of dark adaptation, or increase in sensitivity
in darkness following exposure to bright light. The graph of this in-
crease (Fig. 28) again shows a fairly well-defined kink owing to the fact
that the cones reach their maximum sensitivity at a rapid rate before the
sensitivity of the rods begins, slowly, to increase at all. In pure-rod,
duplex, and pure-cone eyes the expected differences in the slope of the
curve, and in the presence or absence of a kink, are indeed found when
such criteria of sensitivity as the behavior of the pupil or the electrical
discharges from the retina are recorded.

We have surely seen enough evidence now to convince ourselves
of the duplicity of the visual process. The complexities of the above
evidence may seem rather appalling to the innocent reader; so, let us
try, in the next chapter, to make the process of vision seem fairly
simple after all!

Chapter 4

THE VISUAL PROCESS

(A) ScoTOPic Vision

Any attempt to depict the events which intervene between the impact
of Ught upon the retina and the registration, in consciousness, of the
quahtative and quantitative aspects of vision, must necessarily be largely
guess-work, and can be lucid and connected only if it is dogmatic. The
following treatment is such an attempt, made for the sake of the reader
rather than for the sake of the subject. The literature of the field of
visual physiology is vast and unorganized, and largely unreadable with-
out a considerable background of mathematics. Paraphrased sans mathe-
matics, it is bound to seem largely a series of unfounded generalizations
to any astute physiologist who may read it; but, these latter gentry have
yet to promulgate an inclusive theory of vision in which a sophomore
cannot pick great holes. In the present state of knowledge, one descrip-
tion of what goes on in vision is almost as good as another, and may be
the best one for the beginning reader if, at least, he is able to follow it
without miring down in equations.

Rhodopsin — Perhaps the greatest advance which has ever been made
in this field was the discovery of the photosensitivity of the rod pigment,
rhodopsin, by Boll in 1876, and the elucidation of most of its properties
by Kiihne in the years immediately following. But rhodopsin was at first
used to explain too much, and during its history many of its original
attributes have had to be taken away from it. Physiologists have relin-
quished their beliefs about rhodopsin most reluctantly, since the less one
can credit to it, the farther away seem the solutions of some of the
fundamental problems of vision. However, in very recent years some
progress has been made in the study of other photosensitive substances
in the retina, which may be found to do some of the things formerly
credited to rhodopsin itself.

Rhodopsin was once supposed to be the sine qua non of all of verte-
brate photoreception, and owing to the attention it commanded, photo-
chemical theories of vision rapidly came to be the only ones seriously
considered. But it was soon seen that if vision does have a strictly photo-

RHODOPSIN 75

chemical basis, no one photosensitive substance could be entirely respon-
sible for color vision — at least three such substances are required by the
long-popular Young-Helmholtz theory, and even more were demanded
by some other theories of color vision. Rhodopsin might be one of these
— but where were the others? The resuscitation of Schultze's ideas in
the form of the Duplicity Theory made it necessary to abandon rho-
dopsin as a color-vision photochemical, for it was finally made certain
that some vertebrates have none of it, and that it never occurs in cones.
Still, there were those who believed that vision as such — brightness-
vision both photopically and scotopically, apart from hue perception —
necessitated rhodopsin. These workers argued that there must be in-
visible traces of the substance in cones in order to account for their
light-sense; and this idea has been very long a-dying.

Rhodopsin is still widely regarded as the absolutely essential photo-
chemical substance for rod activity. Even this is an unnecessary belief,
since rhodopsin may be nothing more than a sensitizer, so powerful that
its action masks that of another, essential, material so completely that the
brightnesses of lights are directly related to their effects upon rhodopsin.

The substance is a reddish pigment whose chemical nature is not yet
completely known. It is released from the rod outer segment by sub-
stances which lower surface tension, such as bile salts, saponin, digitonin,
sodium oleate and salicylate, and snake venom. It forms a precipitate
with platinic chloride — an insoluble yellow compound which can be seen
in the rods in permanent microscopic preparations made of retinse which
are kept in darkness for an hour or so before preservation.

Rhodopsin is commonly described nowadays as a hydrocarbon con-
jugated with a protein, through a belief that vitamin A — essentially a
hydrocarbon — is an important constituent (r. /'.). The molecular weight
of rhodopsin is about 270,000. This and other features make it clear
that most of the molecule is proteinous; but of course to say that rho-
dopsin is essentially a protein is like saying that dynamite is essentially
fuller's earth. The business part of the molecule — its 'chromophoric'
(color-bearing) group — is neither a hydrocarbon nor a protein, though
it may be derived indirectly from a portion of the vitamin A molecule.
The latest information* is that the rhodopsin molecule contains a pro-
tein, 'provisual red', and probably a third substance. The chromophore,
provisual red, can be split into a fatty acid and 'visual red'; the latter in

'''Kindly supplied b>- Dr. Arlington C. Krause in advance of his own publication thereof.

76 THE VISUAL PROCESS

turn can be made to yield Visual yellow' and 'indicator yellow'. Certain
of these photosensitive substances have previously been identified as
partial-breakdown products of rhodopsin when it is struck by light.

The most important properties of rhodopsin are its intense colored-
ness, its sensitivity to all visible wavelengths excepting those deep red
ones which (by reflection from it) give it its own color, and the fact
that its response to these wavelengths is to disrupt into colorless or pallid
substances of little or no photosensitivity. It is most affected by the blue-
green region of the spectrum, centering at about A500m|l. One might
expect that this wavelength would appear brightest to the dark-adapted
eye in which rhodopsin has built up to a high concentration. Owing how-
ever to modifying factors (chief of which is believed to be the high
absorption of short-wave light in the ocular media), the brightest point
in the scotopic spectrum is shifted red- ward, to ?L510m[i. One of the two
or more substances into which rhodopsin is broken down by light is
presumed to irritate the protoplasm of the rod and cause a wave of
electrochemical activity, much like the impulses which flow along nerve
fibers, to pass down the rod foot-piece and stimulate the bipolar neuron.

Dark Adaptation — Rhodopsin is not as all-important as it was once
thought to be, but it is largely responsible for the ability of the rod to
'dark-adapt' or lower its threshold — until the amount of light needed to
stimulate it is a tiny part of that required to arouse a cone. While we are
in ordinary daylight there is believed to be but little rhodopsin in our
rods, for the concurrent processes of its synthesis and breakdown are
then in equilibrium at a sub-maximal concentration of the substance.
When we enter a dark place the process of adaptation to dim light
begins at once, since the breakdown all but ceases while the upbuilding
of new rhodopsin continues at the usual rate. In the dim light, a new
balance is struck at a high concentration of rhodopsin, so that a given
amount of additional light will now appear brighter than before, since it
destroys a greater absolute amount of the photosensitive pigment.

Rhodopsin is not quite the whole story in dark-adaptation, however.
The dilation of the pupil, upon going into a dim or dark place, admits
more light to the retina, so that the overall sensitivity of the eye in-
creases somewhat, apart from any change in the retina itself. In the latter,
the first step in dark adaptation is taken by the cones rather than the
rods, for the tiny amount of photosensitive material which they ever
contain is very quickly built up to a maximum (see right half of Fig. 28) .

DARK ADAPTATION 77

Then, too, a part of dark-adaptation — it is hard to say how much — is
accompUshed by switchboard effects in the integrative layers of the
retina, bringing about temporary hook-ups, to gangUon cells, of larger
numbers of visual cells than usual.

In dim light or darkness, the destruction of rhodopsin having largely
or wholly ceased, the new formation of the substance (partly from the
decomposition products still present in the rods, partly from new raw
material absorbed from the pigment epithelium) quickly restores the
concentration to a fairly high level. Within seven or eight minutes, in
fact, the previously depleted rod becomes capable of function. The rods
are now deeply colored and absorb much more of whatever light may
strike them, so that a strong impulse impinges upon the bipolar. Should
we now emerge into a bright place, the light would dazzle us uncomfort-
ably until enough rhodopsin had been destroyed to raise the thresholds
of the rods considerably. This process takes a much larger fraction of
a second than is required for the pupil to constrict. So, the removal of
some of the rhodopsin is the controlling factor in /zg/?/-adaptation —
which we might loosely define as the destruction of excessive sensitivity.
The pupil slowly reopens as the sensitivity of the retina is decreased, and
attains a final 'physiological size' appropriate to the particular species of
animal, and which for man is maintained in all intensities between 100
and lOOOlux — the range within which, presumably, an equilibrium can
be maintained in the photochemical system of the visual cells.

Rhodopsin accumulates to a considerable proportion of its maximum
in half an hour and is almost at maximum in an hour; but it continues
to form slowly for twenty-four hours or more. If anything essential for
its manufacture is deficient in the individual or in his diet, the rate of
formation will be greatly retarded, and the greatest amount ever formed
will be much less than normal. This condition of deficiency leads to
nyctalopia or night-blindness, in which dark-adaptation is incomplete
and the individual feels the handicap when trying to make his way about
in dim places and at night. He may become a menace to his fellows if
he drives an automobile at night and meets many bright headlights
which assault the little rhodopsin he is able to form. In the armies of
years ago, night-blindness — common under conditions of malnutrition —
automatically exempted a soldier from nocturnal guard duty. In modern
warfare, the night-blind individual is particularly useless in defense
against nocturnal bombing, and every effort is made to maintain a high
concentration of rhodopsin in the retinae of night fighter aircraftsmen.

78 THE VISUAL PROCESS

The substance whose lack is the usual cause of nyctalopia was shown
in 1925 to be vitamin A, a colorless material manufactured in the liver
from carotene, a reddish plant pigment. Although there are types of
nyctalopia which are hereditary, and the condition also occurs as a symp-
tom of degenerative retinal diseases, in its various degrees it is usually
the first detectible sign of vitamin A deficiency. Nutritionists and pedia-
tricians are consequently much interested in attempts to devise clinical
tests— by which they mean quick and easy ones — for nyctalopia; but
for various reasons a reliable test which is really simple seems hardly
possible, and the literature of the subject reveals more and more pessi-
mistic statements.

Soon after 1925, the obvious conclusion was drawn that vitamin A
is the precursor of rhodopsin, that it is actually converted into that
substance, and may be formed again when rhodopsin is disrupted by
light. Elaborate diagrams of this closed circuit, with the supposed
intermediate compounds, are commonly seen in print. But the most
recent and careful chemical studies of rhodopsin itself (r. s) have great-
ly weakened our faith in a direct genetic relationship between it and
vitamin A. All that can be safely said at the moment is that the vitamin
is essential for the synthesis of rhodopsin, probably as a minor contrib-
utor rather than as a principal raw material.

Rhodopsin may be the essential, the one and only photochemical sub-
stance that is ever present in rods, but there is no proof that this is
so. There are rods which contain none, though perhaps in all of these
{e.g., in Sphenodon, Xantusia, Phyllorhynchus) the lack of rhodopsin
is owing to these rods' having had relatively recent origin from cones.
They presumably get along perfectly well with the photochemical system
inherited from their cone ancestors — for all anyone knows at present,
the complete color-vision mechanism may still be functioning in them.
The photochemical substance or substances in cones may indeed have
chemical kinship with rhodopsin, for it has recently been reported that
the dark-adaptibility of the cones (which in terms of intensity-limit ratios
is actually about equal to that of the rods) is influenced by the dietary
intake of vitamin A.

Just a few years ago, it was being claimed by the Finnish retinal
physiologists associated with Ragnar Granit that when a rat retina has
been so brightly illuminated that all of the rhodopsin is bleached, the
optic nerve no longer carries the electrical discharges which can normallv
be detected in it during photic stimulation of the retina. This was hailed

ROD VISION 79

as proving conclusively the complete dependence of rod vision upon rho-
dopsin. But workers in the same laboratory have more lately obtained
puzzling indications that very little rhodopsin is ever normally bleached
in the intact animal. They found apparently normal amounts of it in
eyes whose electrical responses had been reduced one-third to one-half
by stimulation with light. Possibly the electrical responses would entirely
disappear while there was still a great deal of rhodopsin in the rods.
This might be new evidence that rhodopsin is a secondary sensitizer
rather than a primary photosensitive material, or it might only mean
that switchboard effects in the retina are more important in light-adapta-
tion than we have been supposing.

Whatever its whole meaning may be, rhodopsin was a clever invention;
for its light-absorbing power makes it responsive to weak light, yet it
conveniently bleaches when, in bright light, the full amount of it would
greatly handicap the animal. Even the particular color it possesses is in
itself adaptive, as will be elucidated later (Chapter 12, section A).
So elaborate a substance could hardly have been present in the 'original'
provertebrate visual cell, which must then have been high-threshold, more
like the cones we know than like a modern rod. Some of the photosensi-
tive ancestor-cells of the rods and cones were left behind in the brain
lining when the eyes evolved, as will be brought out in the next chapter.
These, though sensitive enough to respond to light through the entire
wall of a bird's head (as shown by their reflex control of spermatogenic
activity), contain no rhodopsin as far as we know. If the modern rod
cell depends utterly upon rhodopsin for its photosensitivity as such, it
has come to do so secondarily by discarding some more ancient photo-
chemical for want of efficiency under scotopic conditions.

Rod Vision — We may conceive of the peripheral (ocular) portion of
the rod visual process as taking place somewhat as follows : At the start
of adaptation to dim light there is little rhodopsin in the rods, and so
little of this is broken down by the weak light that only feeble impulses
pass down the foot-pieces. As the amount of rhodopsin increases, a
greater absolute amount is broken down by a given light and the im-
pulses become stronger. Those bipolars with which the largest numbers
of rods connect now receive enough total stimulation to be set off into
conductive activity, and they begin to carry nerve impulses at a certain
low frequency of discharge — each bipolar acting somewhat like a reser-
voir and, so to say, filling up with stimulation and discharging an im-

80 THE VISUAL PROCESS

pulse, the frequency of discharge thus bearing a relation to the amount
of stimulation.

The attached ganglion cells now behave similarly and conduct in
synchrony with the activity in the bipolars. The electrical aspect of their
discharges can be picked up in the optic nerve as action currents
with proper amplifying and recording devices. In the brain, a sensation
of light is now aroused whose strength depends upon the resultant of
the number of active nerve fibers and their frequency of discharge. As
dark-adaptation proceeds further, the number of rods per unit area of
the retina whose activity actually registers in consciousness steadily in-
creases, due to the activation of more and more bipolars having smaller
and smaller numbers of associated rods. As the mosaic of functional
receptor units becomes more and more dense, visual acuity rises hand in
hand with the rise in the strength of the brightness sensation. When
dark-adaptation is complete, both visual acuity and brightness are max-
imal for the intensity being supplied, and any further increase in either
will depend upon an increase of illumination above the threshold of the
cones, thus bringing the latter into play. The destruction of rhodopsin
may then increase to such an extent that the brightness would decrease
in the face of increasing objective intensity — in other words, light adap-
tation would have commenced. Incidentally, rising intensities above the
cone thresholds naturally bring into action more and more cone bipolars
and associated ganglion cells, so that visual acuity continues to rise until
all elements are functioning. Beyond this point, further increase of in-
tensity brings no additional visual acuity — though of course brightness
can increase until all involved optic nerve fibers are discharging into
the central nervous system at their maximum rates.

If, with the retina thoroughly dark-adapted, it is now subjected to
bright light, rhodopsin is immediately broken down in large amounts in
all of the rods which are receiving stimulation, and all of their associated
nerve fibers begin to conduct at high frequency. As the rhodopsin fades,
however, the rod thresholds rise and the frequency falls off. As the rod
thresholds approach those of the cones, a comfortable brightness is
attained with the pupil now reopened, and with the rods perhaps still
all in action, contributing all that they ever can to the resolving power
of the retina — considering that they are of course still summated. In
comfortable illuminations above the cone threshold, however, the cones
are contributing only a part of their potential resolving power, which
becomes maximal only at intensities above 100 lux.

CONE VISION; COLOR 81

(B) Photopic Vision

Cone Vision — Turning now to the cones, we are confronted with the
complex matter of color vision — assuming for the nonce that all cone-
bearing vertebrates do discriminate hues. We can imagine subtracting
color vision from the whole performance of the cone — but what we
would have left, we could describe in terms of a rod mechanism that
had little summation and very little rhodopsin. So, we cannot well avoid
considering the elementary and purely qualitative aspects of color vision
if we are to attempt to picture the mechanism involved and thus round
out our survey of visual physiology.

Color — Color, or better, 'hue', exists only in the mind. No light or
object in nature has hue — rather, the quality of hue aroused as a sen-y
sation is projected back to the object as one of its attributes, just as the
patterns of brightness and darkness in consciousness are projected back
into the visual field to endow objects with their size, shape, tone values,
and movement. For, we perceive objects rather than lights. We can
see objects falsely as to size, shape, and motion, and just as falsely as
to color since color is purely subjective. The color of a surface depends
not only upon its chemico-physical nature, but also upon the kind of
light by which we see it, and upon our memory of the impression it
may have given us under some more familiar illumination. Thus, a par-
ticular dress may look red only in daylight, yet we still call it red under
an artificial light when it may actually be reflecting more yellow light
and should then be seen as orange.

The hue sensation aroused by a light depends primarily upon the
frequency of its vibration, usually expressed as the distance between
successive waves in the vibration, the wavelength. The longest visible
wavelengths, in the neighborhood of 760m|,i, arouse the sensation we call
red; the shortest ones, around 390m[l, give us the sensation of violet,
which must be seen in a spectroscope to be appreciated (since the violets
of textiles and pigments in general are not true violets, but diluted pur-
ples). In-between wavelengths give us the other hues of the spectrum.

When all of the visible wavelengths are being received on the same
area of the retina, either simultaneously or in such rapid succession that
their physiological images persist long enough to overlap or fuse, we see
what we call white light. The removal of some wavelengths from the full
assortment makes the remainder of the light appear, collectively, as a
color. Such a removal may be effected by selective reflection or by selec-

82

THE VISUAL PROCESS

tive transmission. An opaque colored paper or cloth performs the former,
a translucent colored glass or liquid performs both. A colored object is
colored, instead of gray, because it absorbs some wavelengths and reflects
or transmits others. The latter being the ones which reach the eye, they
determine the color of the object. If the object is specially illuminated
only by wavelengths which it can absorb, it can reflect none of them and
will then appear black. An object which in sunlight appears black must,

g yor

Fig. 29 — The physical and psychological spectra.

a, the visible spectrum as formed by a prism.

V- violet; b- blue; g- green; y- yellow; o- orange; r- red.

b, the psychological color circle. Red and violet intergrade through purple; diametrically
opposite hues are complementaries, and make white when mixed in correa amounts.

c, the linear spectrum formed by a lens. The distance from the focus of violet to that of
red (greatly exaggerated in the diagram) is the 'linear chromatic aberration' of the lens.

then, be one which absorbs all wavelengths, just as white objects, to ap-
pear white, must reflect all. Of course no object absorbs or reflects all of
the light striking it. Whether it reflects all wavelengths equally, or some
more^han others, it reflects only a certain percentage of the light energy.
This percentage is the object's reflection coefficient or 'albedo'.

No object can reflect only a single wavelength, and hence no object
Y" can have a pure color. To obtain pure colors, we must select them from a

COLOR 83

band spectrum by means of a slotted diaphragm. Such a spectrum is
formed automatically when a mixture of wavelengths, such as sunlight, is
passed through a narrow slit and then through a prism. Since the refrac-
tive index of the glass is different for each wavelength, being highest for
violet and lowest for red, the colors are sorted out of the mixture and
can be caught on a screen, all in order, as a spectrum (Fig. 29a). If
the light reflected or transmitted by a colored object is concentrated and
passed through a prism, the spectrum formed will naturally have lightless
regions in it corresponding to the wavelengths whose removal from the
sunlight, through absorption by the object, gave the latter its color. Such
a spectrum is an 'absorption spectrum', and is the basis of spectral anal-
ysis, that powerful weapon of chemistry and astronomy with which sub-
stances are detected by means of their specific fingerprints on sunlight.

With a little practise, a normal person can learn to distinguish about
one hundred and sixty distinct hues in the sunlight spectrum.* If we now
let any two of these hues escape through narrow slits and aim them with
mirrors at the same piece of paper or ground glass, or look at one with
each eye, or present them in rapid alternation to one or both eyes, we
will obtain a sensation different from that given by either hue alone.
In most cases, the sensation will be that afforded by some other pure
hue, lying between the chosen two in the spectrum. If however the latter
are far apart in the spectrum, and lie diametrically opposite each other
on the 'color circle' (Fig. 29b), they are 'complementaries' and their
mixture will produce white light. Thus any hue in the spectrum (and
white) can be produced by mixtures, made by one means or other, of some
two other hues. Some white light may need to be added to the spectral
hue in order to make it an exact match for the mixture. We are not of
course discussing here the subtractive mixtures which one obtains by stir-
ring pigments together — the artist's complementary, primary, and second-
ary colors have nothing to do directly with those of the physiologist.

The physiologist often terms red, green, and violet 'primary' colors,
because in none of them can any other hues be seen. Yellow is also con-
sidered a primary by psychologists, as is blue for that matter. Yellow
sensations can be produced by means of simple apparatus which presents
red to one eye and green to the other, but yellow is not reddish green or
greenish red. Yellow, in this instance, is obviously synthesized in the

'''Actually, 160 complexes of hue-plus-whiteness. No one has ever yet determined the (much
smaller) number of hues which would still be discriminable, were saturation eliminated
as a variable.

84 THE VISUAL PROCESS

brain — probably also, as we shall see, even when it is excited monocularly
by monochromatic yellow spectral light. We can, if we like, make an
artificial distinction among the psychological primaries, between those
which can be easily produced by mixtures and those which cannot; but
even red and violet, though at the ends of the spectrum, can be produced
by mixtures. The spectrum really has no ends — it only seems to have,
due to the way in which a prism forms it. Really, it is a closed entity, for
red and violet are adjacent, psychologically — their mixture results in
purple, which lies outside the spectrum but fills the gap between red and
violet in a spectrum which we might imagine bent into a ring (Fig. 29b).

Though the primaries can all be synthesized, they cannot be analyzed
— which is what makes them primaries. In orange one can discern both
the red and yellow components; in purple, the blue and red. But though
blue can be made by mixing green and violet, it does not look as though
it contained either. Yellow and violet, and red and green, are sometimes
called 'disappearing color pairs', since when the members of such a pair
are mixed, neither member can be seen in the mixture.

The mixture of three properly chosen primaries (the most convenient
are red, green, and violet — and these three do have, in a certain way,
an edge on the other two chief primaries, yellow and blue) arouses the
colorless sensation of white or gray, which is also afforded by mixed
complementary pairs of colors such as orange and green-blue, green-
yellow and violet, red and blue-green, etc. In each such pair it can always
be noted that at least one member is not a simple color or primary; and
the two members, between them, always contain red, green, and violet or
can be matched by mixtures of them in pairs. The complement of any
hue can also, obviously, consist of white light minus that hue. A mixture
may be complemented by a pure hue, and the latter by one other pure
hue, by simple or complex mixtures, or by white minus the first pure hue.

Saturation — The whole of the sensation aroused by a colored light or
object has aspects other than hue itself. It has brightness of course, the
psychological counterpart of physical intensity as with achromatic stim-
uli; and it has saturation. Saturation means coloredness as apart from
color, and quite apart from brightness. In a darkroom we could aim,
at the same ground-glass, a beam of pure colored light and a beam of
white light. The ratio of color to white in the resulting spot of light
would be the measure of its saturation. With more white added, the
saturation would go down and the brightness would go up; but instead

SATURATION 85

of simply adding more white light, we could add some white and sub-
tract some colored light, and thus lower the saturation while keeping
the total brightness constant. Again, we could reduce the amount of
colored light without adding extra white, and thus reduce both satura-
tion and brightness. Thus it can be seen that the saturation of a colored
light has nothing to do with the particular hue involved, and is also
quite independent of the brightness.

There are two chief ways in which saturation and unsaturation may
be manifested. Firstly, saturation can represent the extent to which a
spectral color is free from objective adulteration with white light, or the
extent to which a pigmentary color is devoid of admixture with white.
Unsaturation of a colored light-beam by mixture with a white beam has
been mentioned above. A paper- or cloth-color which reflects much light
throughout the spectrum in addition to the strong band of wavelengths
which gives it its hue, is a 'tint' of that hue — unsaturated by the white
it reflects. An artist, mixing Chinese White with an oil color, is un-
saturating that color. Likewise, pigmentary colors may be apparently
unsaturated by mingling them with black, thus yielding 'shades' of their
colors. Admixture with black is really, however, not true unsaturation
but is more nearly tantamount to simply reducing intensity and therefore
brightness — it is like mixing a light-beam with darkness, which would
not unsaturate it even if it could be done! Psychologically, admixture
with black is not quite equivalent to reducing intensity, for blackness
and darkness are not psychologically identical. Brown, for example, is
a black-adulterated color which can be seen as brown only when the
conditions are right for seeing black. In a darkroom, a brown area which
is not surrounded by lighter areas appears simply as weakly orange or
reddish, for the blackness element of the brown becomes mere darkness.
If blackness is 'induced' in an orange area by surrounding the latter with
white in a darkroom, one can obtain the sensation of brown without
resort to pigments, for the orange spot in question need not be pig-
mentary — it can be formed by filtered or spectral light.

It is important, in thinking about saturation, to keep one's attention
upon the amount of color, the 'chroma', present — not upon the character
of the unsaturating factor present, for this does not matter. It need not
even be whiteness which unsaturates, for, if we wish, we may speak of
unsaturating a hue with another hue, and thus think of orange as a red
unsaturated with yellow; but this is more than a little dangerous since

86 THE VISUAL PROCESS

SO many mixed pairs of colors produce sensations which are not analyz-
able blends of their qualities, but entirely new qualities.

Apart from the kind of unsaturation which may be produced syn-
thetically so to speak, by mixing into a color some whiteness from a
separate source entirely outside the color, there is a type of unsaturation
which is inherent in the colored light itself, even in a spectral light of
whatever purity. It is as though the monochromatic spectral beam con-
tained some white light which we could not remove. This kind of un-
saturation is due to the fact that the visual mechanism for the perception
of white is set in operation to some extent by any one wavelength — to a
greater extent by some than by others. If we look at a solar spectrum,
the yellow region (about A,580m[i,) looks brightest to us, and also looks
the least richly colored. We can separate this pallidity of yellow from
its high brightness, by turning to a spectrum in which each wavelength
represents the same amount of energy. In such a spectrum, the yellow-
green region (around A<557m[x) is now the brightest; but the yellow still
seems the least colored color, the richness of the chromas increasing from
it toward both ends of the spectrum.

This kind of unsaturation, or low chroma, is particularly important
physiologically and psychologically. It greatly influences the results of
color-mixtures, for the saturation of mixtures is always low. If for exam-
ple we mix red and green to make yellow, the yellow we obtain is of
low saturation as compared even with spectral yellow, and to spectral
yellow we must add some white light to make a perfect match with the
red-green mixture. The more complex a mixture, the lower the satura-
tion, for we are approaching the result of mixing all wavelengths — which
is, of course, white itself, with the chroma-content at zero.

The degree of saturation of a spectral light can be ascertained by
determining how much of it, added to white, will give that white a hint
of chroma. By such means, red and particularly violet are revealed as
highly-saturated wavelengths, yellow and green as being of low chroma.
We therefore say that the 'white valence' of yellow is high, by which we
mean that we can add yellow to another color without altering the hue
much more than if we had added the same amount of white. Red or
blue, added bit by bit to another color, have more prompt effects upon its
appearance — they have a low white valence, cannot take the place of
very much white in mixtures.

Recalling that unsaturation is usually accomplished by actual objective
admixture with white, we can now see that when the degrees of unsatura-

BRIGHTNESS; THE PURKINJE PHENOMENON

87

tion of two 'pure' hues are compared, we are really comparing their
intrinsic subjective white-sensation-arousing power, their white valences,
or their nearness to whiteness. Yellow is not white, but it is more like
white than red is, because yellow stimuli more effectively stimulate the
whole white-seeing mechanism of the cones and their central connections.

Brightness and the Purkinje Phenomenon — Brightness has the
same meaning in cone-mediated sensations that it has in achromatic rod
sensations, and is just as independent of actual physical intensity. But

THE PURKINJE PHENOMENON
Dark Adaptation Produces

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Fig. 30 — Graphic depiction of the changes which comprise the Purkinje phenomenon.

the relation of brightness to intensity is different for the cone- and rod-
mechanisms. While the brightest part of an equal-energy spectrum is the
yellow-green for the cones, it is in the green for the dark-adapted, func-
tionally pure-rod eye. This shift results in a change in the relative bright-
nesses of colored objects as intensity drops below the cone threshold or
rises above it. This change is the 'Purkinje phenomenon', which is simply
a betrayal of the change-over from predominantly cone vision to rod
vision (Fig. 30; and see Fig, 35, p. 102). It naturally occurs only in
duplex retinae, or duplex retinal areas, and its occurrence is a part of the
great mass of evidence for the Duplicity Theory.

88 THE VISUAL PROCESS

It is only by coincidence that the Purkinje shift has the particular
extent that it has, in any given retina. The luminosity maxima of the
scotopic and photopic spectra might just as well happen to be farther
apart in wavelength, or closer together; or even, by chance, identical,
for they are determined by very different factors. In the one case, the
maximum is determined by the maximum of absorption of rhodopsin —
in the other case, by the peak in the resultant absorption spectrum of
the photochemical substances in the cones. In some animal with a rho-
dopsin of slightly different color, and with a slightly different color-
vision system, the Purkinje shift might be much greater or much less
than in man — or could conceivably be absent (or even might take place
in the opposite direction, though no such case is known.)
f Trichromatic Vision — The fundamental qualities of cone-mediated
sensations, then, are hue, saturation, and brightness. At least a part of
the whole process by which these qualities are established in conscious-
ness is essentially physiological. A part of the process is psychological.
It would be very nice, considering the avowed scope of this book, if we
could carry our treatment of cone vision just to the boundary line and
stop. But unfortunately there is no branch of psycho-physiology in which
it is more difficult to say where more-or-less 'physiological' sensation ends
and strictly 'psychological' perception begins. Some hues, such as red,
green, and violet, appear to be simple sensations. Others, like orange
and yellow-green, are mixtures analogous to the sour-sweetness of lemon-
ade or to a chord in music — trained observers can always discriminate
the separate elements of the complex. But then there are hues, pure
yellow and pure blue, which seem to be more like percepts than sensa-
tions, for each is the product of two simultaneously-evoked sensation
elements, yet cannot be analyzed into those elements. Here, the sum
differs from its parts in a qualitative manner — it is as though when we
hybridized horses with zebras, the offspring were always giraffes!

Since the sensations of all hues and white can be aroused by appro-
priate mixtures of three wavelengths — primaries — chosen from the ends
and middle of the spectrum, normal human vision is said to be trichrom-
atic (tri = three) . It was an eighteenth-century French printer, LeBlond,
who discovered (through a misinterpretation of Newton's writings) that
with only seven colored inks, and black, he could print pictures contain-
ing the whole gamut of colors theretofore obtainable only with a legion
of inks. Being a very economical person, LeBlond experimented further
and found that he could get along with only three colored inks. Thomas

TRICHROMATIC VISION 89

Young formulated a theory of color-vision based upon LeBlond's find-
ings, in which he proposed three sets of receptors in the retina, each
most sensitive to one of three primary colors. Sensations of non-primary
colors were regarded as due to the simultaneous enaction, to varying
extents, of two or all three sets of receptors. Whiteness was due to the
equal stimulation of all three.

Much support for this three-component theory of color vision was
given by Helmholtz in the last century, and nowadays the theory goes
under the hyphenated names of the two men. The Young-Helmholtz
theory calls for three 'somethings' in color vision; but ideas have
changed, from time to time, as to what these somethings are. Young
thought of them as three kinds of nerve endings. Helmholtz thought of
them as three photochemical substances or processes, which he at first
believed to be in three separate sets of cones. Later, he considered that
they probably all occurred in each cone.

Other theorists have complicated matters considerably and, in the
light of the most recent developments, unnecessarily. The perception of
yellow, white, and black formerly gave much trouble and seemed to call
for a minimum of four components in cone vision, as in the theory of
Hering, the principal rival of that of Young and Helmholtz. The binoc-
ular fusibility of red and green into yellow, and the modern concept of
the difference between blackness and darkness as being due wholly to con-
trast, makes the assumption of more than three components unnecessary.

It is entirely likely that the three processes are mediated through each
and every cone. White stimuli do not take on hue when made very small
in area, as we should expect them to do if they then struck only one or
two out of a total of three or more kinds of cones. Again, if there were
three kinds of cones with respect to color sensitivity, visual acuity would
necessarily be very low in a monochromatic illumination which effec-
tively stimulated only one-third of the cones. But visual acuity is not
lower in any monochromatic light (except, perhaps, red) than it is in
white light of equal objective or subjective intensity; and in some such
lights it is even higher. This could mean, as Hecht claims, that all the
cone-types respond nearly equally to any given monochromatic light.
It can also mean that the cones are all alike — at least in any given small
retinal area. They may vary progressively along meridians of the retina,
for the number of hues we can discriminate diminishes from the center
toward the ora terminalis, unless the intensity is very high. Even this
'deficiency' may really have its basis far from the cones themselves.

90 THE VISUAL PROCESS

Binocular color mixture has been mentioned above, in the instance of
the binocular fusion of red and green into yellow. Its existence is fatal
to any theory which places the color-vision mechanism entirely in the
periphery of the visual apparatus — that is, in the retina. There is no
color-sensation, which can be produced by mixing two lights in one eye,
that cannot be duplicated by supplying the two lights, independently,
one to each eye. If color-mixture can be made centrally, one wonders
whether all color-mixtures, even monocular ones, may not always be syn-
thesized centrally. To suppose so necessitates believing that the optic
nerve fibers can simultaneously carry several separate 'primary' kinds
of information, which are integrated into a perceptual whole only after
reaching some level in the central visual apparatus. To account for
binocular color-mixture (and, it can be allowed to account also for
monocular mixture) a multiple synthetic mechanism must exist centrally.
But it would seem difficult for any one photochemical substance in the
cone to be able to give rise to more than one kind of optic nerve impulse.
To account for the transmission of simple primary impulses along the
optic nerve, when the retina is being illuminated by such a mixture as
purple, there must also be a multiple, differentially responsive analytical
mechanism in the periphery.

The binocular synthesis of mixed colors and white results in sensa-
tions identical with those aroused monocularly by the same stimuli. One
reason for this could be that the vision of even one eye by itself is
actually carried out through the binocular (fusion) 'center'. This sounds
roundabout and improbable, but there is considerable evidence for it.
It is difficult to explain otherwise why things look no brighter to us
when seen with two eyes than with only one. The functioning of one eye
can affect the way things are seen with the other eye. To give only one
example: the convergence of a shielded eye causes an apparent lateral
movement of a spot of light seen, in a darkroom, only by the other eye
— especially when the non-seeing eye happens to be the individual's
master or dominant eye. The brain is so accustomed to ascribing most
of vision to the dominant eye, that it can be deceived into supposing
that eye to be seeing even when it is not, and thus 'sees' the spot of light
move in just the way it would have to, to remain visible to the dominant
eye during the latter's rotation. The brain is confused as to which eye
is seeing what, which could only be possible if the two eyes always
formed a team even when only one member of the team works.

TRICHROMATIC VISION 91

The manner in which a mixed color, for instance purple, may be seen
by one eye (or both) presented with purple, or with one eye offered red
and the other violet, is diagrammed in Figure 31. The purple stimulus
in 'a' may of course be steady, or may consist of rapid alternations of
red and violet lights; for, as mentioned earlier, fusion of colors may
occur temporally as well as spatially. When purple strikes a single retina,
impulses somehow tagged 'redness' and 'violetness' pass along the optic
nerve to be combined into 'purpleness' by the same central machinery
that makes purpleness out of redness from one eye and violetness from
the other. In the retina, then, there is some analytical mechanism, two
separate parts of which respond independently to the short and long
wavelengths in the purple light. We suppose the whole of this analytical
mechanism to be a group of (three) photochemical substances.

Left Eye

Right Eye Left Eye

I (none) I ■• — stimulus — - 1 red

i \ peripheral
\ \ analysis '

Right Eye

central synthesis -—>
binocular- mix lure locus
consciousness

Fig. 3 1 — Perception of a compound color : purple.

a, monocularly (or, a purple stimulus might be supplied to each eye), b, by binocular
mixture of red and violet. The inactive components of the visual system are labelled in
faint lettering — all components would of course be active in the perception of the all-
inclusive compound white.

Central Events in Trichromatic Vision — When the dark-adapted
eye is presented with an equal-energy spectrum, that spectrum appears
colorless (some say, faintly violet) but not homogeneous. At the locus
of wavelength 510m[X the spectrum is maximally bright, the luminosity
falling off toward the ends and becoming zero, at the long-wave end,
at a point corresponding to the orange-red of the photopic spectrum.
Konig and Trendelenburg, around the turn of the century, established

92 THE VISUAL PROCESS

between them the practical identity of this 'scotopic brightness curve'
with that of the photopic totally color-blind eye, the absorption spectrum
of rhodopsin, and the curve of the rhodopsin-bleaching power of mono-
chromatic lights (Fig. 33, c/. Fig. 35). The rods are completely insen-
sitive to deep red because rhodopsin absorbs nothing beyond X650mp,,
and they are most sensitive to green because this kind of light is more
avidly absorbed by rhodopsin than any other.

As the intensity of the spectrum is now increased, there is a range of
intensity — called the photochromatic interval — within which the spec-
trum remains colorless. This interval is not the same for all regions.
For red, it is of course non-existent, for as soon as wavelengths longer
than 650m|X are seen at all they are seen by cones, and are seen as red
light. In succession toward the violet end, the other hues appear as the
thresholds of the cones for them are crossed. The now fully colored
spectrum has its brightest part moved (the Purkinje shift) to around
A557m[X, and extends from A,390m^ to ^760m^l. Beyond A,650m|X lies
the pure red. At A,600m[l is orange. The exact center of yellow is at
A,582m^, of green at A,515m[X, of blue at A,476m[X. Beyond the indigo
of X424-455m[i lies the true violet (see Table I, p. 4).

In the neighborhood of yellow and blue the change in hue for a given
change in wavelength is greatest. To be exact, the two maxima lie at
A,580mp, and A,490m(l. Around these values, we can discriminate more
different hues, closer together in the spectrum, than we can elsewhere.
This is because these wavelengths are maxima in the graph of the in-
trinsic pallidity or tinsaturation of the spectrum: as we pass from one
side of such a maximum through it to the other side, the appearance of
the stimulus changes rapidly with a change in wavelength because the
ratio of chroma to whiteness in the sensation is changing so rapidly.

The blue maximum, and the minor peak of brightness in this region,
may be lowered somewhat by absorption in the yellow pigment of the
macula lutea of the retina (see Chapter 8, section D) . As the intensity
is raised however, yellow and blue stand out more and more. The hues
on either side of each of these actually change, gravitating toward which-
ever of the two is the nearer — that is, yellow and blue appear to spread
more widely in the spectrum at the expense of their neighbors, until at
very high intensities yellow and blue alone, greatly unsaturated, fill up
the whole spectrum. At dazzling intensities even these lose all chroma
and a sensation of whiteness is then evoked by any visible wavelength.

TRICHROMATIC VISION 93

Yellow and blue thus appear unique in some respect. We shall see
other aspects of their peculiarity shortly. It is important to note here
only the fact that hue can be influenced by intensity. Apparently when
the visual mechanism is being overworked, either its peripheral analytic
or its central synthetic portion breaks down. We can change the hues
that 'go with' particular wavelengths in still another way : by fatiguing
the reception of a part of the spectrum we can make white light appear
to consist only of the remainder of the spectrum, as in the production of
'complementary after-images'. More important, we can fatigue the syn-
thetic mechanism itself, for if we stare for a time at a light which repre-
sents white-minus-red, and then look into a spectroscope, we will see not
only the red where it 'belongs', but will see nearly the whole spectrum
as red; and where there is no red (at the short-wave end) there is only
darkness.* In the same way, green or violet can be made to spread out
and fill almost the entirety of the spectrum, but yellow and blue cannot
be made to do so. No better confirmation of our choice of red, green
and violet as primary stimuli could be desired.

This phenomenon shows beyond question that whatever the three
somethings may be which comprise the color-vision mechanism, each one
of them has some responsiveness for practically all visible wavelengths.
The results of fatiguing with colors show also that if each one of the
somethings could be isolated and made to act all alone, its action would
be to arouse a sensation of its appropriate primary hue, no matter what
wavelength of light happened to activate it. Most of the 160-odd sep-
arate qualities we can experience, then, must be due to the instigation,
by single wavelengths, of combined actions of the three processes, no one
of which alone could give us more than a single, primary, hue sensation.

A rough idea of these combined actions is given by Figure 32. Each of
the three colored curves represents the spectrum of responsiveness of one
of the three central processes which synthesize our hue qualities, and the
color of the line indicates the quality it arouses when allowed to act
singly. When the redness and green-ness processes are equally active,
the quality 'yellowness' results. When the green-ness and violet-ness

*The Ericksons have recently reported experiments which suggest that all 'fatiguing" for
color may be central, rather than upon a peripheral exhaustion-of-photochemicals basis.
Their hypnotized subjects 'saw' the proper complementary after-image colors after having
had hallucinatory initial color-stimuli suggested to them; and these were persons who, in
the waking state, did not know that there is such a thing as an after-image — let alone,
that it should be experted to be complementary to the stimulus!

94

THE VISUAL PROCESS

N0liVSN3S dO 3anilN9V^

TRICHROMATIC VISION 95

processes are equal, the resulting sensation is 'blue'. When all three are
equally activated (which of course cannot be brought about by any one
wavelength) 'white' results.

At any one wavelength the ordinate, or height of the curves, has a
heavy portion where it lies below all three curves. This represents equal
amounts of activity of all three processes, and so represents the white
valence, or unsaturating whiteness-component, of the sensation aroused
by that wavelength. It needs of course to be given triple weight in any
estimation of the relative whiteness- and chroma-contents of the various
color sensations — their degrees of saturation. Above the triple line, the
remainder of the ordinate represents chroma. The part of it which lies
under two curves, taken twice, represents equal joint action of the pro-
cesses represented by the two uppermost curves. At ?.582m(X for example,
the two uppermost curves cross and these processes are therefore equally
aroused, yielding the compound sensation of yellow, diluted by a great
deal of whiteness indicated by the heavy part of the ordinate lying
below all three curves. Near the ends of the spectrum all of the ordinate
represents chroma, which is another way of saying that these wave-
lengths are seen with complete saturation.

The unique character of yellow is now readily comprehensible from
the graph. It results from the equal action of two processes which singly
would yield respectively redness and green-ness, neither of which can
be seen in yellow. Blue has a similar mode of origin — it is the unpre-
dictable giraffe progeny of the horse of green and the zebra of violet.
All of the sensation-qualities of mixed character except yellow and blue
owe themselves to simpler blendings of sensation-components which, as
with purple and orange, can still be discerned in the blend. The very
names we use for mixed colors — bluish-red, reddish-yellow, and so forth
— emphasize the simple character of their mixtures. On the other hand,
no one would ever call yellow 'reddish-green', or blue 'greenish-violet' —
and yet, in their genesis, that is what they are.

Let us consider just one of these mixed colors whose whole is merely
the sum of its parts: orange. It will serve to exemplify the manner in
which all such mixed colors are registered. At wavelength 600m [i in
Figure 32, it will be seen that the double portion of the ordinate below
the curve of the green-process is only half as tall as the part between the
green and the red curves. But this part which is under the green curve
is under the red curve as well, and hence is to be 'taken twice'. More-
over, it represents equal contributions of redness and green-ness to the

96 THE VISUAL PROCESS

whole sensation aroused by X600m|i — that is, a certain amount of yellow-
ness. An equal amount of uncancelled redness still remains — the chroma
ordinate above the green curve, taken once as to weight in the equation.
At X600m|l, then, the interaction of the three processes produces a large
amount of whiteness and equal amounts of yellowness and redness. Such
a blend, we see as orange.

Before we leave Figure 32 its representation of relative brightness and
saturation need brief consideration. Brightness is most easily disposed
of — as the reader has already gathered, it is represented by the total
height of the variously-weighted portions of the ordinate. If each ordin-
ate were drawn upward like an unfolding telescope to its 'true' height,
the overall profile of the graph would represent exactly the curve of
brightness of the photopic spectrum.

Saturation is maximal (100%!) at the ends of the spectrum — a fact
which often goes unappreciated because of the low brightness of those
regions and the confusion of brightness and saturation in the mind of
the student. Saturation is always the degree of freedom from admixture
with white, whether white external to the source of color is objectively
added to the latter or not; for, the color itself, even if generated by a
single wavelength, contains unsaturating whiteness as long as the wave-
length in question sets off all three components of the central synthetic
mechanism to any extents whatever. Under all ordinary circumstances
we cannot have 'pure' colors, even in the spectroscope, without accepting
an adulteration thereof by whiteness which arises from causes entirely
within the central mechanism. In Figure 32, the intrinsic degree of satur-
ation of any wavelength can be seen as the ratio of total chroma to white-
ness, remembering to take singly the part of the ordinate from the top-
most curve to the next one down, doubly the portion from that curve
to the lowest, and triply the heavy line representing whiteness. It is
obvious, however, that by fatiguing with the complement of a color we
will so greatly reduce the height of the whiteness-ordinate that the satur-
ation of the color will be correspondingly increased. Fatiguing with
violet, for example, makes the yellow of the spectroscope — ordinarily
the least saturated of all its hues — become amazingly rich in chroma;
an experience never to be had otherwise, and never to be forgotten.

Color Blindness — 'Color blindness' is an unfortunate term which in-
cludes at least five, perhaps six, kinds of departure from the normal
trichromatic system. Total color blindness is the only type in which no

COLOR BLINDNESS 97

hues at all are seen, hence is the only type which should ever have been
called color blindness at all. Vision is restricted to white, grays, and
black, and the condition had best be called 'achromatic vision'. It seems
nearly always to be due to the congenital absence, or a gross defective-
ness, of the cones, for along with it there are usually to be seen : (a) low
visual acuity both scotopically and photopically; (b) a central scotoma or
blind spot where the bouquet of foveal cones should be ; (c) a nystagmus
or uncontrollable fluttering of the eyeballs owing to the lack of this cen-
tral fixating region; and (d) photophobia or light-shyness, owing perhaps
to an excess of rods, occupying the spaces where cones should be.

In 'anomalous trichromatic vision', some one spectral region appears
less bright than it does to the normal person, and the individual requires
more of such light, mixed with some other color, to match an inter-
mediate color. An individual who, say, perceives green weakly must mix
more green with less red than the normal individual, in order to match
a standard yellow. This condition is not color blindness — it would much
better be called color weakness.

These color-weak individuals have poor hue-discrimination and an in-
creased perception-time for colors. They fatigue rapidly for colors, which
seem to them to fade upon continued observation; and to identify some
colors they require them in larger areas, with greater intensity and satur-
ation, than the normal. Anomalous trichromates probably outnumber all
other kinds of so-called color-blinds, but since they less often get into
difficulty through unfortunate selections at the neckwear counter, they
usually live and die without ever knowing of their peculiarity.

The conspicuous and familiar color-blind type is the dichromate or
Daltonist, whose confusion of red and green is proverbial — and also
hereditary, in a sex-linked fashion which keeps the defect a rare one in
females. One white man in twenty-five is a dichromate, but only one
white woman in twenty-five hundred. The dichromate is so called because
he requires only two primaries, instead of three, to mix and match any
and all hues and white. It so happens also that he can experience only
two hues instead of the large number* of the normal trichromate; but
the prefix (di = two) on his label does not refer, to this latter fact. The
dichromate is not color-blind — he is color-poor.

^Usually taken as 160-180; but these are the discriminable hue-and-saturation complexes.
Similarly, a dichromate can distinguish a large number (about 60) of spectral regions, tut
chiefly through saturation-difrerences.

98 THE VISUAL PROCESS

The dichromate, in distinguishing most natural colors, must fall back
upon saturation- and brightness-differences. The former are much the
more important to him. Longwave colors look alike in hue to him, but
very different in saturation. It is widely supposed, even by some expert
psychologists, that a dichromate motorist tells red traffic signals from
green ones on a basis of brightness, and is helpless to do so when bad
weather dims them both. This is not the case. The brightness of the red
and green lights could be varied up or down, or the red light made much
brighter than the green (the reverse is usually true) without inverting
his identifications; for the two lights would still retain their very different
saturations.

For a long time, Daltonism was thought to be due to a literal absence
of one of the three sets of receptors, or photochemical substances, or
cerebral perceptual processes, of the Young-Helmholtz scheme of things.
It was the physiologist Fick who showed, many years ago, that this could
not be the explanation; but the lack-of-one-process theory is still taught
far and wide. To adjust Figure 32 to represent dichromatic vision in ac-
cordance with Fick's contributions, none of the colored curves should
be removed. It is only necessary to suppose that the spectrum of respon-
siveness of one of the three 'somethings' has shifted into coincidence
with that of one of the other two.

To be specific, let us suppose that the redness curve is altered so that
it superimposes upon the green-ness curve, and see what should inevit-
ably result in the vision of the individual. Firstly, the spectrum would
be shortened at the red end even in bright light. Secondly, redness and
green-ness would always be contributed equally to the sensation evoked
by all wavelengths from 650m[i to 476m[X. So, in this whole great spec-
tral region the individual could see only yellow with varying degrees of
saturation and brightness. He would have to learn to call the highly-
saturated wavelengths red, and to call the less saturated ones yellow or
green. Thirdly, from 7.476m[A on to the ultra-violet, only violetness
could be experienced, with saturation increasing as wavelength decreased.
But his spectrum would contain something besides yellow and violet;
for (fourthly) at X476m\i all three processes would be in action to the
same degree : white would result at this 'neutral point' in his spectrum.
Fifthly and lastly, purple would not exist for him, for since redness and
green-ness were inextricably tied together as yellowness in the long-
wave part of the spectrum, the mixture of any wavelengths there, even
those seen by the normal as red, with any of the wavelengths seen by

COLOR BLINDNESS 99

himself as 'violet', could yield only white since yellow and violet are
complementary. For such an individual, proper amounts of any two
wavelengths which were not on the same side of his neutral point could
be mixed as complementaries to make white.

Now, the above is actually a fair description of one kind of dichrom-
atic vision, called 'protanopia' in the older terminology since it was sup-
posed to result from the lack of the first (protos = first) of the three
component processes of trichromatic vision. Another, much more com-
mon, type is 'deuteranopia' (from deuteros = second) . This form we can
represent by shifting the green curve in Figure 32 to lie on top of the
red one. The deuteranope experiences no shortening of the spectrum at
the red end, and his neutral point is nearer the red end than that of the
protanope (though neither of the actual neutral points is quite where it
ought to be as theoretically called for by the diagram.) Otherwise, his
experiences are about the same : two hues only, with one at either side of
the neutral point; the same white region at the neutral point; and the
same white or gray sensations from stimuli which appear to the normal
as purple.

A condition much like dichromasy occurs, as a rarity, in one eye only.
The individual is then able to tell us what he sees with that eye in terms
of the trichromatic visual performance of his normal eye. Usually, he
reports that the spectrum contains only yellow and blue, not violet as
described above; but such pathological cases could not be expected to
duplicate perfectly the situation in true Daltonism.

Theoretically, two other kinds of dichromasy are possible, but only
one of them has been found (or else the two have been confused) :
'tritanopia' is so extremely rare that it has not had proper study. We
could represent its two possible versions by aligning the green curve of
Figure 32 with the violet, or the violet curve with the green one. The tri-
tanope's neutral point, depending, would then coincide with either the
protanopic or deuteranopic one. In the latter case, the spectrum would
be shortened at the violet end. In either case, the only possible hue-
experiences, it would seem, would be red and blue. The shortened spec-
trum of at least some tritanopes seems to have been noticed by the older
investigators and recognized in the common name of the condition,
*blue-blindness'. Tritanopia can be simulated in some individuals by ex-
cessive absorption of short-wave light in an abnormally rich macular
pigmentation (see Chapter 8, section D), or in an extremely yellow,
pre-cataractous lens; and also by the yellowing of vision in jaundice

100 THE VISUAL PROCESS

(usually ascribed to tinting of the vitreous by bilirubin — but E. Sachs
finds no such yellowing in icteric dogs; perhaps the retina is colored).

Photochemistry of Color Vision — So much as to suggestions re-
garding what goes on in the higher reaches of the chromatic visual
mechanism. Now, what objective realities can we point to, in the way
of a physiological mechanism for analyzing and transmitting assort-
ments of wavelengths in and from the eye? Sadly, only one dubious
photochemical substance of ambiguous properties.

In 1930, Gotthilft von Studnitz reported the first revelation of a
retinal photochemical since the discovery of Boll and Kiihne. Studnitz
has never given the material a real name — it is just the *Zapfensubstanz'
{i.e., cone-substance) . Several years later Wald in this country, without
reference to Studnitz's work, hypothesized a cone substance which he
named iodopsin (iodos = violet) on the assumption that if one could iso-
late and concentrate it, it would be found to be violet in color. 'Iodop-
sin', however, was based upon technical methods which Studnitz has ever
since insisted could not possibly have indicated his own zapfensubstanz,
but rather involved a serious error on Wald's part, Studnitz has con-
sequently refrained from applying Wald's appropriate name to the sub-
stance which he has claimed to be able to extract and study. For any
detailed discussion of the zapfensubstanz, the reader must go to the
work of Studnitz cited in the bibliography. No one outside of his group
has worked on the substance in all the years since its announcement.
Remarks on it here will be brief,

Studnitz first identified this photosensitive substance by comparing
the capacity of a fresh retina for absorbing light, before and after being
exposed to strong light. After such exposure, the retina was found to
be more transparent than before, which could apparently only be the
result of the destruction of some photosensitive substance. The first
retinae employed were duplex; so, to eliminate rhodopsin from the pic-
ture, Studnitz repeated his experiments on some pure-cone retinae. Here
also he found the substance, which therefore must be in the cones. He
learned how to study it by itself in rhodopsin-bearing retinae, though not
how to isolate its effects very well from those of cone oil-droplet pigments,
which come out in the same solvents and are slightly photosensitive.

By comparing the change, before and after the bleaching with strong
light, in the amount of various monochromatic lights absorbed, Studnitz
was enabled to plot a curve of the absorption spectrum of the zapfen-

PHOTOCHEMISTRY OF COLOR VISION

101

substanz; and this curve eventually received complete confirmation when
he obtained the absorption spectrum of the compound isolated from the
retina by extraction with ether and chloroform. Extracts of fish, frog,
turtle, and mammalian material contained various, always tiny, amounts
of the material whose maximum absorption of light was invariably at
A,560m|X or thereabouts — the position of the peak of the photopic bright-
ness curve, just as the peak of absorption of rhodopsin coincides with
the bright spot in the scotopic spectrum (Fig. 34; cf. Fig. 33).

In fact, the absorption spectrum of the zapfensubstanz proved to be
superimposible over the photopic brightness curve, after some alter-
ations which lay Studnitz open to the serious charge of 'wangling'.

^50

400

500 600

WAVELENGTH(mn)

Fig. 33 — Similarity of the graph of the
absorption spectrum of rhodopsin (frog)
and that of the luminosity of the spec-
trum to the scotopic human eye. Re-
drawn from Grundfest.

^'90
§80

(Teo

4(

500 600

WAVELENGTH(my)

Fig. 34 — Similarity of the graph of the sup-
posed absorption spectrum of the photochem-
ical material of the cones, and that of the
electrical responsivity of the photopic retina
through a portion of the photopic spearum
(here taken as indicative of photopic lumin-
osities). Redrawn from von Studnitz.

Herein lies the chief claim of the zapfensubstanz to acceptance as the
essential photochemical of cone vision — and, at the same time, its most
puzzling quality when the Young-He Imholtz theory is kept in mind.
It is very nice to hear at last that there really is an extractible photo-
chemical substance in the vertebrate cone visual cell. It is not so con-
venient to find that this one substance, single-handedly, appears capable
of accounting for the whole of the photopic brightness curve. There
ought to be three zapfensubstanzes, the overall profile of whose absorp-
tion spectra would just neatly fill out all the corners under that curve!
Studnitz, indeed, recognizes the possibility that what he has called one
substance is really a group of three which his solvents cannot separate
from each other. In fact his very latest curves, derived from snake

102

THE VISUAL PROCESS

material, show three peaks instead of one. He thinks the precursor of
the substance is the carotenoid pigment of the cones' oil-droplets (for
this there is no evidence whatever) and points out that the multiplicity
of such pigments in turtles and birds suggests that several different
photochemicals, a la the multi-component color-vision theories, are formed
from them. How this works out in the lizard, which sees all colors and
yet has only yellow pigment in its oil-droplets — or in man, who has no
oil-droplets at all (see Chapter 8, section D), Studnitz does not tell us.
So far, then, we are told of but the one substance. Its very existence
is most dubious, for leading authorities are very skeptical of Studnitz's

/ ,.' man, a .,
/^-photopic \\ \
scotopic— \\

owl, scotopic-

400 500 600 700

Wavelength (mp)

Fig. 35 — The Purkinje shift as shown
by the relative brightnesses of mono-
chromatic lights to the photopic and
scotopic human eye. Also, the relative
pupil -closing effectiveness of mono-
chromatic lights upon the scotopic
eye of an owl, Asia wilsonianus.
Redrawn from Hecht and Pirenne.

<08

I04

fish-.;'

'6g

t

12 m
h

Q
08-j-

600 550 500 450

Wavelength (mp)

Fig. 36 — Formation of acid (phosphoric?) in
retinje under monochromatic light — supposedly
owing to breakdown of the cones' photosensitive
material, and showing similarity to graphs of
photopic brightnesses. Redrawn from von Stud-

claims and critical of his methods. Granting that Studnitz has really
found a cone-substance — it may really be three, but if so we know not
how to separate them. Its precursor is quite unknown; but its end-
product upon breakdown under light is supposed to be phosphoric acid
(Fig. 36) . When we try to understand the retinal part of the physiology
of color vision, a single zapfensubstanz seems more of a hindrance than
a help. And if we choose rather to believe in the solitary 'iodopsin' of
Wald and Qiase, we are no better off. Different wavelengths would
break down different amounts of the whole concentration of the sub-
stance, and we can easily imagine that corresponding kinds of optic
nerve impulses — differing in modulation or whatnot — are produced and

PHOTOCHEMISTRY OF COLOR VISION 103

then integrated centrally where they set off the respective three com-
ponent processes of the synthetic mechanism. But, for any one wave-
length there is another on the other side of the peak of the absorption
spectrum of the zapfensubstanz, which at the same intensity would break
down the same amount of the substance into, presumably, the same end
products. How then could these two wavelengths possibly arouse differ-
ent sensations? It is impossible to imagine how any one substance could
serve as the analytical mechanism by which purple light is translated
into 'redness modulated' and Violet-ness modulated' impulses in a single
optic nerve fiber. For the cones to generate three qualitatively different
impulses, it would appear that they must contain a triplex photochemical
system.

In truth, the working out of the photochemical system of the cone
may long continue to seem the most difficult branch of the physiology
of the eye. To absorb more light in one part of the visible spectrum than
another, a substance must be colored. In the present state of our knowl-
edge we must suppose that there are tiny amounts of three differently-
colored photosensitive substances in the cone's outer segment. With the
very sloppiest of technique, we can mount the fresh dark-adapted retina
of a frog or a goldfish on the microscope and still see the rich wine of
rhodopsin filling its rods. But with the most careful of methods, we can
succeed in seeing living cones only as completely colorless structures,
whose bland innocence conceals invisible traces of three important some-
things — to our utter exasperation.

Chapter 5

THE GENESIS OF THE VERTEBRATE EYE

(A) Embryological

There are many anatomical relationships in the eye which are ex-
tremely puzzling when we look only at their adult condition, but which
become perfectly clear if we follow their ontogeny. A little knowledge
of the embryonic development of the eye is therefore highly desirable.
The process is a fascinating one in its own right, but we shall examine it
here as a means to two ends : the embryology of the eye can be expected
to shed some light upon its evolutionary origin; and, the developmental
scheme serves as a framework within which all possible adaptive evolu-
tionary changes of ocular structure must fit. If we know how the eye
develops we can guess where it came from, we can see how it has been
able to take on the modifications which fit it for greater efficiency in this
or that environment, and we can see why it has not been able to make
some changes that might seem to us more logical than particular ones
which it has happened to accomplish.

The following account is a generalized one which applies in its en-
tirety to no particular animal, but is based upon the mammals because
their story is known in the greatest detail. Some important departures
characteristic of other vertebrate classes will be pointed out specifically,
but in general the reader who wishes to imagine the ocular embryology
of a lower class needs only to make a mental subtraction, from the mam-
malian process, of those features which the lower group lacks, in order
to have a fairly accurate conception.

The parts of the eye are recruited from three sources in the embryo:
(a) the ectoderm of the neural tube, which is in turn derived by infold-
ing from the surface ectoderm and which later differentiates into the
brain and spinal cord; (b) the surface ectoderm remaining after the
neural tube has been formed and separated from it; and (c) the meso-
derm lying between the neural tube and the surface ectoderm.

Formation of the Optic Cup — These three sources start to make
their respective contributions in this same order. The brain being by far
the most complex organ in the body, it begins to develop before any
other; and the eye gets an equally precocious start since its most essen-

FORMATION OF THE OPTIC CUP 105

tial part, the retina, is a derivative of the neural tube. Even while the
tube is still an unclosed groove in the surface ectoderm, the beginnings
of the two retinae can be seen as a pair of dimples in the anterior portion
of its floor — the part destined to become the forebrain of the embryo.
As the lips of the neural groove approximate and fuse to close the
neural tube and push it beneath the surface ectoderm, these pits or
'foveolas opticas' (Fig. 37a) are each rotated through a right angle so
that they form a pair of bumps on the sides of the closed-in forebrain
(Fig. 37b). They rapidly expand as if blown up from the inside, and
each becomes a bubble of tissue attached to the side wall of the fore-
brain by a broad, very short, hollow stalk.

Fig. 37 — Formation of the optic vesicles.

a, cross section of anterior portion of frog neural groove, as yet unclosed, showing foveolie
opticce. Redrawn from Eyclesheimer.

b, cross section of head of 4mm. human embryo, after closure of the neural groove — the
foveolae now form the optic vesicles. Redrawn from Mann.

/- foveolae opticEc; fb- embryonic forebrain; m- mesoderm; tie- neural ectoderm; /- optic
stalk; se- surface ectoderm; v- optic vesicle.

At this stage the bubble of forebrain tissue is in contact with the sur-
face ectoderm of the side of the head and is known as the optic vesicle,
its connection with the forebrain proper being called the optic stalk. The
stalk slowly shifts its root backward as the brain becomes serially con-
stricted into five chambers, and is eventually connected with the second
of these, the diencephalon or tween-brain.

Two processes now set in, one in the optic vesicle and one in the
surface ectoderm, which go on simultaneously and look superficially as
though one of them must be causing the other : an indentation of the
optic vesicle to form a two-layered optic cup; and an in-sinking of a
portion of the surface ectoderm to form a closed hollow ball of tissue,
the lens vesicle, which comes to lie in the cavity of the optic cup. The

106

THE GENESIS OF THE VERTEBRATE EYE

formation of the lens vesicle is absolutely dependent upon the presence
of the optic vesicle against the surface ectoderm — but not in any
mechanical way: the lens-organizing influence of the optic vesicle is
exerted chemically. If the optic vesicle is removed, no lens vesicle is

Fig. 38 — Formation of the optic cup.

a, b, c, diagrammatic models of optic vesicle, transitional stage, and completed cup as seen
from the side of the embryonic head with the surface ectoderm removed. The curved arrows
in b show the direction of growth of the lateral portions of the vesicle which, while the
indentation of the face of the vesicle is taking place, grow below the level of the axis of the
optic stalk (dotted line) to form the ventral half of the cup. The embryonic fissure is
created by the temporary failure of the down-growing lobes to meet and fuse.

a', b', c', optical sections through the stalk axis (dotted line), corresponding respectively
to a, b, and c. A patch of surface eaoderm has been left in place to show the development
of the lens vesicle.

ef- embryonic fissure of optic cup; g- groove on underside of optic stalk (continuation of
embryonic fissure); i- invagination of face of vesicle; il- inner layer of optic cup (future
retina); Ip- lens placode; h- lens vesicle; ol- outer layer of optic cup (future pigment
epithelium); s- stalk; se- surface ectoderm.

formed; and if the optic vesicle is planted under any other surface ecto-
derm, even on the belly of the embryo, a lens vesicle will proceed to
form from that ectoderm. Similarly, if the developing lens vesicle is
removed, the optic vesicle goes right ahead with its indentation — the
latter is an active process, not caused mechanically by the inward pres-

FORMATION OF THE OPTIC CUP

107

sure of the developing lens; nor is the surface ectoderm passively sucked
inward, to form the lens vesicle, by the cupping of the optic vesicle.

The conversion of the optic vesicle into the optic cup is more than
a simple indentation or invagination (Fig. 38). At first, the dilated
vesicle lies largely above the level of the optic stalk, but after the com-
pletion of the optic cup the stalk is found to be attached to the center
of its back. Figure 38b shows what really happens — a growth of the two
sides of the base of the vesicle laterally and downward, closing in below
the attachment of the stalk. The closure is not at first complete, so that
a slit, the 'embryonic fissure of the optic cup' is left in the ventral

Fig. 39 — Cell-lineage
of the retina. Modified
from Fiirst. At the extreme
left is the initial coluninar-epithel-
ioid condition of the inner layer of
the optic cup. Germinative cells, occupy-
ing a position comparable to that of the
ependymal cells of the brain wall, proliferate a
pseudo-stratified tissue, some of whose elements
eventually retract one or both of the processes con-
necting their cell-bodies with the limiting surfaces. The ••*" -^lJ^::^^ /7
oldest, most vitread of the elements (bottom-most in the drawings) are about the first to
differentiate, and maturation proceeds outward toward the germinative cells, which at last
become the rods and cones.

r- portion of rod; c- cone; h- horizontal cell; m- Miiller fiber; b, b- bipolar neurons;

a- amacrine cell; g- body of ganglion cell; n- nerve fiber (axon of ganglion cell).

meridian of the cup, running from its rim to the cup end of the optic
stalk. Along the under side of the stalk, nearly all the way to the brain
wall, there is now a deep groove which has invaginated during the form-
ation of the optic cup. This groove opens into the cavity of the optic
cup and here forms the apex of the embryonic fissure. The old cavity
of the optic vesicle has been nearly obliterated by the indentation of the
vesicle. It, through its continuation in the optic stalk, still opens into
the forebrain cavity but of course has no communication with the new
cavity of the optic cup or with that cavity's continuation, the ventral
groove of the optic stalk.

108 THE GENESIS OF THE VERTEBRATE EYE

Differentiation of the Retina — The optic cup now has two layers
of tissue in its wall whereas the optic vesicle had but one (Fig. 38c', il,
ol) . The outermost of these layers remains forever one cell thick and its
cells shortly develop pigment granules, the whole layer becoming even-
tually the pigment epithelium of the retina. The cells of the inner layer
of the optic cup rapidly proliferate, forming many layers from which
will be derived the various layers of the adult sensory retina (Fig, 39).
Since it is the outermost of these cells (toward the pigment epithelium)
which are multiplying, their daughter cells are pushed ever inward
toward the cavity of the optic cup. It follows that these innermost cells
are the oldest at any one time and they are naturally the first to differ-
entiate. They lie in the position of the ganglion cells of the adult retina;
and it is into these that they develop, soon protruding their axon fibers
which grow along the inner surface of the optic cup. These fibers all
aim for the cup end of the optic stalk — the site of the future disc — and
here turn outward and grow down through the tissue of the stalk {not
through the groove on its under side) to make their connections in the
wall of the diencephalon. They form the optic nerve fibers; and a few
cells of the stalk tissue, which escape destruction by them, proliferate
the neuroglial cells which help to form the system of interfascicular
septa in the adult nerve.

The further differentiation of the cells of the inner layer of the optic
cup proceeds in a two-fold manner: from the inner surface toward the
outer (next the pigment epithelium) and from the posterior pole of the
cup forward along all meridians toward the rim. At the posterior pole,
the future amacrine cells can be recognized soon after the ganglion cells
and Miiller fibers have differentiated. The bipolars and horizontal cells
next become distinguishable; and, when proliferation finally ceases, the
cells nearest the pigment epithelium (which have been doing the pro-
liferating) are finally free to differentiate into the rods and cones — the
last elements in the retina to mature though they are the most ancient
cells in the eye and are its whole reason for being.

At any one time, these changes are further advanced at the posterior
pole than they are out toward the rim of the cup, where cell-division
may still be seen long after it has ceased in the fundus of the retina.
The optic cup thus grows at its lip, and rapidly increases manyfold in
diameter and in surface area as the embryo enlarges. A convenient con-
sequence of this is that it is possible to study the whole process of retinal
differentiation in a single favorable section of a single embryonic eye,

DIFFERENTIATION OF RETINA; LENS 109

simply by examining regions which are successively farther from the
posterior pole and nearer to the ora terminalis, or rim of the cup. An-
other consequence is that the region of the ora is to some extent perma-
nently juvenile. If the retina is destroyed and subsequently regenerates
(as it will do in amphibians, though not in any other vertebrates) the
new retina grows from the ora terminalis, creeping backward until the
fundus is filled; and a new optic nerve develops pari passu with the
regeneration. A perennial mystery, however, is the fact that the retina
continues to increase greatly in extent after all cell-division has appar-
ently ceased in it — as is the case, for instance, in an amphibian which is
on the verge of metamorphosis, though the eye is then nowhere nearly
adult in size. It is possible that sensory-retinal elements continue to
differentiate from the ciliary epithelial cells (v.i.) at the ora, and the
application of the colchicine technique may solve this problem.

The Lens — All this time, the lens has been developing. Commencing
as a local thickening in the surface ectoderm, the 'lens placode' evoked
by some chemical emanation from the contiguous optic vesicle, it has
invaginated and pinched free of the surface ectoderm, which heals over
it without trace.

Thus is formed the lens vesicle, lying in the mouth of the optic cup
(Fig. 38c'). Its posterior or inner wall rapidly thickens, each of the
cuboidal cells becoming columnar and continuing to elongate until it
is a slender fiber. The growth in length of these cells being in a forward
direction, they encroach upon the cavity of the lens vesicle and oblit-
erate it, forming a solid mass whose anterior surface is still covered over
by the unmodified cuboidal cells of the original anterior wall of the
vesicle (Fig. 40). This cuboidal layer is the lens epithelium, and at the
equator of the lens it forever remains continuous with the greatly thick-
ened posterior wall. In this region of transition, epithelial cells now
commence to elongate and to rotate their axes of polarity until they are
no longer radially oriented with respect to the center of the lens, but
circumferentially disposed (Fig. 41a). The two ends of these elongating
equatorial cells disconnect from the ends of their neighbors in the epi-
thelium and grow apace, one end sliding forward under the epithelium
and the other end backward, guided by the confining capsule which has
already been secreted by the lens vesicle over its whole outer surface.

Thus a layer of circumferential lens fibers is laid down, like one of
the skins of an onion, over the central mass of original, straight lens

110

THE GENESIS OF THE VERTEBRATE EYE

fibers which were formed directly from the cells of the posterior wall of
the lens vesicle. The further conversion of crop after crop of cuboidal
epithelial cells, at the equator of the lens, results in layer after layer of
fibers each of which is added outside of the previous one (Fig. 41b).
Any one fiber being too short to stretch from pole to pole of the lens,
its anterior and posterior ends meet, head-on, the corresponding ends

Fig. 40 — Early stages of the lens. Redrawn from Mann.

a, placode stage, comparable with Figure 38a'; p- lens placode formed in surface ectoderm;
ov- optic vesicle, b, c, lens pit forming and closing off; cl- lips of optic cup. d, lens vesicle
has detached and passed into mouth of optic cup; Iv- lens vesicle; m- mesenchyme which has
now invaded space between optic cup and surface ertoderm. e, cavity of lens vesicle being
obliterated by the elongation of the posterior wall cells to form the first of the lens fibers.
f, lens is now solid, and its present fiber mass will constitute the 'embryonic nucleus' of
later life (cf. Fig. 41b); ^ zone of transition of epithelium into fibers — the locus at which
all future fibers will form; ac- anterior chamber forming as a cleft in the mesoderm, separ-
ating the latter into the future cornea and the future iris stroma, g, new fibers have been
added to the embryonic nucleus and are meeting end-to-end at anterior and posterior suture
planes; s- posterior suture {cf. Fig. 41b, sp).

of a diametrically opposite fiber. These meeting points are aligned in
radial planes within the lens mass, called lens sutures (Figs. 40g, 41b
and c) , which perforce branch more and more toward the surface of the
growing lens as the number of epithelial cells ringing the equator in-
creases and the number of fibers seeking place for their tips against the
suture planes increases. At any one time, there are many superficial
layers in which the fibers have not yet elongated enough to reach suture

Fig. 41— Growth of the lens.

a, diagram of the equatorial region of a growing lens, showing how the cells of the lens
epithelium, e, elongate and reorient their axes of polarity to convert into lens fibers, /, whose
ends slide forward under the epithelium and backward under the capsule, c, as they take
on a circumferential course.

b, diagram showing growth of lens fibers; the youngest, in the vicinity of /, are still in
contact with the epithelium e and capsule c (c/. a). /'- cortical fibers which are still grow-
ing as indicated by the arrows, and have not yet reached suture planes. Their nuclei,
distributed along the nuclear bow nb, slowly fade as the fibers gradually sclerose upon being
marooned in the heart of the lens by the addition of newer fibers peripheral to them.
Oldest, hardest fibers of all are those of the 'embryonic nucleus' en, formed direaly from
the posterior wall of the lens vesicle (c/. Fig. 40). /"- fibers which have reached the suture
plane sp. (All fibers in the section are shown as if in one plane — aaually, they spiral so
that the suture planes of the front and back halves of the lens are at right angles; c/. c).

c, superficial fibers of the adolescent nucleus of the human lens, showing the 'lens stars'
which represent the intersections of the branched suture planes with the surface. Redrawn
from Mann.

d, portion of equatorial section of human lens, showing radial lamellae of lens fibers and the
hexagonal shape of the latter in cross seaion. x 500. From Maximow and Bloom, after
Schaffer. b- branching of a radial lamella, which occurs repeatedly as the equatorial peri-
meter of the lens enlarges during growth. (All the fibers shown in a lie in one radial lamella).

Ill

112

THE GENESIS OF THE VERTEBRATE EYE

planes, creating an unsutured cortex overlying a sutured core, the cortex
becoming proportionately thinner as the lens ages and the rate of fiber-
formation is slowed (see also pp. 20-1).

Fig. 42 — The hyaloid circulation.

a, model of invaginating mammalian optic vesicle, showing future hyaloid artery being taken
up through the embryonic fissure. Based upon figures of Mann.

bw- brain wall; ca- carotid artery; cv- first chonoidal vessels, which will anastamose around
cup rim to form the annular vessel, and will branch over cup surface to lay down the
choriocapillaris; ha- hyaloid artery.

b, model of fetal mammalian eye in optical section, showing the hyaloid system at the peak
of its development. Based upon figures of Versari.

ac- anterior chamber; av- annular vessel; hp- Bergmeister's papilla (neuroglial support at
base of hyaloid, which will later atrophy with the hyaloid vessels, leaving a cup in the
nerve head); c- cornea; cc- choriocapillaris (first vessels of the chorioid to form); Ad-
trunk of hyaloid artery, traversing vitreous cavity; im- ins mesoderm, containing capillary
arcades thrown forward from annular vessel; /- lens; mc- mesenchymal (mesodermal) con-
densation which will form chorioid and sclera; p- lids (temporarily fused over cornea);
pe- pigment epithelium of retina; r- retina, with neuroblastic layer still single anteriorly
but already divided into inner and outer layers in the precocious fundal region; tvl- vessels
of tunica vasculosa lentis, encapsulating the growing lens; vhp- vasa hyaloidea propria,
supplymg the vitreous and the retinal surface — the last vessels of the system to differ-
entiate, and usually the first to atrophy.

This growth process never completely stops until death, though it is
greatly retarded after the eye has reached its adult size. The oldest fibers
of the lens being the innermost ones, it is these which first feel the effects
of being removed farther and farther from any possible source of food
and oxygen, and they sclerose (harden) and die. The sclerosis involves

HYALOID CIRCULATION; VITREOUS 113

more and more outlying layers of fibers until the dead, firm centrum of
the lens has grown in size (by middle age) to the point where little
accommodatory change of shape of the lens is any longer possible (see
Fig. 15, p. 35). The lens is thus unique among the organs of the body
in that its development never ceases, while its senescence commences
even before birth.

The Hyaloid Circulation — In mammals, though not in any other
class, the developing lens is nourished by an elaborate temporary net-
work of blood vessels. The first signs of their development are seen while
the optic cup is just being formed. From a plexus of embryonic capil-
laries lying beneath the vesicle, one especially plump vessel is taken up
into the groove of the optic stalk (Fig. 42a) so that when the lips of this
groove finally close, the little vessel lies along the axis of the future optic
nerve and forms the 'hyaloid artery'. At the optic-cup end of the groove
of the optic stalk, it emerges into the cup cavity. The healing of the
embryonic fissure of the optic cup fixes the point of emergence of the
hyaloid artery at the site of the apex of the fissure. As it traverses the
vitreous cavity it branches around the lens to form a vascular tunic on
the latter, and some of these branches make connections at the rim of the
optic cup with other vessels clinging to the outer surface of the cup, the
beginnings of the chorioidal circulation. A ring-shaped 'annular vessel'
is formed at the cup margin, and from it capillary loops are thrown over
the anterior face of the lens, budding through the mesodermal tissue
which has squeezed in between the lens and the surface ectoderm, and
thus laying down the circulation of the embryonic iris (Fig. 42b).

The whole vascular net around the lens, the other branches of the
hyaloid artery which run along the inner surface of the retina, and
the hyaloid artery itself eventually (before birth) atrophy back to the
head of the optic nerve. Here the hyaloid (now called the central
retinal artery) gives off new branches into the retinal tissue, accom-
panied by branches of the central retinal vein, to give the retina its
definitive circulation.

The Vitreous — In among these temporary vessels in the cavity of the
young optic cup there is a gelatinous tissue, the 'primary vitreous', whose
few fibers are of dual origin, some being produced by mesodermal cells
which invaded the cup with the hyaloid vessel, others coming from the
foot-plates of the Miiller fibers of the developing retina, and even from
the cells of the lens until the formation of the capsule shuts off further

114 THE GENESIS OF THE VERTEBRATE EYE

contributions. Most of the definitive or secondary vitreous is secreted
by the retina during the growth of the eye, the primary vitreous coming
to form a slender cone with its base on the back of the lens and its apex
at the head of the optic nerve (Fig. 43). The final disappearance, from
this primary vitreous, of the last remnants of the hyaloid circulation
leaves it in the form of a conical tube (filled with vitreous thinner than

Fig. 43 — Formation of the vitreous.

a, diagrammatic section of young optic cup showing vessels of the hyaloid system embedded
in the primary vitreous, consisting of mesodermal fibers and cells (which invaded the cup
along with the hyaloid artery ha), together with fibrils secreted by the ectoderm of the cup,
lens, and surface.

b, diagrammatic section of fetal optic cup in which atrophy of the vasa hyaloidea propria
(c/. Fig. 42b) has clarified the peripheral vitreous, to which has now been added much
secondary vitreous (vertical hatching) secreted by the sensory retina. The persisting tunica
vasculosa lentis and the trunk of the hyaloid artery ha are embedded in a cone of primary
vitreous.

c, the definitive situation (c/. Fig. 3, p, 7): the canal of Cloquet represents the remnants
of the primary vitreous, stretched to a slender column by the growth of the eye (diagonal
hatching). The secondary vitreous (vertical hatching) nearly fills the globe. The tertiary
vitreous (horizontal hatching) is constituted by the fibers of the zonule, secreted lastly by
the non-sensory retina. The optic-nerve portion of the hyaloid artery alone persists, as the
central retinal artery era, and has given off new branches into the retinal tissue.

the secondary kind) , the canal of Cloquet. This canal runs through the
vitreous from disc to lens in the adult, with a considerable sag along
its course caused by gravity and time (see Fig. 3, p. 7).

The Vascular and Fibrous Tunics — As soon as pigment granules
appear in the outer layer of the finished optic cup, a network of capil-
laries — the future choriocapillaris — is formed in the mesoderm against
the pigment epithelium. Larger vessels developing outside of these, and

VASCULAR AND FIBROUS TUNICS

Fig. 44 — Formation of the anterior segment (modeled in optical seaion, based
upon the process in primates; scale decreases from a to d).

a, young embryo (cf. Fig. 40f). Anterior chamber has formed; lids closing over cornea;
scleral condensation has appeared.

b, advanced embryo. Chamber is broader; lids are fused by epithelial plug; cornea has
stratified epithelium, mesothelial lining; back wall of chamber still wholly mesodermal, but
optic cup margin has put forth a thin outgrowth bearing meridional ridges (ciliary pro-
cesses); major circle of iris can be made out.

c, fetus. Chamber still broader, its margin nearer to major circle; lids still fused but with
lash follicles. Meibomian and other glands budding in from ertoderm; Descemet's membrane
and canal of Schlemm formed; ciliary muscle and large-vessel layer of chorioid taking shape;
hyaloid system has degenerated; continued forward growth of optic cup margin (leaving
corona ciliaris behind) has given the iris mesoderm its ectodermal backing (from which the
sphinaer is differentiating) but leaves a thin film of mesoderm over the lens — the pupillary
membrane, which will soon atrophy.

d, fetus near term. Chamber will broaden yet more, well past Schlemm's canal; lids re-
opened and well differentiated; cornea and anterior sclera fibrous; reaus muscles formed;
ciliary muscle fully developed; iris complete — dilatator differentiated, pupillary membrane
gone; formerly narrow zone between original optic cup margin and precociously-formed
corona now greatly expanded, creating orbiculus ciliaris and leaving old cup margin far
behind as the ora terminalis; zonule fibers, growing out from orbiculus, have attached to
lens capsule.

ir- inferior rectus; //- lower lid; ot- ora terminalis; sr- superior rectus; «/- upper lid; zf-
zonule fibers.

116 THE GENESIS OF THE VERTEBRATE EYE

connected with them, become the arteries and veins of the chorioid coat.
The mesoderm around the optic cup condenses to form the connective-
tissue substrate of the chorioid and sclera, at first one mass but later
separated by the formation of the epichorioidal lymph-spaces. Other
early mesodermal condensations develop into the extra-ocular muscles
and other orbital contents.

The anterior chamber is formed quite early as a cleft in the mesoderm
between the lens and the surface ectoderm, separating this mesoderm
into that of the iris and that of the cornea (Fig. 40, ac; Fig. 44). The
two layers may become neat and regular even before their separation.
The corneal mesoderm differentiates into the substantia propria, and the
overlying surface ectoderm contributes the corneal epithelium. The
lining cells of the embryonic anterior chamber become the latter's meso-
thelium, secreting (on the inner side of the cornea) Descemet's mem-
brane as their basement membrane.

The iris is thus at first wholly mesodermal, and there is no aperture
in it, the future pupil being filled in by a mesodermal 'pupillary mem-
brane' which must later atrophy. The two ectodermal layers of epi-
thelium on the posterior surface of the iris are laid down by the optic
cup in the following way :

The thick rim of the optic cup, the future ora terminalis of the sensory
retina, suddenly resumes proliferation, and a bud-like prolongation of
it creeps out under the mesoderm of the iris, between that mesoderm
and the lens, forming a thin double epithelium whose two layers are
respective continuations of the pigment epithelium and the retina proper.
This is actually new growth, for the optic cup proper does not expand
to accomplish it, as is evidenced by the fact that the original thick rim
'stays put'. The first structure laid down by this thin anterior continu-
ation of the cup lip is the future corona ciliaris; but when this has been
produced the growing lip does not stop, but cuts through the vitreous
which is joined to the root of the iris and continues out under the iridic
mesoderm as far as the site of the future pupil margin, leaving the
pupillary membrane devoid of an ectodermal backing.

The outer layer of this epithelial fold is pigmented like the retinal
pigment epithelium of which it is a continuation, and during its growth
the pigmentation begins also to involve the inner layer of cells, creeping
backward from the growing lip as far as the root of the iris, where it
stops. This leaves the innermost of the two layers of epithelium which
cover the ciliary body forever free of pigment granules, forming the

LIDS AND GLANDS; NON-MAMMALS 117

ciliary epithelium. In the iris, the outer or anteriormost of the two layers
of epithelial cells eventually loses much of its pigment icf. Fig. 7g, p.
15) as it gives rise to the sphincter and dilatator of the pupil, which
are thus the only ectodermal muscles in the body.

In the ciliary body, mesodermal cells differentiate into the ciliary
muscle fibers, and the anterior chamber widens and deepens greatly
through the erosion of tissue at the iris angle. From the ciliary epithelium
there develop the cuticular fibers of the suspensory ligament or zonule,
which are regarded collectively as the tertiary vitreous and which grow
axiad to gain secondary attachments to the lens capsule. The anterior
surface of the secondary vitreous then drops back to its definitive posi-
tion, its surface presented to the aqueous forming the anterior hyaloid
membrane; and the aqueous of the anterior chamber is free to spread
back into the posterior chamber and the canal of Hannover. With the
formation of the zonule, the main features of the eyeball are established.

Lids and Glands — The lids arise as a circular fold of skin around the
front of the eye which closes in over the cornea, with its circular aper-
ture rapidly becoming a horizontal slit, thereby creating upper and
lower lids. The margins of these fuse together early in fetal life, opening
again much later — from a few days to six weeks after birth in mammals
which are born hairless and helpless. The time of reopening always
coincides closely with that at which the rods and cones have finished
their differentiation. That differentiation, it is interesting to note, can
be speeded up a couple of hundred percent by surgically opening the
lids of the newborn mammal and keeping it and its mother in a lighted
place. The various glands of the lids, the lacrimal and Harderian glands,
and the lacrimal drainage system are all ectodermal derivatives; but
their mode of development is unimportant to us here.

Variations in Non-Mammals — Some major departures from the
above process, which occur in the different vertebrate groups, are men-
tioned briefly below and will be dealt with at some length subsequently,
in appropriate places. Others will be self-evident to the reader when, in
later chapters, he encounters mention of the loss or gain of some feature
by one group of animals or another.

Lampreys : The epidermis and dermis of the skin are never fused to
the cornea to contribute respectively a corneal epithelium and a part
of the substantia propria. A patch of visual cells is already functional
in the primary optic vesicle (see Fig. 54c, p. 126) and persists as 'Retina

118 THE GENESIS OF THE VERTEBRATE EYE

A' in the growing eye until metamorphosis, when throughout the re-
mainder of the much-expanded retina ('Retina B') the visual cells are
suddenly differentiated and the borders of Retina A become indistin-
guishable. Retina A goes out of function when the tiny larva first bur-
rows into the mud, and the eye is blind until metamorphosis, when the
skin covering it becomes transparent and Retina B matures. No intra-
ocular muscles or suspensory-ligament fibers ever develop, for the pupil
is motionless and there is no ciliary body interposed between chorioid
and iris. The lens is propped in place only by the vitreous, which seems
to have evolved its semi-solid nature for this original purpose.

Fishes : Except in the elasmobranchs, the optic vesicle is at first solid
as is the central nervous system, both eye and brain becoming hollow
secondarily. In many of the bony fishes the embryonic fissure never quite
closes, and the chorioid erupts through it to form the 'falciform process'.
Others develop, instead, a network of vessels at the vitreo-retinal inter-
face. Those species which have a pseudobranch develop a huge capillary
mass in the chorioid, the 'chorioid gland'. True lids and associated
glands are usually lacking, though vertical, so-called 'adipose' lids are
common.

Amphibians: The fusion of the skin with the purely mesodermal,
inner layers of the cornea (those continuous with the sclera) is deferred
until metamorphosis, as is the development of the lids. The growing
suspensory-ligament fibers do not obliterate the anterior part of the
secondary vitreous, but remain embedded in it so that no aqueous-filled
cavities are ever formed behind the iris. Despite their entanglement, the
tertiary vitreous fibers are derived only from the ciliary epithelium, the
secondary vitreous solely from the sensory retina, just as in other verte-
brates.

Reptiles and Birds: The neuroglial supporting tissue of the head of
the optic nerve usually proliferates a vascular, pigmented 'pecten' pro-
jecting through the vitreous toward the lens. In birds the elongated
base of the pecten follows the course of the embryonic fissure, developing
from its lips. In some groups, an anterior portion of the embryonic
fissure never closes, and a meridional slit is thus left in the ventral part
of the ciliary body, through which the anterior and posterior chambers
communicate. The third eyelid or nictitating membrane (present also,
as the 'haw', in many mammals) arises as a vertical fold of conjunctiva
at the nasal side of the eye, covered by the upper and lower lids. The
equator of the lens and the ciliary body come into contact and remain

EVOLUTION OF EYE FROM BRAIN 119

SO (whereas in mammals they later separate, owing to the eye's growing
faster than the lens, so that the suspensory ligament is thereby put in a
state of tension, forcing the lens to become flatter during its growth).
In the snakes, the course of development of many parts has been pro-
foundly modified, as is explained in detail in section D of Chapter 16.

(B) Evolutionary

In its simplest terms as seen in the lamprey, the vertebrate eye has
only a very few essential living parts: retina, uvea, fibrous tunic, and
lens. The problem of the origin of the eye is merely the problem of the
status of each of these parts previous to their present association. Yet
though when thus stated the matter appears simple, it has baffled a great
many astute morphologists. The great German anatomist Froriep once
likened the 'sudden' appearance of the vertebrate eye in evolution to the
birth of Athena, full-grown and fully-armed, from the brow of Zeus.

The Eye a 'Part of the Brain' — From the embryology of the eye it
appears that there could have been no complex retina until the chordates
had evolved an internal, tubular brain. The foveolae opticae have been
interpreted as an ancestral stage in which the eyes were essentially a pair
of photosensory epithelial pits in the skin, analogous to those of a
modem Nautilus. Another possibility is that the foveolae are develop-
mental precocities without phylogenetic meaning. Before we can decide
how to interpret them, we shall have to try to determine how far back
the rods and cones may have been photosensory.

If the retina is thought of as a photosensory portion of the brain wall,
outpocketed to keep it near the skin in an ancestor whose body was
becoming larger and more opaque as evolution proceeded, then the scle-
rotic and uveal coats are easily disposed of by homologizing them with
the meningeal envelopes of the central nervous system, the dura mater
and the pia-arachnoid. The sclera is actually continuous with the dura
via the sheath of the optic nerve. The latter also possesses a continuation
of the pia-arachnoid, though this ends outside the eyeball and does not
merge with the chorioid even in the embryo. The vascularity and pig-
mentation of the chorioid are however strongly pia-like characteristics,
and in lampreys there are even striking histological similarities between
chorioid and pia.

120

THE GENESIS OF THE VERTEBRATE EYE

The big difficulties which an eye-origin theory must hurdle are: (a)
the inversion of the retina — the fact that the vertebrate visual cells point
away from the light; (b) the nature of the visual cells before they be-
come photosensory, and the question of their location at the time they
did so; and (c) the question of the status of the lens before it became
associated with the retina as a dioptric structure.

i^"^#il -*- inf

Fig. 45 — Sagittal section of 'brain' of Amphioxus.

(In the position it normally has in the living animal in its burrow). From Walls, after Franz.

aps- anterior pigment spot; dc- two of the dorsal cells of Joseph; inf- infundibular organ,
whose photosensory elements are flagellated ependymal cells.

Early Theories — Between 1874 and 1929 a series of investigators saw
the beginnings of the vertebrate eye in the anterior pigment ^ot of
Amphioxus (Fig. 45, aps). Even by 1890, however, experiments had
indicated that this 'eye' is not sensory at all, and at the present time
this is considered certain.

EARLY THEORIES

121

Lankester, in 1880, suggested that the eye of the vertebrate is com-
parable with that of the 'tadpole' larva of certain of the lower chordates,
the Ascidia. Others interpreted this suggestion as one of true homology,
and a debate sprang up over whether the ascidian eye was a degenerate

Fig. 46 — Illustrating the ascidian theory as originally conceived.

(At a time when the ascidian lens was mistakenly believed to lie toward the brain cavity).
From Walls, after Jelgersma.

a, ascidian eye, consisting of a retinal evagination of the brain wall and an internal lens, //.

b, hypothetical transitional stage in which two lenses were present, one on either side of
the retina.

c, vertebrate retina and definitive, 'outer' lens, derived from skin.

Fig. 47 — Illustrating Balfour's theory. From Walls, after Parker.

Patches of photosensory cells are shown in the successive positions which they are supposed
to have occupied before and after the evolution of the neural tube and the retinal evagin-
ations thereof.

offshoot of the vertebrate organ or a primitive fore-runner thereof. Froriep
later decided that neither of these views could be true, for the retina of
the ascidian eye is not inverted; but he thought that both eyes might
have had common ancestry in a pair of dermal eyes (Figs. 46 and 48).

122

THE GENESIS OF THE VERTEBRATE EYE

Balfour's Theory — It was Balfour, in 1881, who first proposed that
the vertebrate retina originated in the skin and was carried inside the
animal by the evolution of the neural tube (Fig. 47). Several investi-
gators, independently of each other, soon pointed out how well the fove-

Fig. 48 — Illustrating Froriep's derivation of the ascidian and vertebrate eyes.
(From common-ancestral superficial vesicular eyes). After Walls.

a, b, c, d, stages in the evolution of the ascidian eyes, showing the degeneration of one
member of the pair.

a, b', c', d', stages in the evolution of the lateral eyes of vertebrates.

o\x Opticas fit into this hypothesis (Figs. 49 and 50). Balfour's theory-
was the first to account for the inversion of the retina, but it offered no
explanation of the lens. It has however been suggested that inversion was
no accident, but had to be brought about somehow if the highly meta-

BALFOUR'S THEORY

123

bolic rods and cones were to have an adequate blood supply (the chori-
oid) without this lying between them and the light and blurring the
image. Moreover, it must be remembered that we have no certainty
whatever that the chordate nervous system originated as a tube — the
lowest vertebrates, which should show the most primitive situation, de-
velop it as a solid cord and canalize it secondarily.

Fig. 49 — The foveolce opticae in relation to Balfour's theory. From Walls.

a, unclosed brain region of neural tube of frog embryo, showing the foveolce optica, /-/,
as patches of pigmented columnar cells (after Franz).

b, c, d, stages in the evolution of the eyes, based on the development of the foveolae into
the retincB (after Lange).

Fig. 50 — Illustrating Schimkewitsch's

version o

f Balfour's theory.

(Deriving the lateral eyes from one of several pairs of photosensory pits in the surface ecto-
derm, of which the foveolaa optica are the embryological counterparts). From Walls, after
Schimkewitsch.

124

THE GENESIS OF THE VERTEBRATE EYE

Fig. 51 — Illustrating the placode theory. From Walls, after Beraneck.

A vesicular eye derived from a lateral-line organ loses its photosensitivity and becomes the
definitive lens, while its ganglion becomes photosensory and is converted into the definitive
retina.

St

fs

/-^^/

Fig. 52 — Hesse's organs of the 'spinal cord' of Amphioxus. From Walls, after Hesse.

a, a single organ, consisting of a pigment cell and a photosensory ganglion cell, whose
'stiftchensaum', st, was believed by Boveri to be a cuticular struaure comparable with the
outer segment of a rod or cone.

b, cross section of nerve cord, showing various orientation of the organs (enabling the animal
to respond to the direction of light).

THE PLACODE THEORY; BOVERl'S THEORY

The Placode Theory — The origin of the lens was first explained by
Sharp in 1885. He regarded the lens as a modified lateral-line organ
which was, like those organs, a sensory ectodermal pit or bud. The
'placode theory', an extension of Sharp's original idea, proposes that
the lens was once the whole eye and that the present retina served as its
ganglion, eventually taking over the sensory function itself and releasing
the vesicular 'skin' eye to become a lens (Fig. 51). Fatal objections to
this interpretation of the retina arise from the utter absence of embry-

Fig. 53 — Illustrating Boveri's theory. From Walls, after Boveri.
The Hesse's organs become the visual and pigment-epithelial cells of the vertebrate retina.

©logical confirmation of any previous connection of retina and lens,
and from the lack of any evidence that a self-determining lens placode
exists at all as a morphological entity — it will be recalled that it is called
into existence ontogenetically solely by the chemical influence of the
optic cup. Nor does the placode theory account for inversion.

Boveri's Theory — Inversion was explained anew by Boveri in 1904,
in a theory that made use of the two-celled visual organs of Amphioxus,
which had been discovered by Hesse in the 'spinal cord' of this so-called
grandfather of the vertebrates (Figs. 52 and 53). While Boveri's theory

126

THE GENESIS OF THE VERTEBRATE EYE

offers no account of the lens, it gives as good an explanation of the retina
and its inversion as does Balfour's theory; and both hypotheses are widely
taught at the present time. Acceptance of either is impossible, however,
unless the mode of development of the rods and cones indicates either
that they might have been already photosensory while still in the skin.

Fig. 54 — Illustrating Studnicka's theory. From Walls, after Studnicka.

The sensory cells of the median and lateral vertebrate eyes are derived from the flagellated
ependymal cells which line the neural tube, c represents the larval lamprey, in which the
eye is temporarily functional though the retina ('Retina A' — see p. 117) is still only an
uninvaginated optic vesicle and the lens is flat and useless.

or that they might have been derived from the photosensory ganglion
cells of Hesse's organs or the similar 'Joseph's cells' in the head region
of Amphioxus (Fig. 45, dc).

Studnicka's Theory — Unfortunately the cytogenesis of the rods and
cones supports neither Balfour nor Boveri, but confirms a radically dif-
ferent hypothesis first offered in 1912 by Studnicka, and which has yet
to be given consideration in any of the various text-books which afford
a little space to the eye-origin problem (Fig. 54) .

STUDNICKA'S THEORY

127

Studnicka noticed that if one traces the visual-cell side of the inner
layer of the optic cup around the latter and through the optic stalk into
the central nervous system, one emerges into the ependymal layer of the
brain wall. The ependymal cells lining the cavities of the brain and cord
are non-nervous supporting elements which often bear flagella (micro-
scopic whiplashes) which circulate the cerebrospinal fluid. Studnicka
also laid great stress upon the eye of the young larval lamprey (Fig. 54c) ,
which is precociously functional while still merely an optic vesicle, as
indicating that the vertebrate eye was originally merely a 'directional'

Fig. 55 — Comparability of young visual cells with ependymal and other flagellated cells:
embryological support for Studnicka's theory. From Walls.

a, fetal human foveal cone, showing filamentous, centrosomic anlage of outer segment rooted
in diplosome (after Seefelder). b, immature human sperm cell showing anlage of flag-
ellum, consisting of centrosomic filament and diplosome (after Gatenby and Beams), c,
immature cone from retina of kitten (after Leboucq). d, ependymal cell from brain of
carp (after Franz).

one before it became capable of forming images. Since the lens is already
present in the tiny lamprey, but in the form of a flat cushion incapable
of dioptric function, Studnicka argued that it must have existed phylo-
genetically — a vestigial remnant of something else, possibly a sense-
organ — before the retina was devised at all. He also showed that there
are many central-nervous sense-organs in vertebrates, including the
median or pineal and parietal eyes (see Chapter 10, section D), whose
receptors are certainly modified ependymal cells. He has received strik-
ing confirmation in the recent demonstrations of the photosensitivity of
the lining of the diencephalon of many forms, which (in birds) has been

128 THE GENESIS OF THE VERTEBRATE EYE

shown by Benoit and others to act as a photic receptor organ, controlling
reflexly the annual spermatogenetic cycle.

But Studnicka never considered in detail the manner in which rods
and cones differentiate, though this had already been most carefully
worked out by several European investigators. If he had done so, his
theory would surely have seemed much stronger to subsequent text-
writers. For the outer segment, the receptive organelle, of a vertebrate
visual cell develops exactly like any flagellum (Fig. 55a, b). It starts as
a filament of centrosomic material rooted in a diplosome or dumb-bell
shaped centriole embedded in the future inner segment, later becoming
encrusted and thickened by mitochondria which form the conspicuous
spiral filaments making up the bulk of the outer segment (Figs. 23a,
25c, pp. 55, 62; Fig. 26b, B, p. 63). A closer comparabiUty of visual cells
and ependymal cells (Fig. 55c, d) could hardly exist.

Origin of the Retina — If the photosensory parts of the rods and cones
were once ependymal flagella, it is certain that Boveri's theory must be
discarded; for ependyma, even photosensory ependyma, exists in Am-
phioxus side by side with the Hesse's organs and Joseph's cells. It is
equally certain that the vertebrate retina could not have gotten started,
as a photosensitive region of the brain wall, until the latter had become
tubular. Only then was there any need for the ependymal cells to evolve
as elements distinct from nerve cells; and these were primarily supportive
(they still run through the whole thickness of the brain wall in Am-
phioxus and the lampreys), then secretory in function (producing the
cerebrospinal fluid) before it became necessary for them to aid in circu-
lation by means of flagella. No flagella, no sensitivity or photosensitivity;
and it can be regarded as certain that the definitive visual cells were
developed within the finished brain and not, a la Balfour, while the nerv-
ous system was still a part of the skin. Indubitably there were photo-
irritable cells in the provertebrate's skin, as there still are in many fishes
and amphibians — even in cave forms which are never normally struck by
light; but these lost importance as soon as photosensory ependyma had
appeared (Fig. 56). The most primitive homologues of the rods and
cones to which we can point today are the photosensory flagellated epen-
dymal cells of the 'infundibular organ' of Amphioxus (Fig. 45, inf, p.
120), which is a crude visual apparatus seemingly for the detection of
the direction of light by means of shadows cast upon it by the anterior
pigment spot.

ORIGIN OF THE RETINA

129

Fig. 56 — Origin of the retinae of the median and lateral eyes. After Walls.

a, pro-vertebrate stage with photosensory ectoderm and with the nerve cord still a part of
the skin, b, b', alternative stages in the evolution of the neural tube, depending upon
whether one adheres to the 'solid' or 'hollow' doctrine, c, tubular nervous system formed,
but with ependymal lining purely sustentative, secretory, and circulatory, d, ependyma has
become photosensory locally, and photosensory cells have disappeared from the skin,
e, f, g, stages in the evolution of patches of photosensory ependyma into retinae.

Origin of the Lens — When everything else in the primitive eye is so
plausibly explicable, it is really a shame that we cannot be at all sure how
the lens came into existence. The lens placode fits neatly into the set of
cephalic lateral-line organs, and for it to develop into a lens is no more
remarkable than for one of them to generate the olfactory organ or for
another of them, the otic placode, to differentiate into the elaborate

130

THE GENESIS OF THE VERTEBRATE EYE

membranous labyrinth of the internal ear. It would be nice to be able
to insist that the lens placode has a real morphological existence and
that the lens is therefore a captured lateral-line organ, as Sharp be-
lieved; but we cannot do so with clear consciences. The best that can

i/m

Fig. 57 — Illustrating Tretjakoff's theory. From Walls, after TretjakofF.

a, foveolcB opticas stage, b, stage of closed neural tube, showing hypothetical chorioid
plexus, cp. c, hypothetical stage in which the expansion of the chorioid plexus has created
the pigment epithelium and, by forcing the sensory retina to curve, is producing a two-
layered cup. d, stage in which the attachment of the cup to the skin is evoking a muscle,
m, and a lens, /; a remnant of the chorioid plexus forms the umbraculum, urn, corresponding
to the pupillary nodule of an amphibian, e, final condition of fish eye with free lens, /,
operated by retractor lentis muscle, Im; from the umbracular remnant um a lens may be
regenerated, as in salamanders (cf. Fig 106a, pn, p. 266).

be said is that perhaps a former self-determination of the lens has been
replaced by a more convenient immediate chemical control by the optic
vesicle — just as the development of a secondary sexual character may
be under genetic control in one species of bird, while in another the

ORIGIN OF THE LENS 131

same character is caused to develop by hormones, and fails to appear
if the gland which secretes the chemical determinants is removed.

No other current explanation of the lens is anything but lame. The
co-existence of a functional retina and a functionless lens in the larval
lamprey may mean, as Studnicka thought, that the lens existed in some
other status before the rest of the present eye evolved. Possibly how-
ever it means no more than does the precocious presence of function-
less muscles in an embryo before their nerves have grown out to connect
with them. No one would argue that this means that those muscles once
functioned without nervous control.

/-/-^

Fig. 58 — Illustrating Schimkewitsch's theory. From Walls, after Schimkewitsch.

a, hypothetical ancestral skin-eye, with erect retina and intrinsic 'retinal' lens rl. b, phylo-
genetic stage comparable with embryonic cup — the eye, originally dorsal, has swung laterally
and ventrad, becoming passively indented (by resistant tissue) to create the embryonic
fissure; the retinal lens is now uselessly located, c, final condition of the eye, with new
lens derived from the skin; it is from the site of the supposed original retinal lens that
new lenses may be regenerated if the skin-lens is removed in the young embryo or even
(salamanders) in the adult.

Tretjakoff thought that the primitive optic cup was attached to the
skin and developed contractile elements there (which later became the
piscine retractor lentis muscle) for producing to-and-fro accommoda-
tory movements of the optic cup relative to the skin. The lens then
arose as a sort of callus in response to the continual pull of the muscle
cells (Fig. 57). But the lower fishes have no retractor lentis; and in any
case there would have been no need whatever of accommodation until
the lens had already appeared and become capable of forming a crisp
image. Tretjakoff also attempted to account for the fact that in sala-
manders whose lenses are removed, new lenses may regenerate from the
dorsal pupil margins. This has been explained more cleverly, if no more
properly, by Schimkewitsch (Fig. 58).

Franz's theory is new and ingenious. He suggests that the lens
evolved, when the neural tube was just closing, in such a position as

132

THE GENESIS OF THE VERTEBRATE EYE

to concentrate light upon the photosensitive lining of the diencephalon.
Its locus somehow escaped involution with the neural tube and later
moved laterally to be taken over by the new retina (Fig. 59) . No onto-
genetic conditions support this idea, and like the placode theory it stands
or falls with the demonstrability of a self-differentiating lens anlage.

Fig. 59 — Illustrating Franz's theory. From Walls, after Franz.

a, ancestral surface eye corresponding to the infundibular organ of Amphioxus prior to the
closure of the neural tube, b, later stage corresponding to the foveola; opticEe, with the
future lens-forming area labelled la. c, stage of general photosensitivity of lining of dien-
cephalon. The lens (shown in an earlier stage on the left, a later one on the right) is
evolving just outside the region of involution, d, stage of appearance of dorsal diencephalic
evagination — the future pineal eye; the lentogenic areas have shifted still farther laterally.
e, final condition of the pineal (p) and lateral eyes (/e); the lens is now embryologically
derived from the skin far distant from its original location.

The experimental morphologists are very fond indeed of doing things
to embryonic eyes to see what they will do in return. Someday, their
juggleries may disclose that in some species of fish or amphibian a lens
will start to develop without the presence of an optic vesicle. Until

ORIGIN OF THE LENS 133

then at least, and perhaps forever, the evolutionary origin of the verte-
brate lens must remain a tantalizing mystery.

A very good question is: how is it that the lens, derived from the
skin, lies inside the fibrous and uveal tunics— which, above, we homolo-
gjzed with the meningeal coats of the brain? Did the retina acquire its
optical partner before the central nervous system acquired its protective
sheaths? Perhaps so — and, such theories as that of Tretjakoff make such
an assumption necessary. But the lens could easily enough have gotten
through the sclerotic coat after the latter had evolved. Such legerdemain
is common enough in vertebrate history^as witness the presence of the
pectoral girdle inside the rib basket, in the turtles. All that is needed is
a nice timing of embryological events, occurring as an embryonic muta-
tion — if the lens did pass through the dura mater to get inside the eye-
ball, ii assuredly did so in one jump, in some ancient embryo in which
the condensation of the dura happened to be delayed. And lenses have
been getting inside of eyes ontogenetically in that same way ever since.

Chapter 6
ELEMENTS OF VERTEBRATE PHYLOGENY

If one knows something of the history of a group of animals and
its position in the animal kingdom, one may more easily draw correct
conclusions as to how it acquired its characteristic morphology. We
may learn of some structure in the eye of one of the lower animals which
looks intriguing as a possible forerunner of some detail of the human
eye; but we need to know whether the group that exhibits the structure
in question is anywhere near the main line of evolution, or represents
a blind alley from which nothing higher than itself has ever emerged.

A little about vertebrate group inter-relationships is therefore included
here, that the reader may better understand why one animal has solved
a given visual problem in one way while another, given other raw
materials, has had to find a different — perhaps better, perhaps poorer —
solution to the very same problem. In devising adaptive structures, each
animal group has had to do what it could with the materials at hand —
the assemblage of characteristics and structures with which the group
happened to be endowed when it crystallized out of the stream of life.
May we reasonably look to the teleost fish for the prototype of some
amphibian ocular structure? Can we expect to see in the snakes a feature
which the lizards discarded? Can we fairly compare the human eye more
closely with the eye of a salamander, or with that of a bird? A brief
review of the vertebrate pageant will help the reader to answer such
questions as they arise during his study of subsequent chapters.

At the bottom of the vertebrate scale stand the cyclostomes; and just
above them, the many types of true fishes. From one of these types the
first land animals, the ancient amphibians, were derived. They in turn
gave rise on the one hand to the modern amphibians and on the other
to the reptiles. The reptiles differentiated into a large number of orders,
only four of which have persisted to the present day. From one group
of extinct reptiles came the birds; and from another (much older) group,
the mammals — warm-bloodedness and heat-retaining coverings (feathers,
fur) thus having originated independently in the two highest classes of
vertebrates.

134

ELEMENTS OF VERTEBRATE PHYLOGENY 135

The lowest of the vertebrates are the cyclostomes, so named for their
round, suctorial, jawless mouths. The cyclostomes include the hags,
whose eyes are microscopic and functionless, and the lampreys (Fig. 60).
They are eel-shaped, blood-sucking parasites upon fishes. Some small

[Higher P l acentals|
Insect I vores]

[Marsupials^

[Monotremes

t Therapsidans

t [Stegocephalians| !T |Coecilians[

iHolosteans', ' ' ^ |Cladi stians[ /^; ^rossopterygiansj

>^ ^/" 'Dipnoansj

[Modern Chondrosteons^

Primitive
Chondrosteans

L^

.Selachians

Chinnaeras

I Primitive
Elasmobranchs

Primitive
Cyclostomesl

^Lampreys!
^Hagfishes]

Fig. 60 — Inter-relations of the major groups of vertebrates.
Only those extinct groups (marked f) are shown which actually link up living assemblages.

freshwater lampreys have given up parasitism and do all of their feeding
as larvae, breeding for the first and only time a few months after trans-
forming to the adult condition. Parasitic lampreys also breed but once
after years of vegetative activity, and then die. Cyclostomes have no
scales or paired fins, and many other things about their anatomy are

136 ELEMENTS OF VERTEBRATE PHYLOGENY

simple; but it is sometimes difficult to know whether to attribute the
simplicities to primitiveness or to the secondary simplification (mistak-
enly called degeneracy) which is a part of their adaptation to a parasitic
mode of life. As regards the lamprey eye, however, there is unanimous
agreement among modern students that its features are all primitive
and show no indications of degeneracy.

The oldest of the true fishes are the elasmobranchs, whose modern
representatives, the Selachii (sharks and rays) and Holocephali (chim-
aeras), are very different from their extinct progenitors. The elasmo-
branchs were derived from ancient cyclostomes, but not from lamprey-
like ones. Like the cyclostomes, they have cartilaginous skeletons; but
they also have paired fins, jaws, and scales. From those jaws have come
the little bones of the ossicular chain which traverses our middle-ear
cavity; and from some of the rows of scales on the elasmobranchs' lips
came their teeth, the ancestors of our own — and very different from the
horny teeth of lampreys.

The primitive elasmobranchs were a main-line group, for from them
have come all of the higher, 'teleostome' fishes; and through these, the
terrestrial vertebrates. From ancient elasmobranchs there arose an ad-
vanced group of fishes, still with cartilaginous skeletons, called the
Chondrostei. These fishes have had many descendant groups, among
them several which might, any one of them, have given rise to land
forms — for they all spread into fresh waters and swamps, and developed
lungs of sorts, and limb-like fins with which to drag their bodies over
the slime.

These lunged fishes were the Cladistia, the Crossopterygii, and an
offshoot of the latter called the Dipneusti — the lung-fishes proper. All
three of these groups were once numerous as to species and individuals,
but have dwindled to remnants which still cling precariously to life in
competition with the more advanced modern fishes. The Dipneusti, or
dipnoans, have but three living genera : Neoceratodus in Australia (Fig.
61a), the African Protopterus, and Lepidosiren in South America.
There are but two living cladistian genera — Polypterus and Calamoich-
thys, both in Africa. Until very recently it was supposed that the cros-
sopterygians were extinct; but one species, named Latimeria chalumnce,
was lately discovered in the sea off South Africa. This is the only archaic
teleostome known from salt water.

The chondrosteans have persisted to the present time, but are now
represented only by the sturgeons (Acipenser, Huso, Scaphirbyncbus,

ELEMENTS OF VERTEBRATE PHYLOGENY 137

etc.) and the spoonbills or paddlefishes, Polyodon and Psephurus. Very
soon after their own origin, the chondrosteans gave rise to a group of
fishes with bony skeletons, the Holostei — formerly lumped with the
Chondrostei in an artificial group called the 'ganoids'. The Holostei had
their heyday long ago, and have but two living genera, the bowfin
(Amia) and the gars or gar-pikes, Lepisosteus spp. From primitive
holosteans came the Teleostei, the most conspicuous group of modem
fishes, including such familiar forms as the trout, perch, herring, and
goldfish. Defeating the holosteans in competition for habitats and food,
the teleosts have taken the place in the seas and fresh waters formerly
occupied in succession by the chondrosteans and holosteans. But the
teleosts are a blind-alley group from which no higher forms have been
derived.

Fig. 61 — The transition from water to land.

a, an existing dipnoan, the Australian 'dyelleh', Neoceratodus forstert. After Ley.

b, a giant stegocephalian, Mastodonsaurus giganteus (redrawn by E. C. Case, from a
restoration by Fraas); in life, the animal was about fifteen feet long, p- site of pineal eye.

It was probably from swamp-dwelling crossopterygians that the first
land vertebrates came. These were the extinct amphibians which we call
the Stegocephali, from their characteristic head-armor. Some adult stego-
cephalians were but a couple of inches long, but most of them were gross,
sluggish beasts of little brain (Fig. 61b) — very different from the pert
little salamanders and agile frogs of the present time. It is possible that
the Stegocephali are not a natural group, but comprise two groups with
independent origins. It is also barely possible that some of the modern
amphibians originated directly from air-breathing fishes and not from
the Stegocephali. These questions have only recently been raised and
are not yet settled. At any rate, it is certain that the Stegocephali were

138 ELEMENTS OF VERTEBRATE PHYLOGENY

the immediate ancestors of the reptiles — which, with their dry, scaly
skins and a number of internal improvements, were the first vertebrates
to become quite divorced from the waters.

The first land vertebrates must have had an easy time of it. Escaping
the fierce competition of the waters, they found themselves exploring a
new world in which they had no enemies. There was abundance of food,
for the plants had taken to the land eons before. The very ease with which
the land animals could spread and multiply encouraged the rapid pro-
duction of new types. And then, the inevitable happened — some of these
newer forms found the older ones good to eat. Competition on land
eventually became so keen that many reptiles, mammals, and even birds
returned to an aquatic existence. On land, their muscles had had to
sustain their weight and had become far more powerful than those of
fishes. Claws, beaks, and crushing teeth had also evolved, and with such
superior weapons many species found it easy to get a living in the water.

The reptilian group flourished amazingly and ruled the world for tens
of millions of years through its aristocracy, the group we call the dino-
saurs. But even while the twenty-foot tyrannosauri were mangling the
ninety-foot diplodoci, the first of the mammals were furtively sneaking
about looking for dinosaur eggs to suck, and the first birds — derived
from tiny dinosaurs — were getting off the ground for short flights. The
reptiles which we have around us are a mixture of old and new. The
lizard-like Sphenodon (rapidly approaching extinction on a couple of
New Zealand islands) is the sole survivor of the rhynchocephalians, the
rest of which died with the dinosaurs. The turtles are of enormous
antiquity — turtles are among the oldest reptilian fossils we know of,
and they were already perfectly standard turtles "way back then'. The
ancestors of the crocodile group can also be traced back into the begin-
nings of the Age of Reptiles.

The lizards, however, came into existence only recently as an offshoot
of the extinct mosasaurs. The snakes originated as legless lizards, so
very recently (as geological time intervals go) that the most primitive
of them, the boas and pythons, still have vestiges of the hind legs. Leg-
lessness has since arisen independently several times in different families
of existing lizards, but these snake-like forms are still true lizards.

The mammals fall into three great divisions: the egg-laying mono-
tremes of which only the duck-billed platypus (Ornithorhynchus) and
the echidnas are left on earth; the marsupials, which originated in South
America and left primitive types there, but reached their culmination

ELEMENTS OF VERTEBRATE PHYLOGENY 139

in Australia where they had no competition from the higher mammals;
and the placentals, which are the familiar hairy, milk-secreting animals
of the world and the group to which man himself belongs.

As one would expect, the birds, the monotremes, and even the mar-
supials have quite a bit in common anatomically with the reptiles. But
the placental mammals are quite distinct — more different from the mono-
tremes than the latter are from the reptiles. This is especially true as
regards the eye; and from ocular and other considerations Franz has
postulated that the placental mammals originated, not from lower mam-
mals, or (Huxley's view) independently from reptiles, but from forms
intermediate between the amphibians and the reptiles. There is however
no palxontological justification for such a view. The reptiles and birds
are so closely related that they are commonly lumped together as the
'Sauropsida'; and monotreme eyes — to some extent also marsupial eyes
— are sauropsidan in plan except for a radical simplification of the
mechanism of accommodation. The eye of the placental mammal is more
like that of an amphibian than like that of a reptile, but this is no proof
that the placental mammals originated more or less directly from am-
phibians. A more likely view is that the placental mammals had an early
history of strict nocturnality, during which they depended largely upon
other senses and simplified the eye far below the level of complexity of
the eye of the reptilian ancestor. The placental eye thus came to simulate
the amphibian eye through what might be described as a reversal of
evolution.

For our purposes the placental mammals may be roughly divided into
'lower' and 'higher' orders — the former including the insectivores, pri-
mates (including man), bats, sloths, armadillos, ant-eaters, and the 'fly-
ing lemurs' (Galeopithecus and Galeopterus) ; and the latter comprising
the carnivores, seals, whales, and hoofed animals (including the elephants,
hippos, etc.). The rodents and lagomorphs may be assigned to the top
of the lower series or to the bottom of the higher, depending on one's
point of view.

The tree-shrew and the aye-aye are thus at the bottom of the group
and the elk and tiger are at the top — with man very close to the bottom
biologically, ranking high only psychologically, as regards his brain and
mind. Man's order, the Primates, split away from the Insectivora about
50,000,000 years ago. Most of the living groups of mammals have come
into existence since that time. Man himself came along only yesterday,
but his stock is older than most of the mammalian stocks around him.

Part II-Ecologic

Chapter 7

ADAPTATIONS TO ARHYTHMIC ACTIVITY

(A) The Twenty-Four-Hour Habit and the Eye

Of the ways in which natural light can vary, it is the variation of
its intensity which is of most importance to animals, and to which they
have responded by the most profound of ocular modifications. To adopt
the bright hours of day, or the dim ones of night, or to appear indifferent
to their alternations, all require adaptations of the eye. These adapta-
tions for high sensitivity or for relative insensitivity in turn make pos-
sible, or tend to forbid, concomitant adaptations for form-perception
and visual recognition on a basis of pattern and color. Animals have
had to balance the desirability of a given habit with their ability to use
the advantages, and tolerate the disadvantages, which the modifiability
of their eyes in the appropriate direction confers or limits. In this and
the two succeeding chapters we shall examine the adaptations to illumin-
ation-preferences which vertebrate eyes have produced.

In surveying the visual habits of vertebrates one's attention is natur-
ally caught by the extreme conditions of strict diurnality and strict
nocturnality, and one tends to suppose that the intermediate condition
or arhythmicity, of apparent indifference to night and day, represents a
failure to specialize and a lack of adaptation. This is never actually the
case — a truly unspecialized and intermediate type of eye would fit its
possessor, not for twenty-four-hour vision, but for only the brief periods
of morning and evening twilight. The arhythmic animal has to meet a
more severe set of requirements than does the rhythmic one of either
extreme type, and meets them by combining in one visual organ those
adaptations to both bright and dim light which are not mutually exclu-
sive. To anticipate the next two chapters, a strongly yellow lens (as in
the prairie-dog) goes with diurnality but makes vision in dim light im-
possible; and a tapetum lucidum facilitates nocturnality but if non-

lusible and associated with a super-sensitive retina unprotected by a
lit pupil (as in the opossum) , it demands that the animal scrupulously
avoid strong light. Obviously, any attempt by an animal to secure twenty-
four-hour vision by combining a yellow lens with a tapetum would result
in his having wretched vision at any and all times.

143

occ

s

144 ADAPTATIONS TO ARHYTHMIC ACTIVITY

In either type of rhythmic animal we may have fancy adaptations, yet
an ocular situation which is simple in that it is static. But, for an animal
to become capable of arhythmic, twenty-four-hour activity, it is incum-
bent upon him to evolve a more flexible set of ocular features, capable
of physiological change to embrace a wide range of stimuli — in other
words, a dynamic eye in which, when the animal passes from one ex-
treme of illumination into the other, something or several things can be
seen to happen, and can be seen to be adjustive. The photomechanical
changes of the iris and the retina are the most conspicuous 'somethings'
referred to. Adaptation to twenty-four-hour vision has its static end-
products as well, in the evolutionary alteration of the cone: rod ratios
of a rhythmic ancestor, or even in the production of a duplex retina
from an ancestrally simplex one by the transmutation of cones into rods
or vice versa.

Before we take up these physiological and phylogenetic methods of
adaptation toward all-round visual capacity, it will be well to have
certain ecological definitions well in hand. We find that animals may
be classified as:

A. Diurnal; by which we shall take to mean that they are active
chiefly in the daytime, occasionally also in bright moonlight. Such
animals have eyes which are incapable of dim-light vision.

B. Crepuscular ; that is, active only in either or both of the evening
and morning twilight periods. Requires more sensitive eyes, which are
truly neutral, with few or no adaptations for extremes of illumination.

C. Twenty-jour-hour — more properly, 'arhythmic', the former term
applying better to both eye and animal, and both terms signifying that
the animal is about equally active by night and day. Such animals, if
they sleep at all, do so by irregular cat-naps.

D. Nocturnal; being active chiefly at night and confining daytime
activities largely to passive basking. Eyes usually more sensitive than
those of twenty-four-hour animals, and with much better devices for
greatly reducing sensitivity in daylight,

E. Strictly Nocturnal; with such sensitive eyes, so lacking in sensi-
tivity-reducing devices, that the animal is secretive or quiescent by day.

Each of these categories blends and intergrades with the next. Par-
ticularly is this true between 'C and 'D\ in which groups fall nearly all
of the mammals with the larger ones leaning toward 'C and the smaller
species inclining strongly toward 'D' or 'E'. The chief assemblages of

THE TWENTY-FOUR-HOUR HABIT 145

class 'C, twenty-four-hour vertebrates, and their principal bases for all-
round visual capacity, are:

The teleost fishes, relatively few of which are strictly diurnal, noc-
turnal, or crepuscular. Their ability to regulate ocular sensitivity resides
aknost wholly in their rod-rich retinae, in the form of efficient photo-
mechanical changes. Very few have mobile pupils.

The frogs, which again rely chiefly upon retinal adjustments and
possess at least one diurnal adaptation (yellow oil-droplets) which the
toads and the salamanders have had to eliminate, in order to become
respectively nocturnal and secretive.

Many slit-pupilled reptiles, which, being poikilothermous, tend to
bask in the sunshine rather more than would a warm-blooded animal
with the same general type of eye. The crocodiles and particularly the
geckoes have such excellent pupillary control of sensitivity that they
are practically arhythmic though tending to feed more at night.

The larger terrestrial mammals — ungulates, elephants, and large car-
nivores such as the wolves, bears, lion, etc. Here alone do we find
twenty-four-hour eyes which physiologically are relatively static, with
neither special retinal nor, as a rule, extensive pupillary regulation of
sensitivity. These forms straddle the fence by having enough rods-per-
cone to secure fair intrinsic retinal sensitivity, with large eyes and large
retinal images to obtain good resolution of details despite the paucity
of cones. They compensate for the lowered illumination of the larger
image by placing behind the retina a sensitizing device, the tapetum,
which is elsewhere found chiefly among the best-adapted of nocturnal
vertebrates. The vision of these mammals both by night and by day is
good enough so that they depend on it. Hearing and scent are important
enough at long range, but the serious business of stalking involves vision,
whatever the illumination. Day or night, a sightless carnivore would be
helpless — and so would a blinded ungulate.

(B) Retinal Photomechanical Changes

The phenomena which are grouped under this heading were discovered
one by one in the 1877-1887 decade. They consist of changes of position,
in bright and dim light or darkness, of the retinal pigment and the visual
cells, and of minor changes in shape and position of some of the retinal
nuclei. The nuclear changes are largely passive and are of no known
significance for vision; but the migrations of the rods, cones, and retinal
pigment are of great importance in the lower vertebrates.

146

ADAPTATIONS TO A RHYTHMIC ACTIVITY

Pigment Migration — It will be recalled that the cells of the retinal
pigment epithelium often bear groups of long processes which interdigi-
tate with the visual cells (Fig. 20d and e, p. 44) and that in the latter
a portion of the inner segment between nucleus and ellipsoid is often
contractile and then bears the name of myoid (Figs. 22, 23, 24; pp. 54,
55, 59). It is the retinal pigment (fuscin) in the pigment-cell processes,
and the rod and cone myoids which are chiefly concerned in the photo-
mechanical changes of the retina. These changes are most conspicuous
in duplex retinae and are concerned with both light- and dark-adaptation
of the retina.

Fig. 62 — Photomechanical changes in the retina of a fish, Phoxinus lavis.
From Kiihn, after von Frisch.

a, visual-cell layer and pigment epithelium in light-adaptation, b, dark-adaptation.
e- pigment epithelium; r- rods; c- cones; /- limitans; n- nuclei of visual cells.

When an animal equipped with photomechanical changes emerges
into bright light, a large portion of the retinal pigment — that which is
in the form of rodlets or short needles rather than tiny spherules — starts
to flow slowly down into the pigment-cell processes. These may be num-
erous and so slender that the granules pass into them in single file, or
they may be fewer and much more bulky. In as little time as half an hour
(though usually more slowly) the pigment will be found to be largely
scattered along the length of the processes and may reach nearly to the
external limiting membrane, being piled up into a dense mass at this
limit of its excursion. It thus forms a system of cylindrical sheaths sur-

RETINAL PHOTOMECHANICAL CHANGES 147

rounding the visual cells and blocking off from them any light rays
which approach them at angles to their axes. Where the myoids are very
slender (as in most fish rods) the expanded pigment may close in densely
enough between the rod ellipsoids and the limitans to shut off even the
axial rays from the percipient outer segments of the rods (Fig. 62) .

Fig. 63 — Visual-cell migrations in a catfish, Ameiurus nebulosus. x 500.
After Welsh and Osborn.

a, depigmented section of light-adapted retina, showing rods elongated toward pigment
epithelium and cones retrarted toward external limiting membrane.

b, depigmented section of dark-adapted retina; cones elongated, rods retrarted.

Visual-Cell Movements — Cones always escape being thus shielded to
any extent by the expanded, light-adapted pigment. They either sit,
permanently, directly upon the limitans or, if migratory, contract into
that position — away from the advancing pigment — in the light. Rods how-
ever, if they migrate at all in bright light, do so in the direction toward
the pigment (Figs. 62 and 63), The effective covering of the rods by
pigment is thus the sum of the pigment expansion and the elongation of

148

ADAPTATIONS TO ARHYTHMIC ACTIVITY

the rod myoid. The two movements are not perfectly synchronized, how-
ever, for the visual cells usually complete their migrations much more
rapidly than does the retinal pigment, though always consuming from
several minutes to an hour or more in the process, in different species.
There may be both indefinite and very definite differences within a single

Fig. 64 — Photomechanical changes of the leopard frog, Rana pipiens. x 500.

a, ventral periphery of light-adapted retina. The expanded pigment obscures the visual cells,
but a cone and a rod have been emphasized to show their positions.

b, same region, dark-adapted. The outlines of the visual cells have been reinforced. Note
that the cone myoids are greatly lengthened, the rod myoids somewhat shortened, as com-
pared with a. Toward the right is a double cone, whose chief member has migrated but
whose accessory member never leaves the limitans (c/. Figs. 22c, 23d, 24b, pp. 54-59).

retina, for the cones may be either uniform or very ragged in their re-
sponses, and both pigment and cones may respond less in particular
retinal areas than in others. In fishes the single and twin cones migrate
at different rates to different extents, and in other vertebrates the acces-
sory members of double cones never migrate whether the chief cones do
or not (see Fig. 24, p. 59, and Fig. 64b) .

SIGNIFICANCE AND DISTRIBUTION 149

If the animal now enters darkness or even a dimly-lighted situation,
the movements proceed, more slowly than in light-adaptation, to reverse
themselves : the pigment granules glide back up out of the processes and
concentrate as a dense band in the cuboidal cell-bodies of the epithelium,
the rod myoids shorten and draw the sensitive outer segments away from
the pigment and thus toward the light, and the cone myoids elongate to
push the cone bodies toward the pigment — sometimes to no apparent
purpose, but in some animals thereby making appreciably more room for
the rods to gather in a smooth layer close to the limitans (Figs. 62, 63,
and 64).

Significance and Distribution — Where the photomechanical changes
are as complete as described above, and carried out smoothly and within
an hour's time or less, the whole machinery is clearly of great value in
adjusting the retina to the external illumination. The workings of the
Duplicity Theory are beautifully seen in these phenomena, for the cones
are most advantageously placed for action in bright light, the rods being
then shielded from excessive stimulation (or from any at all) ; and in
dim light the rods are fully exposed while the cones get out of their way,
whether this latter happening has any obvious value or not. As a device
for equalizing the actual stimulation permitted to the visual cells in
various illuminations, the photomechanical system at its best is excellent
and has only the single drawback of slowness. Even this defect may be
unimportant in the case of an animal with sedentary habits and deliber-
ate movements, for temporal changes in natural illuminations are rarely
rapid. But the low speed of the retinal migrations would seem to be
detrimental to an agile species which flits from light to shade sporadic-
ally and lacks any more rapid means of regulating the illumination of
its visual cells. Among such forms would be fishes which move rapidly
from the bright surface to the dim depths and vice versa, and those
which inhabit coral reefs and the like, which may help to explain why
the latter are commonly crepuscular.

Table II summarizes the occurrence and relative effectiveness of the
photomechanical changes in the various vertebrate groups. The reader
will note a general tendency for them to dwindle in importance as one
passes from lower to higher forms, the reason for which will be discussed
in Section C.

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150

IMMEDIATE CAUSATION 151

Immediate Causation — It is evident from the table that there are few
important vertebrate types about whose photomechanical changes, or
lack of them, we cannot make positive statements in a descriptive way;
and the reader has just been promised an integration of the apparent
hodge-podge of their distribution, and an interpretation of the phylo-
genetic degeneration of these ingenious phenomena. But there is no
branch of physiology which is in a less satisfactory state than the whole
matter of the immediate nature, causation, and control of the photo-
mechanical changes.

The unwieldy literature of the subject is full of contradictory con-
clusions based on seemingly equally sound lines of evidence, on failures
to take account of the great individual physiological variability of the
lower vertebrates (particularly the amphibians!), and on simple ignor-
ance of other workers' results, especially of conclusive negations of some
of the pioneering researches.

We do not even know whether either extreme position of the retinal
pigment or of the rod or cone myoids represents a condition of relax-
ation, or whether the expansion and retraction of the pigment and the
elongation and shortening of myoids are all active processes. We can
glibly say that the movements of the pigment are "due to protoplasmic
streaming" but (though it could easily be ascertained on isolated epi-
thelium in vitro) we do not know whether the pigment cell can respond
in either direction, autonomously and directly, to light and darkness.
We have no conception whatever of the intracellular mechanism which
changes the length of a myoid, though these changes are enormously
greater than those which take place in a striated muscle cell whose
fibrillar machinery is fully revealed to microscopic view. And we are
greatly puzzled by the fact that apparently the same stimulus, or lack
of stimulus, which causes the myoid of one visual-cell type to elongate,
simultaneously causes the other to shorten. It is known that myoid vol-
umes remain constant at all lengths, and that shape-changes elsewhere
in the visual cells are purely passive. It is known that contractile cone
myoids respond by shortening in the presence of acids, and that retinae
which contain cones are acid in the light and alkaline in the dark.
Studnitz has injected phosphoric acid into dark-adapted fishes and found
that the pigment and cones took their 'light' positions. Injections of
alkali into light-adapted fishes made them dark-adapt. Studnitz thinks
that even the effects of adrenalin chloride are due to its acidity, not to
the hormonal base. To what it is that rod myoids respond, and how, no

152 ADAPTATIONS TO ARHYTHMIC ACTIVITY

one can say. Contractile ones look no different from non-contractile;
and there are such paradoxical situations as that in the frog, where the
common 'red' rods, with stubby myoids, have a respectable migration
while the scanty 'green' rods, with very long myoids like a teleost rod
or a dark-adapted frog cone, move but little if at all (see Fig. 23, p. 55).

The photomechanical phenomena are interesting enough and baffling
enough in their normal operation, but perhaps the most remarkable thing
about them is that they may actually work better when out of their
normal environment : it has been found that the pigment and cone move-
ments become almost twice as extensive in a salamander eye which has
been transplanted, in the larva, into the location of the ear!

As to the control of the movements, opinion is divided between two
schools of thought. Most of the work — not all — on fish material indi-
cates that efferent nerve impulses control the movements. Cutting one
nerve to the eye may halt the migrations, and cutting another in addition
may let them recommence. In one fish, the day-night rhythm of the retina
is known to persist even in constant darkness; nor does a frog stay dark-
adapted in darkness — in a few hours the cones elongate, then shorten.

Much of the reported work on amphibian material favors the idea of
control by blood-borne substances. Nerve-cutting has little effect, vessel-
ligation a considerable one. The transplanted eyes referred to above were
entirely divorced from nervous control, but adequately vascularized. The
effects of drugs, narcotics, and anaesthetics are ambiguous. The effects
of temperature are especially mysterious, for both high and low tempera-
tures cause light-adaptation in the dark and inhibit the dark-adaptation
of previously light-adapted animals. Excised dark-adapted eyes will light-
adapt readily, but excised light-adapted eyes will dark-adapt only in the
surprisingly special environment of a second frog's body cavity. Emo-
tional states interfere with the phenomena, but these could have their
effects by means of either nerve-impulses or hormones. Yellow light is
more effective than other colors, speaking either for a reflex control from
the visual apparatus itself (as in the case of iris reactions in higher ani-
mals) , or for a direct influence of acid, formed maximally in the retina
under yellow light. On the other hand, old evidence — still commonly
cited — for reflex effects from one eye to the other and from the skin to
the eyes is under grave suspicion, for in the experiments the animal's
breathing was interfered with and fear was introduced, by the employ-
ment of leather hoods. Either of these factors is now known to be
enough to make a frog light-adapt, though he be in darkness.

FUNCTIONS OF THE PUPIL 153

The whole subject requires a very careful review and deserves the
attention of at least one cautious investigator prepared to devote his
active career to it. Practically everything which has been done in the
way of experiments upon the mechanism of the phenomena needs re-
peating with better technique than has been used. Not a single experi-
ment has yet been made with all factors controlled, nor a single graph
plotted with nearly enough animals averaged at each point. The photo-
mechanical changes are so fascinating that their students have been a
little too impatient to know what makes them go.

(C) Pupil Mobility

Functions of the Pupil — The pupil ordinarily has two chief respon-
sibilities. It must fix the immediate illumination of the retina, if it can,
at a value above the threshold of stimulation and below the point of
dazzlement or injury; and it must restrict the perceived light-pencil to
the center of the lens as far as possible. The pupil may be relieved of one
or the other of these duties. Thus in the chameleons the lids are fused
to the surface of the eyeball and their opening is a small one which
'stops down' the broad lens without benefit of changes in pupil diameter.
Again, a strongly nocturnal animal may so conduct himself that he is
seldom or never exposed to bright light, and his wide pupil may not
need, or have, much ability to close down, to convert a dazzling external
illumination into a tolerable intra-ocular one.

Though not at all exceptional, such conditions are nevertheless assoc-
iated with the extremes of diurnal and nocturnal adaptation and be-
havior. The pupil may have little to do in a night-prowling species which
conceals itself well in the daytime and has no wish to bask in exposed
positions. It may have little to do in a sun-worshipper whose pure-cone
retina is so insensitive that various natural brightnesses above his thresh-
old are about equally comfortable to him. The slit pupils, so characteristic
of those nocturnal forms which do court the sunshine, deserve special con-
sideration beyond the scope of this discussion (see Chapter 9, section C) .

The need for considerable pupil 'excursion' — range of size change —
is thus the greater, the more the animal attempts to attain twenty-four-
hour visual capacity. In such animals the responsibility of the pupil and
its controlling mechanism is greatest also, for the two aims of the pupil
are increasingly at cross-purposes when the period of daily activity be-
comes longer and longer. In the brighter hours, the closure of the pupil

154 ADAPTATIONS TO ARHYTHMIC ACTIVITY

serves both of the aperture's functions equally well; but as the animal
attempts to make use of the evening and night hours, or to set back the
alarm-clock in the morning, the pupil must walk an increasingly precar-
ious tight-rope. It must open far enough to permit of stimulation, but
not so far that the blurring of the image takes more away from vision
than the increased light confers. Fortunately, as the intensity falls very
low, the widening pupil finally begins to add more to the quality of the
image, in brightness, than it takes away, by aberration. As day passes
into night, the now familiar acuity-sensitivity seesaw (p. 69) begins
inexorably to move. In any but a very strictly diurnal animal, sensitivity
goes up, perhaps very high; and in any and all animals, acuity inevitably
comes down.

A highly mobile, precisely controlled pupil prepares its owner for both
night and day. We have seen that the same can be said for a well-devel-
oped system of photomechanical changes. An active iris in a given animal
may be free to give its whole allegiance to illumination, or its movements
may be tied reflexly more closely to accommodation, convergence of the
two eyes, or emotional changes, or may even be under the control of
the will. The pupil may be so blocked by the lens that its closure is
impossible unless the iridic sphincter is able actually to compress the lens
(a possibility which, as an adaptation to amphibious habits, is realized
in some vertebrates) . In the majority of fishes, the blockage is so com-
plete and the lens so firm or so large that any attempt at pupil movement
is hopeless and the iris is actually devoid of muscle.
Pupillary versus Retinal Adaptation — Being more familiar with
movable pupils, we are likely to think of the photomechanical changes
in the retina as being able to save such situations, and take the place of
extensive pupil mobility. Historically, it has really been the other way
'round; for as we saw in the preceding section, the phylogenetic history
of the photomechanical changes has been one of fairly steady reduction
from a peak in the teleosts to complete absence in the mammals, the
birds being exceptional, since in them, despite their high position and
their mobile pupils, the photomechanical changes have been resuscitated
for special reasons which will later be set forth.

Concomitantly, there has been a steady development of pupil mobil-
ity — among twenty-four-hour and nocturnal animals — from nothing in
most fishes to a maximum in the mammals. We may reasonably expect
to find then, at any evolutionary level, one or the other of these regula-
tory mechanisms in good condition (consult Table II, p. 150).

PUPILLARY VS. RETINAL ADAPTATION 155

A pure-rod animal may need neither photomechanical changes nor a
mobile pupil, if he is content to be strictly nocturnal; and a diurnal ani-
mal will need neither very badly if he has a pure-cone retina and can
afford to be blind in dim light and utterly dependent then upon other
senses — as a pure-cone retina necessitates. But if a form whose retina is
duplex is to be able to appear indifferent to depth of water or to night
and day, or if a pure-rod animal is to be able to bask in comfort and to
defend itself from an enemy which routs it out of its daytime slumber, it
must have a widely excursive pupil or effective photomechanical changes.
Only one other mechanism, of limited value and with primarily other
functions, can sometimes be called into play for the regulation of stim-
ulation : the lid apparatus — sometimes, as regards its awning-effect, sub-
stituted for by projections on the upper part of the iris. The importance
of the lids in this connection can best be judged from instances in which
they are absent. Thus for example in the rays, the vipers, and the geckoes,
movable lids are lacking and the pupil is capable of an exceptional degree
of closure as compared with relatives which do have functional lids.

We can expect to find that a pupil will tend to open unless something
makes it close. The inherent elasticity of the connective-tissue stroma of
the iris tends to insure this, and in some animals, notably certain small
mammals in which a dilatator is lacking, it is the only antagonist of the
sphincter. Where there is a dilatator, it is a thin sheet, but a broad one ;
and its total bulk compares favorably with that of the sphincter. One or
the other may be the stronger in a given case; but the orientation of the
dilatator, other things being equal, gives it a big advantage over the
sphincter. It is as though the two muscles are pulling on opposite ends of
a lever of the first class, the ratio of whose arms is 3.1416:1; for the
sphincter, contracting around the periphery of a circle, must shorten
TT units while the radially-oriented dilatator relaxes one unit, and the
sphincter cells must be capable of contracting TT times as fast. Of course
if a pupil can move at all it can both open and close; but it is sometimes
more important for it to open in dim light than for it to close in bright.
Where the pupil is static, it is even more necessary for a nocturnal an-
imal to have a large one than for a diurnal animal to have a very small
one, for the latter can always partly close his lids. Where it is mobile,
it is more desirable for a nocturnal pupil to close promptly in bright
light than for it to open so suddenly in dim light, where the accumu-
lation of rhodopsin is very slow anyway. Hence it is that many a small
nocturnal animal has a powerful sphincter muscle and no dilatator at all.

156 ADAPTATIONS TO ARHYTHMIC ACTIVITY

In emergency situations, in the higher vertebrates, the pupil seems to
try to make sure of enough light — its response to pain, to rapid deep
breathing, or to strong emotion of any kind is to dilate, sometimes so fast
and far (as in the hyaenas) as to seem to be under the animal's control.
Close scrutiny of an object, ordinarily a calm and non-emergency proce-
dure, is on the other hand accompanied by contraction. This 'accommo-
dation reflex' is not a true reflex, but a fortunate accident of innervation.
The iris sphincter and the ciliary muscle are supplied by the same nerves.
The 'reflex', which in man occurs more with convergence than with the
accompanying accommodation, and is in that aspect truly reflex, is of
some value in all its possessors (though of most value in those vertebrates
whose irides actually aid in accommodation; see Chapter 11, section C).
In its accommodated form the lens has more spherical aberration. It
therefore needs more stopping-down, and receives this upon the reflex
closure of the pupil, thus increasing resolving power for approaching ob-
jects. As objects approach, the amount of light received from them in-
creases enough to compensate adequately for any accommodatory reduc-
tion of the area of the pupil.* Another pupil reflex in man, of no obvious
value, has recently been described : it consists of a slight contraction at
the moment of fusion of the two monocular images into a single stereo-
scopic one, as when one is observing through a stereoscope.

In the birds, whose photomechanical changes are more conspicuous
than one would expect from the phylogeny of the changes and of the
pupil, the reason appears to be that the bird pupil pays less attention to
illumination than to accommodation and emotion. The 'play' of the
pupil of a captive wild bird will readily convince one of this, though the
irides of tame birds, such as chickens, may react quite staidly to light.
There is thus no inconsistency in the fact that the birds have both iridic
and retinal photomechanical changes well developed (Table II, p. 150).

The behavior of the pupil is influenced more immediately, as well as in
in the long evolutionary run, by the presence or absence of retinal migra-
tions. The first reaction of a pupil (i.e., partial closure) upon a sudden
increase of illumination is not permanent. It gives opportunity for the
retina to reduce its sensitivity; and when this has been sufficiently effected,
the pupil slowly reopens to a size which is smaller than its original one,
and is constant until a further great change in intensity. This physiolog-

*In the dog, according to Nicolas, the accommodation reflex works backwards — the pupil
dilating for near, contracting for distant objeas; and there is no consensual reflex. These
peculiarities have yet to be explained.

PUPILLARY VS. RETINAL ADAPTATION 157

ical adaptation of the pupil is to be sharply distinguished from the imme-
diate reaction it gives to increased illumination. Upon a reduction of
illumination the pupil only dilates to a new constant size, there being
rarely a brief preliminary contraction. The rate of the complex light-
adaptation and of the simpler dark-adaptation of the pupil depends upon
the method by which the retina changes its sensitivity. When only cones
are present, as for example in diurnal snakes, the change in sensitivity is
slight and rapid and the pupil also makes quickly the slight adjustment of
which it is capable. Where many rods (but no photomechanical changes)
are present, as in the guinea-pig for instance, the light-adaptation of the
pupil is governed by the relatively rapid destruction of rhodopsin. Where
both rods and photomechanical changes are conspicuous the rhodopsin is
more abundant and, especially in fishes and owls, slow to bleach. The
pupil then adapts much more slowly (frogs) or not at all (fishes) , since
retinal sensitivity is altered primarily by the relatively slow pigment
migration. It is in fact quite probable that in the teleosts the rhodopsin is
seldom all bleached, since the rods are completely shielded by expanded
pigment. Higher vertebrates, it would seem, must be able to form more
rhodopsin since so much must be destroyed at every light-adaptation.
Very likely, the greater instability to light of the rhodopsins of higher
vertebrates (through which the rhodopsin is quickly destroyed, and the
threshold of the retina as quickly raised) is partly a consequence of the
lack of such perfectly protective photomechanical changes as the lower
vertebrates possess.

Pupil movements are thus not only less marked, but less rapid, in prim-
itive forms which still depend primarily upon retinal migrations. Phyloge-
netically there has been a steady perfection not only of the pupil as an
adjusting mechanism, but also of its method of actuation and control. In
the few fishes which have iris muscles, these are pigmented and respond
directly and autonomously to light — the sphincter by contracting, the
dilatator by losing tonus. These actions are extraordinarily slow — elas-
mobranch pupils take two or three minutes to close in bright light and
an hour or so to re-open in the dark! Such muscles are unresponsive to
electrical stimulation and to neurotropic drugs like atropin, since such
agencies operate through nervous connections. In the amphibians and
some reptiles some degree of autonomy persists, although in the intact
animal it is masked by the superposition of a control through the nervous
system by means of reflexes originating in the retina. In the frog it has
recently been reported that an intra-ocular reflex occurs — the pupil of the

158

ADAPTATIONS TO ARHYTHMIC ACTIVITY

excised eye contracts somewhat if the retina is stimulated. In the higher
vertebrates, at least in adults, reflexes alone are of importance although
some direct response is known to occur even in two or three mammals
and man; and emotional changes can now affect the pupil, though
whether this is incidental or not, useful or not, is difficult to say. In the
mammals, 'consensual' reflexes from one eye to the other appear: the
movement of both pupils when only one is stimulated (known only in
the rays and the pigeon, outside of the mammals) ; and the neurological
tie-ups of the pupil to accommodation and convergence become rigid.

Fig. 65 — Pupillary opercula in fishes (o- operculum ) .

a, eye of Raja clavata. x 2. After Franz, b, illuminated pupil of R. clavata. After Franz,
c, eye of a flatfish, Scophthalmus rhombus, as seen from above. x3. From Franz, after
Grynfeltt and Demelle. d, upper part of head of stargazer, Uranoscopus scaber. x 4.
Redrawn from Hein. /- lower 'lid'; s- limit of sulcus under lower 'lid', e, f, g, stages in
the expansion of the operculum of a loricariid catfish, Plecostomus. Redrawn from Roth.

Comparative Survey of the Two Methods — In the lampreys there
are no iris muscles and most observers agree that the pupil is static. The
lens touches the cornea and blocks the pupil, and the mechanism
of accommodation (Chapter 10, section A) is such that this relation-
ship is never changed. There are no photomechanical changes in lam-
preys; but their eyes as a whole are built for diurnality. When lampreys
do swim at night, as when going upstream to breeding grounds, they are
in all probability depending upon senses other than vision (like diurnal
birds migrating at night) .

COMPARATIVE SURVEY OF THE TWO METHODS 159

The elasmobranchs are conspicuous among the fishes for having highly
mobile (though excessively slow — v.s.) pupils. The sphincter is unusual
and primitive in that it is never separated from the epithelium which
generates it, as in other vertebrates. They have no retinal photomechan-
ical changes — indeed, no retinal pigment except in the extreme periphery
to which the tapetum lucidum does not reach. Most forms are active
principally at night, but some like to doze, basking, at the surface. A
few may be found active at any hour, and a considerable number live in
the deep sea and are in a constant environment as regards light. The
light-lovers have broadly elliptical, usually vertical pupils which dilate to
circles in low illuminations. The more strongly nocturnal species have
more mobile pupils which close in bright light to narrow slits set diag-

Fig. 66 — Eye of a shark, Squalus acanth-

ias, showing mydriatic pupil rigor, x 1.

Redrawn from Franz.

a, when pupil is freshly illuminated.

b, after illumination of long duration.

/ o/a

Fig. 67 — Dorsal iris-angle region of a teleost,
Chrysophrys aurata. After Grynfeltt.

a- argentea; al- annular 'ligament'; cm-
ciliary muscle; d- dermal contribution to
cornea; i- iris; ip- inner portion of primary
cornea; n- nerve; op- outer portion of pri-
mary cornea; ot- ora terminalis; pc- pars
ciliaris retinae; pi- pars iridiaca retinae; sl-
suprachorioidal lymph space; so- scleral
ossicle; v- blood vessel.

onally or horizontally. They are thus safe from dazzlement and defense-
lessness when they come up to sun themselves. The flattened, upward-
gazing rays are provided with an 'operculum' which can expand to fill
the pupil from within (Fig. 65). The electric ray or torpedo, however,
relies upon a horizontal slit, which a tiny operculum can divide in the
middle. The pupils of elasmobranchs need not necessarily hold their full
contraction in bright light, but are privileged to reopen again after a
time just as though photomechanical changes had taken place — for these
fishes have photomechanical changes in the chorioid which alter the sensi-
tivity of the eye (see Chapter 9, section D) . Some sharks (e.g., Squalus,
Mustelus) in fact develop a 'mydriatic pupil rigor' if kept for several
days in a lighted room — their pupils become widely open and refuse to
close down when additional light is thrown on them (Fig. 66) .

160 ADAPTATIONS TO A RHYTHMIC ACTIVITY

The sturgeons are elasmobranch-like in habits as well as otherwise.
Their pupils (Acipenser fidrescens, Scaphirhynchus platorynchus) are
broad, pointed vertical ellipses or rhomboids, which appear to move only
passively as the lens blocks or unblocks them (in accommodation ?) . The
other chondrosteans, and the holostean fishes, have not been studied.
The lungfishes have no iris muscles although one (Protopterus) has a
mobile pupil. Here the contractility of the unmodified epithelial cells of
the pars iridiaca retinae seems to be involved, as possibly also in a few
teleosts.

Among the teleosts only the eels and the flattened upward-lookers
(e.g., Uranoscopus and Lophius) have much pupil excursion. The com-
mensal pearl-fish, Encheliophis (=Fierasfer) jordani, also has the eyes
aimed upward and is highly exceptional in that its pupils can close to a
mere dot. Many of the flounders and their relatives, and one or two arm-
ored catfishes, have a pupillary operculum (Fig. 65). Most teleosts have
no functional iris muscles whatever, though the non-contractile 'sphincter
of Grynfeltt' is often present. In atypical eyes, like those of Periophthal-
mus, a functional sphincter may be present without a dilatator. The lens
bulges far through the pupil except when pulled backward in accommo-
dation, but does not necessarily actually block it, for in many species
a narrow 'aphakic' (lenseless) space surrounds the lens. The teleost iris
is usually so anchored to the cornea by the so-called annular ligament
(more properly, 'iris angle tissue' — Fig. 67, al) that any iris muscles
would be powerless to alter the pupil. In the minority which do have
iris muscles (and weak annular ligaments) these are peculiar in that the
dilatator consists of true, discrete muscle cells lifted free of the posterior
epithelium and embedded, like the sphincter, in the stroma.

Most teleosts thus depend upon retinal photomechanical changes, which
were evolved by these fishes or by their holostean ancestors. The retinal
movements control stimulation well enough and the animal does not miss
the stopping-down effect of a contractile pupil because of the peculiar
optics of its eye. One would expect the spherical lens to have an excessive
degree of spherical aberration and to need more stopping than the flatter
lenses of terrestrial forms. But the teleost lens has a radially graduated
index of refraction and the retina is a spherical surface, concentric with
the lens. Hence the retina receives a sharply focused image from any
angle and the eye is in effect both periscopic and aplanatic. Constriction
of the pupil would serve no useful purpose. Indeed, the pupil margin
need not overlap the lens at all; and the iris may even be lacking, as in

COMPARATIVE SURVEY OF THE TWO METHODS 161

some deep-sea fishes (Fig. 84c, p. 213), the lens then being huge and
filling the anterior chamber. The teleost pupil may close slightly in
accommodation, probably passively due to its elasticity, when unblocked
by the receding lens; but this is quite meaningless not only because the
lens needs no differential stopping (being fixed in shape), but because
the active accommodation of teleosts is for distant, not near, objects
(see Fig. 98, p. 251).

The pupils of amphibians have more excursion than those of teleosts,
though not as much as they would need if the amphibians did not have
rather good photomechanical changes. Thus the frog, despite its poten-
tially sensitive duplex retina and its extremely large rods (Fig. 64,
p. 148) , has a pupil identical in behavior with that of a pure-cone grass
snake devoid of photomechanical changes. If the frog also lacked retinal
photomechanical changes, his pupil would have to close farther than it
does to permit him to be out where the snake could see him! A few anur-
ans have peculiarly shaped pupils. That of Bombina contracts to a play-
ing-card 'heart'; and in those whose retinae are probably the most sensi-
tive, the spade-foot toads (Scaphiopus spp.), the contracted pupil is a
vertical lozenge, the playing-card 'diamond'. The two other suits of the
deck are apparently not represented among amphibian pupils, but there
are still other weird shapes whose meaning is quite unknown (Fig. 87,
p. 223).

The weak amphibian sphincter pupillae is replaced by a much more
powerful one in the reptiles and here, as in birds also, the iris and ciliary
muscles are of the striated variety. This change may have been inevitable
upon the supervention of a control which is almost completely nervous
and sometimes voluntary, though the return to smooth intra-ocular
muscles in the mammals argues against this supposition. At any rate,
the sauropsidan iris is capable of extremely rapid action, though par-
ticular species do not necessarily ever tax this capacity. The turtle pupil,
fish-like, is blocked by the lens and does not respond to light at
all, contracting only as an accessory to accommodation. Turtles have
practically pure-cone retinae with slight, slow retinal migrations or none
at all. Their insensitive eyes require neither type of protection from
strong light, and in turn limit their possessors to photopic vision and to
dependence upon olfaction in dim light or muddy waters.

In diurnal lizards the iris is but slightly responsive to light, as is true
also of diurnal snakes, some of which have quite motionless pupils.
Nocturnal lizards are usually pure-rod, and nocturnal snakes are rod-

162 ADAPTATIONS TO ARHYTHMIC ACTIVITY

rich or even pure-rod. Many species in both categories are fond of
basking, and the geckoes are often active in the brightest of Hght. This
twenty-four-hour activity is made possible by great pupil excursions,
which are perhaps exaggerated by the absence of movable lids. Thus,
some geckoes if not most or all, and even one or two snakes {Leptodeira
annulata, for example) can close their pupils completely. The gecko,
with a large eye and retinal image, and a retina which, though pure-
rod, often has excellent resolving power (since the rods are but little
summated and owe their sensitivity to their size and to their rich content
of rhodopsin) has probably the best allround, night-and-day eye of
any vertebrate below the mammals.

The crocodile group is nocturnal. Its members, notoriously fond of
basking, depend for the protection of their sensitive duplex retinae upon
the lids and pupil rather than the retinal photomechanical changes, which
are here at a low ebb. Highly active pupils, among the reptiles, thus
go with pure-rod and duplex retinae and are the more mobile, the more
the species or group scorns concealment in the daytime. The circular
pupils of the diurnal majority are relatively or quite inactive, as would
be predicted from their pure-cone retinae.

Bird pupils are very active, but the photomechanical changes have
made a phylogenetic 'come-back' in this group. The paradox is resolved
when one notes the lack of precise adjustment of the avian pupil to
illumination. It plays so much that, although experimental proof is as
yet lacking, many workers have suspected it of being under the bird's
voluntary control. At any rate, it is easy to understand why in the birds
the retina has had to re-assume the responsibility of regulating its own
stimulation — the pupil cannot be trusted to do so.

Mamimalian pupils — except those blocked by enormous lenses in some
strongly nocturnal forms (Fig. 71, p. 173) — are comparable in mobility
with those of birds, but are better-behaved with respect to intensities and
thus make retinal migrations quite superfluous. Excursion is greatest, of
course, in nocturnal forms which love to bask, like the cats and foxes.
It is reduced in many ungulates, and is least in crepuscular forms such as
the bats, in secretive night-prowlers, and in such sun-worshippers as the
ground-squirrels. In short, the more constant are the illumination-condi-
tions in which a group prefers to be active, the less mobility the pupil
exhibits. The pupil closes almost completely in Tarsius, Pedetes, dormice,
and cats, very far in the otters and (by means of an operculum) in some
whales. It has an exceptional range of movement in the seals — but not

DUPLICITY AND TRANSMUTATION 163

primarily, strange to say, for the regulation of intra-ocular illumination.
The unique physiological role of the seal's pupil will be found explained
on pages 446-8.

In the mammals, the retinal photomechanical changes are entirely
gone. In this group of vertebrates we see the end result of the evolution-
ary replacement of those older equalizing devices by the more rapid,
hence highly superior, one afforded by the iris musculature.

(D) Duplicity and Transmutation

The duplex retina itself is clearly an adaptation for the extension of
the seeing-period over a greater number of the twenty-four hours. Rods
and cones are homologous inter se, and one type must have preceded
the other in evolution; for, an intermediate type of visual cell partaking
equally of the qualities of modern rods and cones is quite impossible
of conception.

The accepted belief is that the rod is the more ancient and that the
cone is an improvement upon it; but what real evidence there is points
to the exact reverse of this view. The problem involved here reminds one
of the question: "Which came first, the hen or the egg?" but it is not
without theoretical importance in connection, particularly, with color
vision. The evidence derives largely from the embryology of the visual
cells as interpreted in phylogenetic terms. There is not space here to set
it forth in detail, so the designation of the cone as primitive is bound to
seem a little arbitrary.

Considering the flagellar origin of the outer segment (see Fig. 55,
p. 127) the percipient parts of ancient visual cells must have been
filamentous before they could have become massive, and we cannot
imagine the pro-vertebrate to have possessed already so ingenious a
material as rhodopsin or to have been anything but a strictly bright-
light, pelagic organism. Until some of the visual cells became enlarged,
and grouped in their connections to ganglion cells, there could be no
increase in potential sensitivity which could release the animal from
bondage to the sun; and until the invention of rhodopsin, there could
be no visual activity by moonlight. But withal there must be no whole-
sale conversion of visual cells if the capacity for daytime activity was
to be retained — else the animal would merely have succeeded in shifting
the active period without substantially extending it. Improvements in
the dioptric apparatus making it more and more desirable, for the sake

164 ADAPTATIONS TO ARHYTHMIC ACTIVITY

of form-perception, to retain cones as well as the newer rods, the duplex
retina as we know it today finally crystallized in a condition which made
it possible at last for an animal to become arhythmic if various consider-
ations made that desirable. A mechanism for discriminating hues was
probably added rather late as a refinement whose first purpose was far
from the aesthetic one which color-vision seems, to our anthropocentric
minds, to serve (see pp. 463-4) .

Present-day pure-cone retinae are thus no more primitive than pure-rod
ones, for both represent the secondary discard of a cell type for the sake
of extreme speciaUzations — which, as always, demand in payment the
surrender of plasticity. And, not only have various vertebrates at various
times swung from twenty-four-hour capacity toward diurnality or noc-
tumality, but they have returned from one extreme through arhythmicity
or crepuscularity and even gone on to the opposite extreme.

Wherever even a few cones have been retained in a rod-rich retina,
or a few rods in an almost pure-cone one, manipulations of sensitivity
need be only quantitative and are as readily carried out in evolution as
an alteration of the ratio of white blood cells to reds. But where the
ancestors of a given group retained only one visual-cell type, it might
seem impossible for any descendants ever to produce the other. Exactly
this has happened, however, and apparently far more often among the
reptiles than in any other extant group. Historically, these were the first
vertebrates to feel fully the strain of being highly active without benefit
of a high body temperature. Not only were they deprived of the warmth
of the ancient waters, but they were without the energy-saving buoying
effect which a fish enjoys. A little exertion goes a long way when the
weight of the body is supported by water, and the tenderness of cooked
fish flesh, like that of the disused flight muscles or 'breast meat' of a
chicken, is a reminder of the easy lives such muscles lead.

It is not surprising that in the first terrestrial groups (the stego-
cephalians and the reptiles) many sub-groups tended early to develop
strong diurnality and pure-cone retinae, counting upon the warmth of
the sun to speed metabolism to a degree which would permit of athletic
agility in the search for food. Moreover, diurnality was an especially
safe habit because of the temporary paucity of enemies on land. But the
reptiles have had their heyday and have perforce yielded their place in
the sun to the more successful birds and mammals. Most reptiles are
still strictly diurnal, but as their enemies have multiplied and their
average size has steadily decreased since the days of the dinosaurs, many

DUPLICITY AND TRANSMUTATION 165

have come to be grateful for the shield of night over at least a part
of their activities.

To regain a duplex retina and twenty-four-hour capacity — let alone
to go still further on into nocturnality, loose or strict — the pure-cone
reptiles have had actually to convert or transmute some or all of the
cones into low-threshold, massive, cylindrical elements. In most cases
these have been able to re-invent rhodopsin and thus fully deserve to
be called rods. Intermediate stages in these transmutations can be seen
in living species, which show us therefore some of the steps by which
the original duplex retina may have come into being in the earliest verte-
brates. The conversion of a diurnal reptile into an arhythmic or noctur-
nal one may be illustrated by considering a series of snake species which,
though quite unrelated to each other, each exhibit a stage of adaptation
through which the subsequent members of the series must once have
passed.

All round-pupilled snakes have only cones, of three types as shown
in Figure 26a (p. 63). Two of these are single, one large and abundant
(Type A) , the other small and scanty (Type C) . The third is the unique
double cone (Type B) invented by the higher snakes to replace the lost
double cones of their lizard antecedents (see Fig. 24, p. 59) .

In N. ndtrix, for example, these cone types are normal and typical.
Cemophora is a secretive snake in which the Type A and Type B outer
segments have enlarged, thus lowering their thresholds; but the biggest
change is in the Type C elements. These are no more numerous than
usual, but they have become rod-like in form (Fig. 68a).

The mud-loving and secretive rainbow snakes, Farancia and Abas tor,
maintain the large cone outer segments, and in them the numbers of the
stubby Type C rods have increased until they equal or exceed the total
number of "A" and "B" cones. The Type C elements probably still lack
a rhodopsin at this stage of transmutation.

Any pit-viper, such as Agkistrodon, shows the next logical steps. The
rods have multiplied until they have a human-like abundance relative
to the cones (Fig. 68b) , and they are longer than in the rainbow snakes
and now contain rhodopsin. With this retina, and a small eye with a
small, bright image, the pit-viper has enough sensitivity to require con-
siderable pupil mobility, and the animal can prowl at night and bask in
comfort and safety in the daytime, sometimes even feeding actively then.

From the perfected duplex retina attained in the pit-vipers, among
many others in which this same secondary adaptation to day-and-night

166

ADAPTATIONS TO ARHYTHMIC ACTIVITY

vision has occurred, still further steps may be taken. Thus in Leptodeira
the rods are very numerous, long, and slender, and the bodies of the
cones have gotten up out of their way, their ellipsoids being perched on
the tips of the rods like so many pumpkins on a picket fence (Fig. 69) .
The cone outer segments themselves are very much larger than in
pure-cone diurnal forms like N. natrix, Coluber, etc. Rhodopsin is
abundant in Leptodeira, and the retina is so sensitive that the pupil
closes completely like that of a gecko. In Tarbophis and Dasypeltis the

Fig. 68 — Transmutation in snakes, x 1000.

a, visual-cell types of a secretive colubrid, the scarlet snake, Cemophora coccinea. Compare
Figure 26, p. 63. Types A and B have enlarged outer segments, but Type G (which is
greatly outnumbered by A + B, as in diurnal forms) is the most rod-like of the three.

b, visual-cell types of a crotalid, the copperhead, Aghstrodon mokasen. Types A and B
have remained cones, but Type C (which greatly outnumbers A-i-B) is a perfea rod and
contains a rhodopsin.

cones seem definitely to have lost importance, for while they are still
elongated far beyond the usual position, their bodies and outer segments
are much reduced in size as compared with Leptodeira. In these three
genera (as also, it happens, in the flying-squirrels) the visual cells are in
a condition of 'permanent dark-adaptation' (in terms of the photome-
chanical changes, which do not occur in snakes or squirrels) and the
animals are strongly nocturnal — thus really lying beyond the scope of
this chapter though serving to show the lengths to which a species can
go, if it must, to change its habits and their structural basis.

DUPLICITY AND TRANSMUTATION

167

There are other cases in which nearly all (S phenodon) or absolutely
all the cones of a pure-cone forebear have been transmuted into rods;
and the result is not necessarily a strictly nocturnal animal, for the pupil

O.N.

J

:^ L^rsen

(^ ^ e-G.

G LarsGn
b

Fig. 69^ — Duplex snake retirice. x 500.

a, a nocturnal colubrid, Leptode'tra annulata, whose rods (derived by transmutation from
the Type C cones of a diurnal ancestor — compare Fig. 26) are very numerous, and whose
cones have taken a position which, in terms of the photomechanical changes of lower verte-
brates, might be called one of permanent dark adaptation.

b, for comparison, a boid, Tropidophis melanurus, whose simple, duplex retina is more
ancient than the cone-simplex one from which the Leptodeira pattern was evolved.

C- cone; D.C.- double cone (= Type B); S.- ganglion-cell layer; I.N.- inner nuclear layer;
L.- limitans; O.N.- outer nuclear layer; P.E,- pigment epithelium; R.- rod; S.C.- single
cone (=Type A).

is so well developed in some reptiles that it can often make possible
twenty-four-hour activity even when, behind it, lies a pure-rod retina.
Round-pupilled lizards have only single and double cones, which in

168 ADAPTATIONS TO ARHYTHMIC ACTIVITY

Xantusia have enlarged their outer segments and lost their oil-droplet
pigment. The geckoes have still further enlarged the outer segments,
discarded the colorless oil-droplets, and re-invented rhodopsin. In
Coleonyx, for example, the transmuted rods are enormously long cyl-
inders (Fig. 25, p. 62) and, though sensitive in the extreme, are ade-
quately protected by the slit pupil from dazzlement in the daylight. At
the same time, the rods of Coleonyx are slender enough, and little-enough
summated, to aflFord respectable visual acuity. Thus Coleonyx has been
able to become arhythmic by installing a hinge in the middle of the sensi-
tivity-acuity seesaw. The geckoes can be comfortable in bright light with
a pure-rod retina, while their diurnal lizard relatives, with pure-cone ret-
inae, are completely blind in dim light. It may be a little clearer now, why
diurnality is a more restrictive habit than noctumality; for while a pure-
cone animal cannot see anything, even hazily, at night, a duplex or even
pure-rod species can always see in the daytime, though perhaps not acute-
ly — the real danger being that he will see too much light (bats, owls) if
his share of photomechanical changes, pupil mobility, or lid apparatus is
unable to reduce the stimulation of his rods to a comfortable value.

Pure-rod snakes, as well as lizards, exist by virtue of transmutation. A
few pure-cone ones (e. g. Lampropeltis , Rhinocheilus) have increased
sensitivity somewhat by enlarging the outer segments, eliminating color-
filters (yellow lenses) , and by hooking up more cones to each optic nerve
fiber. Arizona and Trimorphodon have carried these processes so far that
their pupils have had to become elliptical, and in Hypsiglena and Phyl-
lorhynchus (Fig. 26b, p. 63) the visual cells are all morphologically rods
though devoid of rhodopsin. When we can observe so clearly the second-
ary, apparently easy derivation of unquestionable rods from indubitable
cones, it becomes easier to understand why both of these so diverse cell-
types are usually required for a well-rounded visual capacity. And, it is a
little easier to see that in order to become duplex, and thus more widely
useful, the cone-like receptors of the provertebrate retina could spawn
rods without necessity of their having to be formed de novo from a sepa-
rate cellular ancestor. The first rods in the world were produced by the
transmutation of cones, and the process has been occasionally repeated,
wherever needed, ever since the vertebrates came on land.

Chapter 8
ADAPTATIONS TO DIURNAL ACTIVITY

(A) DiURNALITY AND THE EyE

D'turnality and Sharp Vision — The adoption of diurnality entails a
sacrifice of sensitivity. This is hardly possible without a marked increase
of visual acuity, for if the cones are multiplied at the expense of the rods,
resolving power inevitably rises. While it is theoretically possible for an
animal with a pure-rod retina and crude vision to be strictly diurnal,
given the right type of pupil, in actual fact it never happens.

Adaptation to diurnality is thus, at the same time, adaptation for sharp
vision. Diurnal animals are relatively keen-sighted, and their other habits
are such as to demand keen sight; but it is of course impossible in most
cases to say whether they are diurnal and cone-rich in order to have sharp
vision (which is probably true of the birds) or have only cones simply in
order to be diurnal, without making the most of the opportunity to gain
sharp vision (which may hold for the snakes) . The relationship between
visual acuity and diurnality, in so far as it expresses needs and the pro-
duction of adaptations to fill those needs, is perhaps most easily seen in
a rough analysis of feeding habits :

Diurnality, Acuity, and Food — Animals which feed upon small ob-
jects such as seeds and insects must be able to resolve them, which is pos-
sible only for an eye rich in cones and hence diurnal in capacity. Most
lizards, birds, and primates are in this category; as are also the tree-
shrews, at least, among the insectivores. It is important to remember that
insects themselves are poikilothermous, hence most species are most active
and available under diurnal conditions. Nocturnal insect-feeders can
place no reliance upon vision, but must either rely upon hearing and
touch for securing individual insects (bats) or else 'trawl' blindly through
the air for flying insects with wide-open mouth (goatsuckers, frog-
mouths) . The dependence of most birds upon sunlight is proverbial. So
is their visual acuity. In this respect, man acknowledged even the small
birds to be his superior, centuries ago — it was the habit of the medieval
falconer to carry a caged shrike on his saddle, to keep track of the falcon.
As long as the shrike acted fearful and excited, the hawker knew that his
proud tiercel was in sight — though not to him\

169

170 ADAPTATIONS TO DIURNAL ACTIVITY

Poikilothermous vertebrates, generally, may be diurnal for the sake of
the activating effect of sunlight upon metabolism and locomotor activity,
unless they happen to be particularly defenseless or especially dependent
upon prey which in itself is nocturnal. Predaceous fishes, most reptiles,
and some frogs fall here.

Predaceous vertebrates, generally, require fairly sharp vision at rela-
tively close range in order to pursue and capture prey and obtain a grasp
upon it which will be advantageous to them in any ensuing combat. Be-
ing ordinarily swifter than the prey — at least for short bursts — there is
added need for acuity of vision, which must keep pace with speed if
'crashes' are to be avoided. These factors are especially operative in
fishes, lizards, and birds; and they are largely responsible for the acuity-
adaptations tenaciously retained by those carnivorous mammals which
attempt to compromise between sensitivity and acuity by having large
eyes. Small, small-eyed carnivores on the other hand are nocturnal,
largely because the small prey animals which they are able to master
have taken refuge from them in nocturnality.

Defenseless, herbivorous prey animals which rely upon speed for escape
must recognize enemies at a distance. This in itself demands high visual
acuity; and the factor of distance, besides reducing the retinal-image size
of the potentially dangerous object seen afar, greatly reduces its bright-
ness. Vision at a distance is therefore altogether impossible in dim light.
The ungulates, and the more strictly diurnal mammals, must have high
visual acuity for safety, and their acuity-devices will work only under
bright-light conditions. Lastly, predators which specialize on diurnal prey
must ordinarily be permanently or temporarily diurnal themselves — the
hawks, for example, as also the bear during his annual gorge on salmon.

However, we must not suppose that in every act of predation both par-
ties are under optimal conditions and fighting to best advantage. On the
contrary, many a predator is nocturnal in order to seek out prey which,
being itself diurnal, is asleep at night and hence at a disadvantage. Con-
versely, the diurnal predator may depend not upon diurnally active food
animals, but upon nocturnal ones which, sleeping in their burrows by
day, are then easily surprised and subdued. The diurnal snake exploring
the nests of slumbering rodents, the nocturnal marten investigating a
squirrel's dray, are examples of these advantageous employments of the
sleep-time of the victim.

We can easily imagine that diurnality and nocturnality have come and
gone, sometimes repeatedly, in particular lines of descent. Prey animals

DIURNALITY, ACUITY, AND FOOD 171

have become nocturnal to avoid predators. Predators have in turn be-
come nocturnal to continue to find food easily. To escape the nocturnal
predators, prey animals have again become diurnal. Those species and
groups which could not invert their habits at need were doomed unless,
by sheer weight of numbers, by phenomenal fecundity, they were able to
compensate (as species) for the enormous losses of ill-equipped indi-
viduals.

The Eye as a Whole — For an eye to mediate sharp vision, an essential
requirement is a large retinal image. The greater the number of visual
cells over which the image is spread, the greater the resolution of the de-
tails of the image. The histology of the retina is a very important factor
but, after all, it can only say the last word in the story the eye tells the
brain. There are strict limits to the fineness of the receptor mosaic, and
its performance is in turn limited by the size of the image presented to it
by the dioptric apparatus.

The simplest way to gain a large image is to have a large eye; and
'large' here refers to absolute, not relative, size; for whereas with other
organs of the body it is relativity to each other that determines adequacy
of size, the eye is essentially an optical instrument and obeys the laws of
inter-organ proportioning only grudgingly, disobeying them entirely
whenever, with impunity, it can. Biologists tend to overlook this fact, and
frequently remark of large animals, such as the whales, that "their eyes
are so small in proportion that they must be just about useless"— forget-
ting that the world looks the same size to a whale, a man, and a mouse.
They all see as much, but not as well. Were a squirrel as big as a horse,
it would have an eye as big as a horse's; but that is not to say that if a
horse were as small as a squirrel, it would see as well with an eye propor-
tionately small. The squirrel would, on the other hand, be much better
off with eyes as big as a horse's — if it had room for such eyes in its head.

The big reason for this fact — that it is absolute rather than relative size
which, ceteris paribus, determines visual acuity — is that the absolute
dimensions of retinal elements vary within only narrow limits however
large or small the eye may be. Tripling the diameter of the eyeball does
not entail tripling the diameter of a cone visual cell. Rather, it results in
a tripling of the number of visual cells in a given linear distance on the
retina. The image is then three times as broad, and visual acuity is en-
hanced threefold.

In practice it is only exceptionally that high visual acuity can be gained

172

ADAPTATIONS TO DIURNAL ACTIVITY

merely by having a large eye whose parts are proportioned as they are in
small twenty-four-hour eyes. It is only in large animals such as the ungu-
lates and the great cats that we find high visual acuity attributable prin-
cipally to large ocular size as such.

Where the habits of the animal demand that he go all out for visual
acuity, we find the eye to be large both absolutely and relatively. Thus in
the birds the eyes are proportionately colossal and occupy so much of the
head (Fig. 70) that their fundi may actually roll upon one another in

Fig. 70 — Eyes and brain of the English sparrow, Passer domesttcus, in situ, from the ventral
side. X 5^^. Redrawn from Wood and Slonaker,

c- optic chiasma; e- external rectus; g- Gasserian ganglion; h- Harderian gland; in-
inferior rectus; io- inferior oblique; ir- internal rectus; /- lacrimal gland; m- medulla;
o- optic nerve; ol- optic lobe (midbrain); p- pituitary; 5- third cranial (oculomotor)
nerve — supplies the superior, internal, and inferior reai and the inferior oblique; 4-
fourth cranial (trochlear or pathetic) nerve — supplies the superior oblique; 5- fifth cranial
(trigeminal) nerve, several of whose branches carry fibers to the eye and adnexa; 6- sixth
cranial (abducens) nerve — supplies external reaus.

the mid-plane of the skull, like a pair of segmental gears. Only in species
of little brain can such things be.

The partial dependence of resolving power upon absolute ocular size
has a consequence upon relative ocular size. It has been stated as a law
that eye size is inversely proportional to body size (Haller's ratio) . The
reason why this should hold for nocturnal forms as well as for diurnal
ones will be given in the next chapter; but it is a very different reason.
Keeping only diurnal forms in mind, it is easy to see why the eye should

THE EYE AS A WHOLE

173

be relatively large in, say, small birds and yet relatively small in such an
animal as the horse. Though the horse has larger eyes than any other
land mammal, there is ample room for even such large eyes in the head.
The small bird must give over a far greater proportion of the head to the
eyes if they are to be large enough in actual measurement.

NOCTURNAL:
5

ARHYTHMIC:

DIURNAL-

Fig. 71 — Intraocular proportions in relation to intensity habits.
Redrawn from various sources.

inferior side of eyeball; n- nasal side; s- superior side; /- temporal side.

Another factor which, by operating upon actual ocular size, has its
effect upon relative ocular size, is locomotor speed. Great speed demands
high resolving power for better perception of movements and for the
avoidance of collisions (Chapter 10, section E) ; and this calls for a large

174 ADAPTATIONS TO DIURNAL ACTIVITY

eye. In predaceous fishes, lizards, birds, ungulates, squirrels, and other
swift and agile forms, large eyes go with swiftness of movement (Leuck-
art's ratio).

Wherever the eye of a diurnal animal is actually small it may be that
visual acuity is low because, considering the animal's habits and needs,
it need not be any higher. This is the situation in the snakes. Far more
often, the eye is small because there is simply no room for a larger one.
Internal adaptations then appear, which compensate for inadequate size;
and the same adaptations occur in even very large eyes, supplementing
the effect of size per se, wherever maximal visual acuity is desired.

These internal rearrangements usually consist at least of a flattening
of the lens and a shallowing of the anterior segment of the eyeball. (It
should be remembered that the anterior segment is not defined as the an-
terior halj of the eyeball, in front of the equator, but as the portion anter-
ior to a plane tangent to the back surface of the lens. This may com-
prise very much less than half of the volume of the eye). These changes
have taken place in the birds and are perhaps most marked in the
chameleon and in the higher primates (Fig. 71). The squirrels are
conspicuous for having more nearly spherical lenses than other strictly
diurnal vertebrates. The human eye, among mammalian eyes in gen-
eral, is atypical in the other direction, in its possession of so very flat
a lens. One gets the impression from the human, as also from most bird
eyes, of an ordinary-sized anterior segment grafted onto an oversized
posterior segment which 'doesn't belong' to it. This impression is actually
quite true to the facts, for it is not that the parts of the anterior segment
have been made smaller in order to gain visual acuity, but rather that the
fundus of the eyeball has been made larger, the lens then flattening in
order to move the focal level back onto the now more distant retina.
The fishes are peculiarly fortunate in that they are able, because of the
extraordinarily high refractive index of the lens, to obtain a broad image
without the eye having to be as deep as it is broad. The fish eye is con-
sequently flattened (Fig. 77b, p. 185) and encroaches less upon the in-
ternal structures of the head.

The effect of this alteration of the relative size of the anterior and pos-
terior segments is to move forward the nodal points of the dioptric sys-
tem. The distance from the optical center to the retina being thereby in-
creased, the image enlarges just as it does when we draw a stereopticon
lantern farther away from its screen. For the greater distance of 'throw'
of the image, the lens must now bend the light-rays less sharply if they

THE DIURNAL RETINA 175

are still to focus on the retina; hence the reduction of its sharpness of
curvature. If we imagine the acuity-requirements of an animal to be stead-
ily increasing through evolution, we may visualize the consequent gross
changes in the eye thus :

1. A steady increase in absolute size until the eye is relatively large
if the animal is small. If the animal is large, the eye may then still be
relatively small though absolutely large. The result is an enlargement
of the image and an increase in resolving power since the visual cells do
not enlarge proportionately, but instead become more numerous per
angular unit of the image.

2. A faster growth of the fundal portion, the anterior segment be-
coming, more and more rapidly, relatively small as compared with the
posterior. The result is an increase in the size of the image relative to
the size of the eye, with a consequent increase in resolving power.

3. A relative or an absolute forward movement (or both) of the
optical center of the cornea-lens system, further expanding the image
owing to the increased distance from optical center to retina (Fig. 71).

4. A relative diametral shrinkage and flattening of the lens or the
cornea (or both) , increasing the focal length to suit it to the increasing
distance from optical center to retina.

5. A relative diminution of the size of the pupil and of its excursion
of movement, there being abundance of light entering the eye under
diurnal conditions (so that the pupil can be small) and, in the pure-cone
retina in which diurnality tends to culminate, a restricted range of sensi-
tivities (so that there is no point to having the pupil capable of opening
very widely or of closing extremely) .

(B) The Diurnal Retina

ConeiRod and Receptor:Conductor Ratios — The diurnal retina is
invariably rich in cone-substance. This clumsy term must be used in at
least this one place, for the sake of emphasizing that it is the relative
total masses, not the numbers, of cones and rods which count in retinal
adaptations to sensitivity. For, an animal may have dozens of rods to
every cone and still be suited best for diurnal activity — if the rods are
tiny and the cones massive. This is actually the case in the bright-light
teleost fishes (Fig. 22b, 23c, p. 54). Apart from them, the rule is that
relative numbers of cones-per-rod are high in diurnal forms, low in
nocturnal. And within the teleost group, this rule of numbers of course

176 ADAPTATIONS TO DIURNAL ACTIVITY

holds. Wunder made counts in a number of species, and found the
greatest number of rods (810,000 per square miUimeter of retina) in the
nocturnal Lota. Lota also had the fewest cones (3400/sq. mm.), the
diurnal Tinea the most (9000/sq. mm.). The catfishes, however, have
thick rods in their crude eyes. Wunder found no other teleost with so
few rods as Amieurus (l8,400/sq. mm.), whose rods are almost am-
phibian in plumpness (c/. Figs. 63 and 64, pp. 147-8) .

The most strictly diurnal vertebrates have only cones in their retinae.
Among these are the great majority of lizards and snakes (all of those
with round pupils), some (perhaps many) birds, and the majority of
the members of the squirrel family — at least, the marmotines (ground-
squirrels, prairie-dogs) are certainly pure-cone, and all others except the
flying-squirrels are probably pure-cone.

In many birds, only a few rods can be found and these may be
present over only a part of the whole retinal area. Cones outnumber rods
very greatly in all diurnal birds which have any rods at all. Turtles have
very few rods among their cones, and some species may have none. In
freshwater lampreys, the cones and rods are equal in numbers; but in
marine species the rods are more numerous to give the added sensitivity
demanded by deeper water.

The most nearly diurnal of the amphibians — the frogs — have much
higher cone-to-rod ratios than do some vertebrates which are more
strictly diurnal than they; but in the amphibians the rods are so large
and the cones so small that we have here a situation which is the reverse
of that in the teleosts. The actual effect is of a preponderance of rods —
just as in teleosts, with the rods very numerous but very tiny, there is
an effective preponderance of cone-substance.

Except for the vertebrates above-mentioned, none is known to exceed
by very much the cone-to-rod ratio of man, which is about 1 : 20 and
seems very low — until we take account of the great size of the eyes of
primates, large carnivores, and ungulates, whose retinal image sizes are
such that many rods may be allowed to leak in between the cones with-
out the visual acuity being pulled down below that of a small bird whose
retina is pure-cone and whose cones are contiguous. Thus, where an
animal has room for a large-enough eye, he can afford to have a duplex
retina without sacrificing too much visual acuity, and then has the
opportunity of seeing something in twilight or moonlight, whether he
takes the opportunity or not. Most do — and thus it is that ungulates,
large carnivores, and primates are able to stay up after the birds have

THE DIURNAL RETINA

177

gone to bed, and tend toward twenty-four-hour activity. The presence
of enough rods to make this possible would sometimes affect visual
acuity too adversely, except for the development of a small pure-cone
area, the 'area centralis', in the otherwise duplex retina. Such an area,
like the whole of a pure-cone retina, is necessarily blind in dim light.
The outer nuclear layer, formed by the rod and cone nuclei, tends to
have few rows in diurnal retinse. Cones being usually more plump than
rods, there is more room for their nuclei to lie directly against the ex-

|Diurnal|

receptors '

(many cones)

summoted

but little

in:

BIPOLAR CELLS-^

finally
sunnnnated
but little
* in:

GANGLION CELLS*

-•-BIPOLAR CELLS

nally

summated

extensively

in:

GANGLION CELLS

Fig. 72 — Diurnal and nocturnal retinae contrasted.

The diagrams represent two related species, one of which is diurnal and the other noaurnal.
The characteristic differences in the relative thickness of the nuclear layers are the result of
the visual-cell patterns and the differing extents of summation in optic nerve fibers.

ternal limiting membrane. Where rods are few or absent, this makes for
a thin outer nuclear layer. In some lampreys, there is but a single row
of nuclei. Turtles and squirrels have but a couple of rows, as do the
amphibians — in the latter it is the unusual bulk of the rods, and their
relatively small numbers, which is responsible. Where the rods are
slender and are as numerous as they are in man, the outer nuclear layer
becomes thick; and (Fig. 69a) it becomes far thicker still, of course, in
twenty-four-hour and nocturnal eyes (except, again, in amphibians) .

178 ADAPTATIONS TO DIURNAL ACTIVITY

Where the cones are slender, hence numerous per unit of retinal
area, their nuclei pile up in several layers. This is true in lizards and
particularly in birds; and in all cases, in the pure-cone spots in duplex
retinae referred to above and treated at length in the next section. The
snakes are quite conspicuous, among pure-cone forms, for having single
outer nuclear layers — the reason being that the cones are generally fatter
than their own nuclei (Fig. 68) , since only a few snakes (e.g., Dryoph'ts,
Malpolon, Sepedon) have taken advantage of their diurnality to obtain
high visual acuity by slenderizing their cones.

Though the outer nuclear layer tends to be thin, the inner nuclear
and ganglion layers tend to be thick in diurnal animals. This is an
expression of the reduction of summation (see pp. 47, 67) , of the increase
in the number of neurons per number of visual cells, for the preservation
of the high resolving power which the multiplication and slenderization
of the cones tends to produce. A diurnal retina can thus often be dis-
tinguished at a glance from a nocturnal one, for in the former the inner
nuclear layer is usually thicker than the outer, this situation being re-
versed in the nocturnal retina (Fig. 72). A considerable portion of the
characteristic thickening of the inner nuclear layer of diurnal retinae is
due to the greatly increased numbers of horizontal and amacrine cell-
bodies ; for, as diurnaUty is adopted and perfected by a vertebrate group,
these integrative cells are multiplied even faster than the straightforward
conductive ones (bipolars and ganglion cells) and may, as in birds,
come to outnumber the latter. Though it would seem that ganglion:
bipolar: visual-cell ratios would take up and finish the job of fixing
visual acuity where the size and quality of the image and the concen-
tration of cones leave off, the 'switchboard' effects of the horizontally in-
tegrative neurons have a mysterious and very considerable concern with
the sharpening of the mental picture, probably by manipulating contrast
phenomena. This particular specialization makes the bird retina the
thickest of all— though it should not be thought that the variation of
retinal thickness from group to group of animals is a very great one,
for it is surprisingly slight.

Minimization of the Physiological Scotoma — The 'blind spot' of
the retina may, in thoroughgoing diurnal eyes, be called upon to modify
itself in sympathy with the efforts toward improving detail- and form-
perception. The insensitive head of the optic nerve, called the 'disc'
from its usual appearance when seen with the ophthalmoscope, causes

NULLIFICATION OF THE BLIND SPOT 179

a physiological (normal) scotoma or gap in the visual field within which
nothing can be seen. We humans are not aware of our blind spots, for
since the two retinal topographies are mirror-images of each other and
both are aimed forward, any object whose image falls within the disc of
one retina is simultaneously imaged upon functional retina in the other
eye. We are not even aware of the blind spot when one eye is kept
closed, and can demonstrate it to ourselves only in an experiment such as
is shown in Figure 73. An animal whose eyes are on the sides of his
head, however, might as well have one eye closed so far as concerns what
the other fundus is seeing; and hence he cannot fill in, with each eye,
the blind spot of the other.

The blind spot becomes a serious matter only where the disc is rela-
tively large; but this happens to be inevitable when the eye is especially
well adapted for diurnality. For, it will then have a preponderance of
cones, and the consequent great numbers of ganglion-cell axons make
for a relatively heavy optic nerve and a large disc. On the other hand,

Fig. 73 — Demonstration of the blind spot.

Cover the right eye; fixate the star steadily and move the book slowly toward and away
from the face. The words at the left will disappear and reappear as their image swings
on and off of the head of the left optic nerve.

the disc of a mouse is a mere dot, for each of the few optic nerve fibers
is connected with hosts of rods.

In three diurnal assemblages the disc has become a narrow, greatly
elongated oblong : in the squirrels, the birds, and the predaceous pikes,
salmonoids, and percoids among the teleost fishes. Elsewhere it is usually
circular but it may be oval, reniform, triangular — always, however, com-
pact. A fatally large, compact disc has been avoided in the fishes by
permitting the developing optic nerve fibers to fill in the whole length of
the embryonic fissure of the optic cup, instead of massing them at the
apex of the fissure (see p. 108) as other vertebrates do. The optic nerve
thus often departs from the fish eyeball as a ribbon rather than a cord,
and becomes crumpled edgewise to gain a circular cross-section between

180 ADAPTATIONS TO DIURNAL ACTIVITY

eye and brain (Fig. 105e, p. 261). In the birds, the stripe-like disc is con-
cealed under the base of the 'pecten', a pleated fin of pigmented, highly
vascular tissue which arises embryologically from the lips of the embry-
onic fissure and projects lens-ward through the vitreous (Fig. 80, p. 188).
The birds thus have only one narrow scotoma where they might have
had two if they had located the pecten elsewhere.

The squirrels exhibit the most remarkable of all modifications of the
disc (Fig. 74). It is a stripe, oriented horizontally to interfere minimally
with the perception of vertical contours which are so important to an
arboreal animal. It has been moved far above the optic axis whereas in
other vertebrates it is almost invariably located close below the axis or
even on it, in the center of the fundus. Since it is the lower part of the

Fig. 74 — The optic disc in various members of the squirrel family.

(In schematized views of the fundal portions of left eyes, the anterior segments being cut
away; the drawings are not to the same scale).

a, prairie-dog, Cynomys ludoyidanus (inhabits open spaces, very bright light), b, wood-
chuck, Marmota monax rufescens (inhabits less bright places), c, gray squirrel, Sciurus
carolinensis leucotis (inhabits dense woods), d, flying squirrel, Glaucomys v. volans (noc-
turnal, with a nearly pure-rod retina).

retina which looks upward, vision of the sky, where the squirrel's chief
enemies soar, is thus left unimpeded. The stripe-like disc is so slender
that it bites out only tiny bits of vertical lines; and a tiny head or eye
movement, up or down, will move any horizontal line off the disc and
onto functional retina. Where the number of optic nerve fibers varies
from species to species, the stripe varies in length (but not in width),
in sympathy with the species' preference for bright light — from 7%%
of the diameter of the eye in the sun-worshipping ground squirrel
down to 30% in heavy-timber tree squirrels and even less in the Eu-
ropean squirrel (where also it widens somewhat) , which seeks the darkest
woodlands. The palm squirrel and the nocturnal flying-squirrels, as
might be expected, have perfectly orthodox small, circular discs located
just below the center of the fundus.

ARE/E CENTRALES AND FOVEJE 181

(C) Are^ Centrales and Fove^

The Area Centralis — An important feature characteristic of the best-
adapted diurnal eyes, and found in many twenty-four-hour eyes (as an
adjunct to their diurnal activity phase) is the area centralis. It is best
defined as a circumscribed retinal area within which the retina is so
constructed as to afford a marked local increase in resolving power.

The name 'area centralis' is not too fortunate, for the area is not
necessarily near the center of the fundus — though it happens to be in
man, whose morphology has greatly influenced all anatomical termin-
ology. In the human and other primates, the macula lutea (= yellow
spot) of the retina is synonymous with 'area centralis', but the term
'macula' is most improperly applied to the areae of other vertebrates.
Similarly, the word 'fovea' is often badly misused, and it will be well
to get these three terms firmly and accurately in mind :

An area centralis is only exceptionally pigmented, making of it a
yellow spot on the otherwise colorless retina. Only then can it properly
be called a macula lutea. This latter term should consequently be re-
served — if, indeed, there is any need for it at all — for the areae centrales
of the higher primates, and possibly the chameleons. No others are
known to have the diffuse yellow pigmentation of the inner layers of the
retina in the area centralis.

Again, only certain areae centrales have a depression or pit in the
center; and it is just this pit, not the whole area, which should be called
a fovea. An area centralis can occur without a fovea — it may actually
be thickened, not thinned — but a fovea can exist only within an area
centralis.

The various features of a full-fledged area centralis can best be set
forth if we enumerate them as steps in the evolution of such an area in
a hypothetical vertebrate. This animal must have taken on diurnality
and — unless of course he eventually dispenses with rods entirely — must
have a large-enough eye to be able to afford to devote a portion of the
retina to an area centralis without sacrificing the ability to see in dim
light with the greater part of the retina.

The first obvious thing to do is to increase, locally, the number of
visual cells per unit area of the retina. This is brought about partly by
making them more slender, partly by packing them more closely to-
gether than they are outside the area. Since the rods are like so much
deadwood when it comes to affording highly-resolved images to the

182 ADAPTATIONS TO DIURNAL ACTIVITY

consciousness, they are progressively eliminated and the area comes to
be a pure-cone island in a duplex sea of unmodified retina.

As the rods are eliminated and the cones are aggregated and slen-
derized, the threshold of stimulation of the area tends to rise. The
areal cones would then go out of action, in failing illumination, before
the more massive extra- areal ones; but they counteract this tendency by
evolving longer and longer outer segments. This local thickening of the
visual-cell layer causes the external limiting membrane to bulge inward
toward the vitreous, and may even make the pigment epithelium bulge
outward against the chorioid ('fovea externa'). Retinal blood vessels,
where these are present (mammals) tend now to be excluded from the
area so as not to interfere with clear perception, and the chorioid may
have to thicken locally to carry the extra nutritional load. The increased
length of the visual cells has a fortuitous but very fortunate effect upon
the burden carried by the mechanism of accommodation (see pp. 30-1).

a

Fig. 75 — Well-developed (avian) and poorly-developed (human) iovex. x 271/2.

Cross-hatched in each diagram is the portion of the foveal retina which is actually thinner
than the retina outside the area centralis. The superior avian fovea is less a 'thin spot' than
is that of man. a, foveal region of hawk, Buteo b. borealis. b, macular region of normal
human retina.

The increase in the percentage of cones results in a great increase
in the number of bipolar and ganglion cells, since cones are summated
less in them to begin with, and less within the area than outside of it
— each cone, ideally, coming to have its own bipolar and ganglion cell
transmission-line to the brain.

The thickenings of the visual-cell, outer nuclear, inner nuclear, gang-
lion-cell, and nerve-fiber layers add up to a local thickening of the retina
as a whole. Where this might become extreme, a fovea develops — not
to combat the thickening as such, but rather the convex surface thereof
which bulges into the vitreous.

The Forea—The reader, stopping at any point in the above discussion,
would then have already read a complete description of some area cen-
tralis which actually exists in some vertebrate or other. Most arese do
not go on to develop a fovea, and fewer still of these have produced the

ARE^ CENTRALES AND FOVE/E

183

local yellow pigmentation which creates a macula lutea and is a final
refinement in making the area centralis the spot of maximal visual acuity.
For the full comprehension of the meaning of the foveal depression we
must revert for a moment to the elements of physiological optics.

A light ray passing through the cornea and lens and striking the
retina perpendicular to its surface will travel on through the retina with
its direction unchanged. It was long thought, however, that an appre-
ciable amount of the light would be absorbed and scattered in the retinal
tissue before reaching the visual-cell layer, thus not only being lost for
purposes of image-formation but, more important by far, tending to
blur the image. The depression of the fovea was then thought of as a
thin spot produced for the sake of thinning, and serving to remove tissue

vitreous

vitreous

Fig. 76 — Local magnifying action of the foveal depression (based on the
central fovea of a hawk, Buteo b. borealis).

from in front of the important central bouquet of cones in the area. This
theory must be discarded however, for in the best of areae (in lizards and
birds) the portion of the depressed retina, which is thinner than the
retina outside the area, is smaller than in arex with shallow foveas which
are known to be degenerate (Fig. 75). The retina, in life, is completely
clear and actually extinguishes no more light than the same thickness of
vitreous — which, of course, fills in the foveal excavation.

A clue to the real meaning of the fovea (Fig. 76) was made available a
half-century ago in some observations of Valentin on the refractive index
of retinal tissue; but, it went unrecognized as a clue until very recently.
The data never seemed of any possible usefulness, and one finds no
figures given in modern reference books. But the index of the retina was

184 ADAPTATIONS TO DIURNAL ACTIVITY

carefully measured by Valentin in a number of animals and was found
to be always substantially higher than that of the vitreous. What this
means is that if a light ray should strike the vitreoretinal boundary at
anything but a right angle it will be refracted away from an imaginary
perpendicular to the surface at the point of its impact.

The foveal depression is designed deliberately to take advantage of
this refraction. The foveal portion of the retinal image is expanded on
its way through the retinal tissue, and is thus magnified somewhat when
it reaches the level of the visual cells. In birds the magnification is about
13% linearly, 30% in area; and it is probably greater in lizards. The
linear increase directly affects visual acuity. The areal increase improves
the perception of 'pattern', though it adversely affects sensitivity to
external illumination. A part of the lengthening of foveal cones, two
advantages of which have already been mentioned, is perhaps in com-
pensation for the local dimming of the expanded portion of the image.

When an area centralis has done everything else possible to increase
the number of receptor-units over which the image will fall, the further
increase afforded by a deep fovea makes the production of one decidedly
worthwhile — nay, mandatory, for the convex bulge in the internal limit-
ing membrane over a highly-developed area centralis would tend to
converge the rays of light and make the image, at the level of the visual-
cell layer, smaller. The shallow depression in the area centralis of a soft-
shelled turtle (Fig. 78b) or the average teleostean fovea probably does
little more than cancel the minifying effect of the area's convex inner
surface. The deeper the actual depression goes below the original level
of the retina, the higher the mound or 'circumfoveal eminence' created
around the depression by the displaced tissue. Since a continuous steep
slope is thus produced from the crest of the mound to the bottom of the
depression, this sloping surface becomes an effective magnifying device,
of optically unique description.

Distribution — No lamprey has an area centralis, but one occurs in
Mustelus — the only genus of sharks known for certain to have any
cones at all. It is marked by a noticeable concentration of ganglion
cells (Fig. 77a). An area centralis is very commonly seen in bony fishes,
and a fovea (Fig. 77b) has been found in a score or so of teleosts (see
Table III, p. 187) , never as deep as in lizards but with both rods and twin
cones excluded from it. The areae centrales of frogs, most turtles (Fig.
78), and all crocodilians are devoid of foveae and are imperfect in that
they contain rods as well as cones— indeed, the crocodilian is nocturnal

ARE^ CENTRALES AND FOVE/E

185

and it is more than likely that its area centralis is an area of especial
sensitivity, not of acuity at all.*

In only two genera of snakes is a fovea positively known to occur.
The East Indian long-nosed tree-snake, Dryophis mycterizans (Fig. 79)
has a keyhole-shaped pupil with the slot of the keyhole pointing forward
well beyond the rim of the lens, thus constituting an extensive aphakic
space. The fovea in Dryophis is at the outer rim of the retina on the
temporal or caudal side of the eye, and a line from it through the center
of the lens passes out through the slot in the keyhole pupil, along a
groove on the cheek in front of the eye, and straight forward parallel
to the axis of the body. It is significant that herpetologists have long

Fig. 77 — Area centralis and fovea in fishes.

a, portion of retina from sagittal section of eye of a shark, Mustelus mustelus. After Franz.
ac- area centralis (note increased length and concentration of visual cells, number of
ganglion cells).

b, eye of a teleost, Serranus scriba, horizontal section; retina shown in black. After Kahmann.
/- fovea; n- nasal side; ^ temporal side.

*The same suspicion falls upon the ungulates and carnivores, hardly any of which are
strictly diurnal. The majority of afoveate arese would in faa bear re-investigation with this
suspicion in mind, for it is already known that the special area of the opossum has its
histological peculiarities aimed at increasing sensitivity, not resolving power. There appear
to be circumscribed central areas of extreme sensitivity in the retinje of the echidnas and
some 'edentates', for these nocturnal animals are reported to wince and close their eyes in evi-
dent distress whenever the light-beam of an ophthalmoscope strikes the small area mentioned.
This, by the way, is quite a different thing from the phenomenon in the human eye which
has led some careless ophthalmologists to refer to the macula lutea as the 'most sensitive'
spot in the human retina. It is the least sensitive spot, becoming quite blind in low illumi-
nation — but it happens to be the pupillomotor area, the part of the retina which controls
reflexly the closure of the pupil when illumination is suddenly increased. The fovea of the
owl is also the pupillomotor area — and here, perhaps, it is extremely sensitive as well, in
the true sense of 'sensitive'.

186

ADAPTATIONS TO DIURNAL ACTIVITY

been in agreement that this snake has the sharpest sight and the most
accurate judgment of distance of any in the world. A very similar situa-
tion obtains in the African bird snake, Thelotornis ktrtlandi; and prob-
ably also in Dryophiops, whose pupil is similar.

a in turtles.

sagittal section of retina through the area centralis of the western painted turtle, Chrys-
emys picta marginata. The optic nerve head is out of the picture a bit to the right,
b, section of retina through the fovea of a soft-shell turtle, Amyda sp. Redrawn from Gillett.

pe- pigment epithelium; r- receptor layer; /- limitans; on- outer nuclear layer; op- outer

plexiform layer; in- inner nuclear layer; ip- inner plexiform layer; g- ganglion layer; n-

nerve fiber layer.

Fig. 79 — The East Indian long-nosed tree-snake, Dryophis mycterizans.

a, right eye in situ, from the side, showing aphakic portion of pupil and cheek groove which
permits straight-forward vision, x 4. From alcoholic specimen, as- aphakic space; /- lens;
g- groove, b, face, showing provisions for binocular vision, x 2. From Franz, after Beer,
c, anterior segment of right eye, showing form of iris, lens, and aphakic space, x 4. From
Franz, after Beer, d, head from above, cut away to reveal eye in section, showing line of
sight from temporal fovea through lens and aphakic portion of pupil and along cheek
groove, x 2. From alcoholic specimen and microscopic preparations.

TABLE m-AREAE AND FOVEAE

AREA

FOVEA

CO

u

I

CO

Ll.

Cyclostomes

Elosmobronchs

Mustelus only;
central and round

ChondrDSteans,HolosteGns,Dipnoans,aadistians

Teleosts

Many

temporal; poorly
defined at best

Bothy frocfes (deep-sea)
has pure-rod fovea

A few littoral marine spp.

temporal (nearly cen-
tral in HipDOcampus)

shallow to medium
(deeo in Gire/lo sp.l)

AMPHIBIANS

Anurans

crescent over _^

ODtic DODilla-. ^T^

Urodeles and
Ccecilians

REPTILES

Sphenodon

central

medium (pure-rod!)

Crocodilians

horizontal band (prob-
ably not an acuity area)

Turtles

central, round

Amyda only; shallow

Lizards

Nocturnals

Diurnals

central; round or oval
(temporal in Voranus)

deep (shallow in large
skinks and Voranus)

Snakes

Nocturnals

Diurnals

temporal; poorly defined

Dryophis, Dryophiops,
and TheloforniS; medium

CO
Q

CD

Most (including most vultures?)

central, round

medium to deep

Some ground-feeders; domesticated spp.

round, poorly defined
at best; often absent

pigeons only
(shallow and variable)

Some ground -feeders; many
swimmers, divers, and waders

central and round, set in
horizontal band which is
also organized for acuity

r

nedium,in round orea^

t

Hawks, eagles, swallows, terns

two circular, fovea te '"

areas connected by -

horizontal band--

^^=- (terns. =«°) '

o
>

two- central (deep) &
temporal (usually med-
ium, but is the deep-
er of the two in eaales)

Kingfishers, bitterns, humming-birds,
some wing -feeding passerine spp.

two: central and ten> ■
poral, both round, not
connected by a band

two; central (deep)
temporal (medium)

Some gulls, shear -waters, flamingo

horizontal bond

linear (trough-like) fovea

Owls, Apus apus, Sfrigops habroptilus

temporal, round (a fain
central one also in /I/^5

shallow; sometimes none

MAMMALS

Most

Ungulates

more or less temporal; us
ually broad horEontal banc

Carnivores (espec. felids)

central, compact

Sguirrels(espec marmots)

horizontal bond,
not well defined

Primates

Lower
(and Aotus)

Lemur cgtfa,L.macoco
and Aofus only; centra

Higher

central , round

deep but broad in man
(more abrupt in some?)

187

188 ADAPTATIONS TO DIURNAL ACTIVITY

In lizards the area is central, and is circular or oval; but in birds it is
often a long horizontal band, as in Figure 80a (minimizing the need for
eye movements) and has in it a central circular or oval fovea. In a num-
ber of birds a second fovea, seldom as well-developed as the central one,
lies temporally from the latter (Fig. 80b). Such a temporal fovea is
comparable with the single fovea of Dryopbis or a teleost, in that it and
its mate in the other eye can both be brought to bear upon the same
point in space ahead of the bird. The central or nasal fovea is useful
only for monocular vision sidewise from the head; and in most birds,
whose eyes aim much more sidewise than forward, it is the only fovea.
In the owls, only a fovea temporalis is ever present, and it may be very

Fig. 80 — Ophthalmoscopic appearance of bird eyes, showing pecten (ventrally),
arecE, and fovea. After Wood.

a, right eye of pigeon guillemot, Cepphus columba, showing horizontal linear area centralis
and single central fovea, x 3. b, right eye of Anna's hummingbird, Calypte anna, showing
central foveate area, and temporal fovea (in cutaway; cf. Figs. 114-5, pp. 308-9). x 10.

shallow or even lacking. One swift, Apiis apus, approaches the owls
in that its central fovea is barely visible though the temporal one is
well developed. Only birds ever have two foveae per eye, but George
Moore has recently found that some of the killifishes {Fundulus spp.)
have two horizontal, ventro-temporal, ridge-like areae.

In diurnal birds and in most lizards, excepting the monitors and the
more chunky and sluggish of the skinks, the fovea is deep and its slope
Cclivus') is convex. This convexiclivate type of fovea (Fig. 81) occurs
only in the very best-constructed of areae centrales. The less perfect areae
of fishes, Sphenodon, owls, domestic birds, and man all have shallow
and concave Cconcaviclivate') foveae (Figs. 75b, 82). It is safe to say
that most of these (the fishes excepted) are degenerate and formerly,

ARE^ CENTRALES AND FOVEJE

189

in some ancestor, tended more toward the convexiclivate type of profile.
The visual cells of Sphenodon show that this animal was once diurnal
(see Chapter 16, section C) and at that time it no doubt had a fovea

Fig. 81 — Central (nasal) fovea of the European bank swallow.

Exemplifying the deep, convexiclivate type characteristic of birds and lizards. After Rochon-
Duvigneaud.

Fig. 82 — Fovea and surroundings in Sphenodon. x 90.

Illustrating the shallow, concaviciivate type characteristic of fishes and of those vertebrates
whose fovece have become degraded through domestication or the abandonment of strict
diurnality. s, sclera; c, chorioid; r, retina. (The retinal and chorioidal pigment have been
bleached from the section; note that only rods are present — this is the only rod fovea in a
terrestrial vertebrate).

190 ADAPTATIONS TO DIURNAL ACTIVITY

as acutely deep as that of any lizard. Its pure-rod retina was once a pure-
cone one, so that Sphenodon, having retained the fovea despite the trans-
mutation of its cones into rods, now enjoys the only pure-rod fovea
which is known to us, except for the very mysterious case of a reputed
fovea in one deep-sea fish (Bathytroctes). Similarly, the foveae were cer-
tainly much better developed in some of the owls' diurnal ancestors.
The shallowness and variability of the pigeon's fovea has long been con-
sidered the consequence of semi-domestication, for in the fully domesti-
cated fowls the fovea is gone completely. On the other hand, the con-
caviclivate foveae of the few foveate teleosts, and that of the only known
foveate turtle (Amy da) have probably never been any deeper — they seem
merely intended to counteract the convexity of the area centralis. And,
by the way, some pure-cone animals with extremely good vision — the
ground-squirrels, particularly — have never produced a fovea simply be-
cause their entire retina is built as well for acuity as is the macula of man.

If the variable, shallow, and gradually-curved human fovea has not
degenerated from a deeper and much more abrupt depression, it is diffi-
cult to see what could have called it into being. Its magnifying action on
the image is probably negligible compared with that of a convexiclivate
fovea. Nothing much seemis to be known as to the shape of the foveal
depression in some of the monkeys and apes which are more strongly
diurnal than man himself. In the marmoset (Hapale jacchus) however,
the fovea has a very steep clivus and a small flat floor. The sooty manga-
bey (Cercocebus torquatus) probably has the most cone-rich retina of
any primate, and its foveal cones are the longest and slenderest in mam-
mals; but the shape of its fovea is unfortunately in dispute. One or two
divisions of mankind — the Hottentots, certain natives of India, and the
Tierra del Fuegans — are known to have phenomenal visual acuity; but
the profiles of their foveae are not accurately known. Their sharpness of
sight has always been attributed to an unusual slenderness of the foveal
cones.

The distribution of areae and foveae, and particularly their topograph-
ical locations in various retinae, are discussed further in section C of
Chapter 10. As we have seen, the modifications themselves are devoted
entirely to the raising of local visual acuity, but their locations are of
such importance in connection with eye movements and space-perception
that their full significance can be gathered only from a later consider-
ation of these matters.

INTRA-OCULAR COLOR-FILTERS 191

(D) Intra-Ocular Color-Filters

Color vision itself is a potent aid to visual acuity in its broad sense,
and was certainly evolved for this application rather than for the
aesthetic ones which it has come to have in human vision. But color
vision is such a large topic, with so many ramifications, that it needs a
long section to itself (Chapter 12). In the present section, we shall con-
sider a group of devices which occur only in the eyes of diurnal animals
(some, not all, of which have color vision) and promote their visual
acuity, and which look at first glance as though they must have some-
thing to do with creating color vision — though actually they are just
as effective whether their owners happen to be able to distinguish hues
or not.

Types and Distribution — The yellow pigmentation of the human
area centralis — making it a macula lutea — was discovered by Soemmer-
ing in 1818, In 1840, Hannover first described the oil-droplets which are
characteristic of so many vertebrate cones (Fig. 22, p. 54). Some or all
of these are always yellow, when any pigment is present in them at all.
By 1867, Max Schultze had called attention to the fact that the rich
network of capillaries in the inner layers of the mammalian retina con-
stitutes an effective yellow screen through which the visual cells must
look. In 1887 Schiefferdecker found that in certain fishes the cornea is
yellow. (Soemmering, long years before, had seen the color in the pike,
but thought it to be in the aqueous humor) . Other species have recently
been added to Schiefferdecker's list, and in the past few years it has
been found that diurnal squirrels, tree-shrews, snakes, geckoes, and lam-
preys (except Geotrid) have yellow lenses. It has been known for many
years that the adult human lens is yellow, but not until very recently
has it transpired that this is actually of advantage to sharp vision in
bright light.

This imposing list of intra-ocular color-filters exhibits at first glance
considerable variety; but (see Table IV, pp. 200-1) they are almost all
yellow; and where they are not, they are still of long- wave colors — and
they are confined to diurnal vertebrates. It thus appears logical that some
inclusive interpretation may hold for all of them, and after a large num-
ber of false starts such an interpretation has finally been given. But until
a few years ago the macular pigment, retinal capillaries, and yellow comeae
were neglected or forgotten, and the yellow lenses went undiscovered for
a most surprisingly long time, while attention was fastened upon the

192 ADAPTATIONS TO DIURNAL ACTIVITY

colored oil-droplets. As long as these held the stage, the mental myopia
of investigators prevented anyone's noticing the other types of filters
and using them to help explain the baffling oil-droplets.

The Color-Vision Theory — The oil-droplets were formerly believed
to occur in a much greater variety of colors than is actually ever the case.
Those of birds seemingly ran the gamut of the visible spectrum; but
under modern apochromatic microscope lenses the violet, blue, and green
droplets lose their colors and are seen to be actually devoid of pigment.
They owe their chromatic appearance, under cruder lenses, to purely
optical phenomena. Only red, orange, and yellow droplets occur in birds
and turtles along with some colorless droplets. Most groups provided
with colored droplets contain nocturnal species whose droplets are all
colorless. The pigments involved are carotenoids, and those extractible
from chicken retinas have recently been tentatively identified as astacin,
sarcinene, and xanthophyll.

When belief was current in a more complete spectral representation,
the theory of oil-droplet function first advanced by Krause in 1863 (and
based at first upon the supposition that lizards, as well as birds, had 'all'
colors) was most popular, and still has adherents. According to this
theory, each color of oil-droplet makes possible the independent sen-
sation of the corresponding color in the spectrum. The supposition was
that the bird has but one (not three) photochemical substances in its
cone outer segments (see p. 91), and that this undifferentiated sub-
stance would be affected equally by any and all visible wavelengths of
light. Discrimination of wavelengths on a qualitative basis — color vision,
in other words — would be possible only if certain cones were allowed
to be stimulated only by certain wavelengths, others by other wave-
lengths, and so on. The differently colored oil-droplets, standing in the
pathway of the light on its course toward the percipient outer segments,
were supposed to ensure this differential stimulation of different sets of
cones, which in turn connected with different sets of brain cells in which
the respective color sensations were registered. This mechanism of color
vision has seemed so simple and plausible that some students of human
visual physiology have fled to it as a refuge from the necessity of think-
ing through the state of affairs where, as in man, color-vision occurs with
all the cones alike, and have postulated that minute colored oil-droplets
occur in human cones— the while being careful not to look to see if they
are really there.

COLOR-VISION THEORY OF OIL-DROPLETS 193

The ingenious color-vision theory of oil-droplet function falls to earth
under several blows: the number of oil-droplet colors does not in fact
correspond to the range of the bird's spectrum, which is now known to
be co-extensive or even a little wider than our own. Lizards have a com-
plete color-vision system, yet have only yellow oil-droplets. There are
vertebrates far below the birds — the fishes — that have color vision with-
out benefit of oil-droplets, which could then scarcely be considered a
primitive device for hue-discrimination. Most important of all, it has
been known (though almost forgotten) for decades that the cones of
the bird fovea contain only yellow droplets, the red ones stopping at
the margin of that all-important retinal pit. This demonstrates not only
how wholly illogical it is to suppose that the bird would be able to per-
ceive only yellow in the fovea, and all other colors only outside it, but
also that the different colors of droplets are of unequal importance and
have different uses, not one common function. The exclusively yellow
droplets in the avian fovea line up with the yellow filters, whether com-
posed of oil-droplets or not, of all other vertebrates. Yellow droplets
appeared first in evolution, in lower vertebrates; and where the oil-drop-
lets are decadent, as in nocturnal birds, some yellow ones may persist
but no red ones ever occur. The red filters of birds and turtles can be
temporarily ignored while we consider what the much more common
yellow filter may do for photopic vision.

Yellow Filters and Chromatic Aberration — The image formed by
the natural dioptric system of the eye does not lie in a single plane or
spherical surface, even when the object is a plane or a curved surface
concentric with the eye. The image has thickness, owing to aberration
which is of two kinds, spherical and chromatic. Spherical aberration
results from the failure of the cornea and lens to bring parallel rays to
a single point, and since it is chiefly caused by the improperly curved
peripheral portions of the corneal and lens surfaces, it is effectively
combatted by the pupil which acts as a 'stop'. When the refractive power
of the lens is increased in accommodation, the pupillary aperture auto-
matically contracts to afford the smaller stop which is then demanded.
Chromatic aberration is due to the fact that the different wavelengths
of white light are not all bent to the same extent when they are refracted
at boundary surfaces. The refractive index of a substance is thus differ-
ent for each wavelength — it is this phenomenon of 'dispersion' which
makes it possible for a prism to form a spectrum by sorting the 'colors'

194 ADAPTATIONS TO DIURNAL ACTIVITY

out of 'white' light. The shorter waves are bent most, longer waves pro-
gressively less. As Figure 29c (p. 82) shows, this results in a series of
focal points beyond a lens, the violet focus being nearest and the red
focus farthest away. The distance occupied by these foci is called the
linear chromatic aberration, and in the human eye it is considerably
more than the whole thickness of the retina. In the refractionist's lan-
guage, the aberration amounts to about two diopters. The 'normal' or

C

/

550

Wavelength (mp)

.401- m
t <

Q

Fig. 83 — Graph showing how yellow filters combat chromatic aberration.

(Curve of transmission spertrum smoothed from data of Ludvigh and McCarthy on absorp-
tion in the lens, cornea, and humors of the human eye, integrated with data of M. Sachs
on absorption in the most completely studied macula among his nine examples; dispersion
curve for the human dioptric media, showing the relative refrangibility of the various wave-
lengths, plotted from data of Polack).

The curves bring out the fact that the short waves, which are most strongly dispersed and
which consequently contribute most to chromatic aberration (c/. Fig. 29c, p. 82), are the
ones most strongly absorbed (i.e., least well transmitted) by the yellow filters interposed
in their path within the eye.

emmetropic human eye is actually emmetropic only for yellow light, and
is, simultaneously, 0.75 diopters hypermetropic for red and 1.25 diopters
myopic for violet. Since the dioptric apparatus ordinarily places the
yellow focus in the visual-cell layer, we must actually accommodate when
diverting our attention from a blue object to a red one at the same
actual distance from the eye, and must relax accommodation upon look-
ing back at the blue object. This fact is employed by astute artists to
heighten the illusion of depth in their paintings.

YELLOW FILTERS AND CHROMATIC ABERRATION 195

If a particular color-focus lies squarely in the visual-cell layer, the ho-
monomous color-value of the external visual field will be crisply focused
but all others will be represented, at the level of the visual cells, by sets
of blur-circles. Fortunately the ends of the spectrum are much less bright
than the yellow region; but even so, chromatic aberration results in a
considerable blurring of the image.

In the fovea, chromatic aberration is partly compensated for (except in
birds) , by the greater length of the foveal cones (how many things we
find we can do with that greater length!), for a greater number of color-
foci can thus lie in the length of one cone. But foveal cones have their
limits in length, and fall far short of dealing adequately with chromatic
aberration by such means. Obviously, there would be no chromatic aber-
ration if a single wavelength of light were passing through the eye to the
receptor layer. To bring this about, however, would mean the elimination
of color vision — and of nearly all the light. A compromise must, then, be
made by which the spectrum is narrowed down enough to make a big
dent in chromatic aberration, without sacrificing much of the physiologi-
cally effective energy of whole sunlight, or many of the colors which
occur most commonly in nature.

A yellow filter serves this purpose admirably. It cuts out much of the
violet light and some of the blue, which are the colors responsible for
most of the chromatic aberration, as Figure 83 demonstrates. At the same
time it lets through, unimpeded, most of nature's hues, and passes the
spectral regions which look brightest to both light- and dark-adapted eyes.

Other Values — This reduction of the effects of chromatic aberration is
not the only performance of a yellow filter. Most scattered light is of
short wavelengths, and under bright-light conditions this scattered light
results in glare. Glare and dazzle are minimized by a yellow falter. Simi-
larly, the unfocusable shortwave light scattered in the atmosphere, and
responsible for the bluish cast of distant mountains and for the blue of
the sky, is cut out by a yellow filter which, as every photographer knows^
creates a sharper image.

Still another effect is the enhancement of contrast. It will be recalled
that the same color-sensation can be aroused by different mixtures of
wavelengths. One can easily find, say, two books on the shelf whose col-
ors appear to be identical blues or greens. Yet a spectral analysis of the
light reflected from them might show the like-seeming colors to be wholly
different in wavelength composition. Almost any filter of colored glass or

196 ADAPTATIONS TO DIURNAL ACTIVITY

gelatine, placed before the eye, will make the two books look unlike; for
certain wavelengths reflected by the pigment of one, and absorbed by the
filter so as to change the color seen through the latter, are not necessarily
emanating from the other pigment at all. By absorbing wavelengths com-
mon to the two unlike mixtures, the filter brings out the fact that they
are unlike, which is something the unaided eye cannot detect.

A filter thus produces contrast between colored areas which otherwise
would look alike and would therefore be without a discernible boundary
between them. This fact was put to important use in World War I, when
colored goggles worn by reconnaissance aviators enabled them to detect
green camouflage produced by paints whose reflection-spectra were not at
all like those of the chlorophylls of actual foliage. Modern 'foliage'
camouflaging is more troublesome to both adversaries, for it has to con-
sist of actual foliage, which must be replaced frequently as it fades.

A filter naturally tends to abolish just as many contrasts as it pro-
motes; but promotion is in advance of abolition when yellow filters
and natural colors are under consideration. By cutting out the different
amounts of blue in different but alike-looking green mixtures, the greens
are made to look unlike; and almost any other contrasts can be sacrificed
by the animal if only those between greens, so numerous in nature, can be
enhanced. The oil-droplet type of filter has a special advantage, since the
many colorless or other-colored droplets scattered among the yellow ones
in the whole mosaic will permit the perception of any contrasts which the
yellow droplets tend to iron out, and vice versa. By altering the propor-
tions of the different colors of droplets in different parts of the retina,
particular color-contrasts are enhanced in particular parts of the visual
field. Thus in the pigeon the ventronasal three-quarters of the retina have
the yellow droplets predominant, giving maximal contrast of objects seen
against the sky by eliminating the latter's blue color; while the dorso-
temporal quadrant, being especially rich in red droplets, affords maximal
visibility to objects seen against the green of the fields and trees over
which the bird is flying. In World War II, antiaircraft observers have
stumbled onto such tricks, and have learned to use filters when scanning
the sky for enemy planes.

One thing which yellow filters might do— but don't— would be to absorb
harmful ultra-violet rays before these could reach the delicate cone outer
segments. Experiments have shown, however, that none of these rays sur-
vive absorption in the cornea and lens of a pigeon's eye, whose oil-drop-
lets consequently cannot possibly be purposed to protect against them.

OTHER VALUES OF YELLOW AND RED FILTERS 197

Red Filters and the Rayleigh Effect — A very widespread supersti-
tion, showing itself in such things as red airport beacons and amber fog-
lights on automobiles, is the notion that some colors — notably red — pen-
etrate fog better than do other colors or white light. The supposed phe-
nomenon is attributed to the 'Rayleigh effect', which is the scattering of
light inversely as the fourth power of the wavelength. The short waves
are scattered the most, the red and infra-red ones scarcely at all, resulting
in the blue coloration of the sky and in the remarkable clear pictures
which can be taken through haze with infra-red-sensitive plates.

But as far as the visible spectrum is concerned, there is no Rayleigh
scattering at all when the particles which cause the scattering are larger
in diameter than 0.75 [X. Natural mist and fog droplets, and solid particles
suspended in natural waters, are invariably at least several times this size,
and scatter light quite irrespective of wavelength. Red oil-droplets can-
not, then, be designed to sharpen images by eliminating Rayleigh-scat-
tered light in misty weather or in water, as some have thought. The tur-
tles and birds have nothing in common, and if this inclusive explanation
will not hold for the red oil-droplets of the two groups, room is left for
independent explanations of the two cases.

Value of Red Oil-Droplets in Birds — Most birds are such early ris-
ers that they expose themselves to Rayleigh scattering — not by gross mist
particles, but by molecules of water and gases in the atmosphere of even
the clearest of sunrises. At this time of day the sun's rays slant through
such a long atmospheric pathway that they appear reddened, the same
being true of the sunset — which is more familiar to most of us. The bird,
getting in most of his day's work at dawn and shortly after, is aided by
his red droplets. As the day wears on and the sunlight whitens, the yellow
(and on dull days, the colorless) droplets take over — the orange ones
affording a smooth transition. If this explanation is true, one would ex-
pect late-rising birds to have few red droplets. This is indeed the case, for
whereas the song-birds average 20% red droplets, the hawks have but half
of this number; and in the crepuscular swifts and swallows there are but
3% to 5% red droplets.

Value of Red Oil-Droplets in Turtles — The significance of the red
droplets of turtles is rather different. More than any other diurnal verte-
brates, they have the problem of seeing over the glary surface of water.
Since they have intensity to spare, they can afford red droplets for the
even greater effect upon chromatic aberration which a red filter will have,

198 ADAPTATIONS TO DIURNAL ACTIVITY

as compared with a compromise yellow one. On less bright days, the tur-
tle's yellow, or even his colorless, droplets automatically replace the red
ones as the most important constituents of the whole mosiac. Thus the
birds and turtles, having sufficiently cone-rich retinae, have been able to
differentiate the cones into several populations. Where most retinae are
rod-and-cone, or duplex, the turtles and birds have produced what may
fairly be called multiplex vision.

The workings of the turtle's oil-droplet mosaic can best be gathered
from an account of a clumsy, man-made imitation worked out empirically
by the United States Navy, as described to the author by Mr. Laurence
Radford of the Bureau of Ordnance :

"The Navy uses both red and yellow color filters in optical instru-
ments. Both are made of Corning Glass. The red cuts quite sharply at
about ^6000-6200 [A.u.j and the yellow at about ?u5 100-5300 [A.u.].
These filters are used because much experience has shown that they are
helpful, and the particular filters selected were chosen after considerable
study, both experimental and theoretical.

"In my opinion these filters are effective for our purposes because they
reduce glare due to scattered light and minimize the eflFects of the chro-
matic aberration of the eye, and for these reasons almost exclusively.
These two effects are produced more intensively by red than by yellow
filters, i. e., the amount of scattered light transmitted by the red is much
less than by the yellow because the latter transmits the green; and with
the red filter the effect of chromatic aberration is practically eliminated.
But there are conditions when the red filter cannot be used effectively,
perhaps because of insufficient intensity of illumination, or perhaps be-
cause it would reduce the color contrast. Hence the two colors, giving us
essentially the choice of two degrees of the same effect."

The red and yellow oil-droplets of the domestic hen have been found
to cut the spectrum off respectively at ^5800-5900 A.u. and ^5150-5250
A.U., the extracted red pigment (astacin) and yellow pigment (xantho-
phyll) at A,5900A.u. and ^5200 A.u. respectively when dissolved in
castor oil. Perhaps when the droplets of turtles are studied more carefully
they will be found to come even closer to justifying the Navy's choices!

In this connection it is significant that the kingfisher, whose visual
problem, like that of the turtle, is complicated by glary water, has 60%
red droplets — three times as many as the average bird. So much for the
functions of the intra-ocular color-filters. Some remarks on their nature
and evolution are now in order.

PHYLOGENY, CHEMISTRY OF FILTERS 199

Phytogeny and Chemistry of the Intra-Ocular Filters — The old-
est of all appears to be the yellow lens, which occurs in lampreys (but
not in the nocturnal Geotria) . Here, as well as in snakes and squirrels,
the pigment involved (lentiflavin) is soluble in weak alkalies. It is pres-
ent in full amount in albino squirrels, hence cannot be scattered melanin,
but is a chemically distinct substance (consult Table IV, next page).

In at least one of the two or three diurnal geckoes (Lygodactylus) , and
in the strongly diurnal, squirrel-like tree-shrews (Tupaia) the lens is also
yellow though nothing is as yet known about the pigment itself. Presum-
ably it is lentiflavin which, since it has been evolved repeatedly in such
widely-scattered groups, probably has as its precursor some substance
which is present in all vertebrate lenses.

The most intense colorations of the lens are reached in the ground-
squirrels and prairie-dogs, where the lens is almost orange. The lenses of
all other American sciurids (excepting the pale ones of the gray squirrel
and the colorless ones of the flying squirrels) are alike in color and are
matched by a 2 mm. thickness of American Optical Company 'Noviol 0'
glass. 'Noviol 0' is matched by the lens of Malpolon monspessulanis,
regarded as the most sharp-sighted snake in Europe, and will probably be
found to be exceeded in coloration by the lenses of Dryophis and its rela-
tives. Other diurnal snakes have paler lenses, the coloration being deep-
est in swift, bright-light species such as the racers and whipsnakes. Cre-
puscular snakes have little lentiflavin, nocturnal species none at all. Lam-
prey, Lygodactylus, and Tupaia lenses compare with those of a gray
squirrel or a whipsnake.

The yellow coloration of the human lens is the result of a precocious
aging of the lens nucleus which commences actually before birth, and is
thus not on the same footing as that of other yellow lenses. It grows
steadily in depth throughout life — the lens of a child has been found to
absorb 10% of the blue light entering the eye, that of a 78-year-old man
85%. In the normal adult human eye, absorption in the dioptric media
increases gradually from the long-wave to the short-wave end of the spec-
trum, attaining a value of over 90% in the violet. In old age the spec-
trum is cut off in the blue-green region and aged artists find that their
blue-containing pigment mixtures look wrong to younger persons, unless
the painting is done under an illumination which is particularly rich in
short-wave light, such as that from a mercury vapor lamp. The pigment
is melanin formed by the interaction of protamine and cysteine liberated
by protein-breakdown. The development of the coloration is thus due to

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202 ADAPTATIONS TO DIURNAL ACTIVITY

an essentially senescent change, and its optical usefulness is the sheerest
of accidents.

Oil-droplets and yellow corneae both appear first in the chondrostean
and holostean fishes respectively. The oil-droplets of the sturgeon are
colorless, though they were not necessarily always so. They have been
used as an argument that the oil-droplet was first evolved as a colorless
focusing device; but the sturgeon has a nocturnally-adapted eye, and one
would expect its oil-droplets to be colorless even if they had been pig-
mented in some diurnal ancestor.

In the diurnal Amia, the whole cornea is yellow, with the color intensi-
fied dorsally. The pigment itself has not been studied, but it is probably
the same ichthyocarotin which occurs in many of the dermal chromato-
phores of fishes generally. Some teleosts, notably the markedly diurnal
pikes (Esox spp.) have as strongly yellowed corneae as Amia. In a spe-
cies of darter from Georgia, so new to science that as yet it has no name,
Hubbs reports a central, homogeneous, deep yellow coloration in the
cornea, opposite to and co-extensive with the pupil. Other teleosts have
various, usually diffuse and pallid yellow colorations; but in most species
the cornea is quite colorless. However much a fish may prefer bright sun-
light, that light is dimmer through water than it would be on land. No
fish can see more than a few rods at best owing to the extinction of
light in water, hence few can afford the luxury of a yellow filter unless
they are content to use their eyes mostly near the surface. Most fishes
enter deep, dim water at some time of the year. They must also do with-
out vision when beneath a covering of ice and snow. The eels are
exceptional, below the mammals, in having retinal capillaries; but these
are not intended as a filter — their significance is a very special one (see
pp. 405-6).

Of the amphibians, only the frogs approach diurnality, and these have
oil-droplets which may be colorless, or yellowed by the same carotenoid
pigment which colors the animal's fat. Other amphibians lack even color-
less droplets.

Among the reptiles Sphenodon is at once conspicuous since, though
nocturnal, and with its visual cells almost all converted from cones into
massive rods (see Chapter 16, section C), the oil-droplets and some yel-
low pigmentation thereof have been retained. The reader will remember
that Sphenodon has also kept the fovea of its diurnal forebears. (Fig.
82, p. 189). The turtles have ruby-red, orange, and lemon-yellow oil-
droplets. The crocodilians, like the similarly nocturnal toads, have got-

PHYLOGENY, CHEMISTRY OF FILTERS 203

ten rid of all droplets. So have many lizards and the snakes; and it is
in these two groups that we find evidence that once the oil-droplets have
been lost, they can never be regained :

Most lizards are diurnal and have bright yellow and colorless oil-drop-
lets. In the chameleons, there is claimed to be an additional yellow pig-
mentation of the inner layers of the retina in the region of the fovea,
though this matter requires further investigation. Secretive and fossorial
lizards such as Anniella have lost most of the pigment of the oil-drop-
lets, and nocturnal above-ground forms like Xantusia and Heloderma
have only completely colorless droplets. The logical final step has been
taken by the geckoes, which probably passed through a Xantusia-Vkt
stage (consult Fig. 25, p. 62) but later eliminated the useless, color-
less oil-droplet entirely. Some geckoes are so small, with such tiny eyes
(e. g., Sphcerodactylus and Gonatodes spp.), that they are able to be
more or less diurnal without benefit of a slit pupil. A couple of genera of
good-sized geckoes {Phelsuma and Lygodactylus) are round-pupilled
and diurnal, and have eyes large enough to demand special provisions for
this habit. It is probable that in them the visual cells have been recon-
verted into cones, and in Lygodactylus at least the lens is known to be
yellow.

The bearing of the structure of the eye upon the problem of the origin
of the snakes will be discussed later (Chapter 16, section D) ; suffice it to
say here that their lack of oil-droplets shows them to have originated as
light-shunning forms. The yellow lens has appeared here (as in Lygo-
dactylus and the squirrels) because the oil-droplets could not reappear,
upon the adoption of diurnality by forms whose photophobic ancestors
had discarded them. It is safe to say that any group which has oil-drop-
lets has had unbroken ancestry in forms similarly provided. Thus, the
presence of yellow droplets in frogs indicates that the early amphibians,
the Stegocephali, had droplets and were diurnal— as indeed we should
surmise from their bulk, their consequent need of the warmth of the sun,
and their complete freedom from terrestrial enemies during their evolu-
tion from the fishes. A similar argument would attribute diurnality to
the dinosaurian ancestors of the birds.

Of the mammals, the monotremes are usually called nocturnal though
the duck-bill is not strictly so, and has oil-droplets whose color or lack of
it has not been ascertained. Droplets occur in marsupials but are always
colorless so far as is known, though once erroneously reported to be pig-
mented in kangaroos. The placental mammals are nearly all crepuscular

204 ADAPTATIONS TO DIURNAL ACTIVITY

or nocturnal, with twenty-four-hour eyes among the ungulates and car-
nivores. None of these have filters. Only a few placental mammals,
mostly squirrels or primates, are strongly diurnal. The yellow lenses of
tree-shrews and squirrels, like those of diurnal geckoes and snakes, are to
be looked upon as substitutes for the irretrievable oil-droplets of remote
diurnal ancestors, which had been discarded by more immediate noc-
turnal ancestors.

The retinal capillary supply likewise makes its first appearance (except
for the eels) among the mammals, and cannot be ignored as a yellow-
filtering device. However, it is the least effective of all such devices, for
the capillaries are in general no less abundant in nocturnal mammals
than in diurnal ones, indicating that they absorb so little light that they
do not interfere with scotopic vision. Again, in areas centrales the capil-
lary network is not richer but is actually diminished, as though the shad-
ows of the vessels caused damage to the image which was not compen-
sated for by any differential filtering action. In the few mammalian areae
which have foveal depressions the capillaries are eliminated entirely. It is
in such areae (in the primates) that we find yellow pigment in the inner
layers of the retina — filling in, as it were, the lacuna in the capillary
plexus, but far more efficient as a filter than any equal area of the capil-
lary screen.

The nature of this pigment in the macula lutea is unknown. No studies
have been made of its status in sub-human primates. The amount is
known to vary greatly in different human individuals — being sometimes
so great as to render the person wholly blind to blue. Old observations,
now considered questionable, seemed to demonstrate more of the pig-
ment in brown-eyed than in blue-eyed persons. It has been claimed to be
soluble in alcohol and to change color in acids and alkalies. No modern
biochemist has given any attention to the pigment or to a resolution of
these apparent ambiguities of genetic and chemical behavior; but a fair
guess is that the substance belongs to the carotenoid family of pigments
and may be subject to the influence of diet. Simple experiments on the
perceptibility of blue stimuli would show whether the macular pigment
can be increased by feeding carotene or related substances to human
subjects; but such experiments have yet to be made.

The effectiveness, in human vision, of the combination of macular
pigment and the yellow lens is difficult to evaluate. We do know that
for a few weeks after a person has had cataracts removed, white light
looks decidedly bluish to him. We can only guess how much less sharply

PHYLOGENY, CHEMISTRY OF FILTERS 205

we would see without our filters, by determining how much more sharply
we see with additional yellow filters placed outside the eye. The fact that
we can gain appreciably in visual acuity by that means — as any expert
rifleman knows — shows, by analogy with the squirrel species of various
brightness-preferences, that the human eye is not purposed for use in
the very brightest of light. The prairie-dog, which prefers such light,
has his intra-ocular filter already so deeply colored that any extra-ocular
supplement to it would probably take more away from his vision than
it conferred. We are also led to consider man as not inherently strictly
diurnal by the fact that the ground-squirrel, the bird, or the diurnal
reptile unblinkingly tolerates intensities which force us to screw up our
eyelids or run for a pair of dark goggles.

Chapter 9
ADAPTATIONS TO NOCTURNAL ACTIVITY

(A) NOCTURNALITY AND THE EyE

Nocturnality and Crude Vision — The support of nocturnality, in
animals whose eyes mean much to them, comes wholly from great sensi-
tivity to light. This is possible only with a preponderance of rods in the
retina, which in turn makes for low visual acuity. However, if a noc-
turnal animal emphasizes rhodopsin and the length of his rods rather
than their diameters, and keeps summation in optic nerve fibers at a
minimum, he may be able to retain good resolving power in bright light
— ^provided he has means of reducing greatly the sensitivity of the eye
under those conditions. Such means, as we shall see, are exemplified by
the common slit-shaped pupil and the rare occlusible version of the
'tapetum lucidum'; and the geckoes show what can be done to make an
extremely sensitive eye very valuable in the daytime even to an essen-
tially nocturnal animal, if that animal insists upon being able to come
out by day with safety.

Nocturnal adaptation of the eye need not, therefore, be as restrictive
as bright-light adaptation. No cone-rich or pure-cone eye is useful at
night, but a pure-rod eye may be quite useful by day. But it is only
among the geckoes, in Sphenodon, and perhaps in the owls that forms
having great sensitivity have been able to combine with it a respectable
degree of resolving power. By and large, ocular adaptations for sensi-
tivity demand such a sacrifice of visual acuity that they make nocturnal
animals largely dependent upon senses other than vision.

The nocturnal animal is primarily an ear- and nose-animal; and this
is particularly true of aquatic forms, to which the chemical and auditory
senses are especially important because of their enhanced value over
distances in water. Both audition and olfaction are promoted under
nocturnal conditions, though not because of anything the nocturnal
animal has done to modify the receptors of those senses. Odors and
sounds are carried better by the night air and are dispelled more slowly
because of the absence of rising air-currents. At night, too, sounds have
an augmented attention-value since they are of fewer kinds and are out
of competition with abundant visual stimuli.

NOCTURNALITY AND VISUAL ACUITY 207

The diurnal animal, because he is cone-rich, has an acuity of vision
which makes the eye his best sensory instrument; but the nocturnal form,
being cone-poor, has unsharp vision and can make more accurate identi-
fications of enemies and food with his nose than with his eyes. The
'minimum separabile for parallel lines — the angular distance they must
be apart to be seen as separate — has been determined experimentally for
a number of animals by various investigators. Some of the values ob-
tained, not necessarily at all close to maximal and minimal values for all
vertebrates, are listed in Table V.

Table V

VISUAL ACUITIES FOR PARALLEL LINES (From various sources)

, . , Visual Corresponding distance Visual angle corresponding

Diurnal animals: angle, on retina, to imm. distance

minutes micra along visual cortex

Human adult 0.44 L89

0.48 2.06

0.50 2.14

(different reports) 0.80 3.43

0.82 3.52

0.83 3.56

Child 0.62 2.67

Chimpanzee 0.47 1.86

Rhesus monkey 0.67 2.33

Rhesus monkey,

along visual axis 4'

Rhesus monkey,

7° from visual axis 20'

Cebus monkey 0.95 3.31

Pigeon 2.70 4.89

Pigeon, 'homer' 0.38 .69

Gamecock (no fovea) 4.07 9.58

Nocturnal animals:

Cat, along visual axis 5.5 1°

Cat, 30° below axis 5°

Alligator 11.0

Opossum 11.0

Rat, pigmented 26.0 23.8

Rat, albino 52.0 47.7

208 ADAPTATIONS TO NOCTURNAL ACTIVITY

Advantages and Limitations — It may be stated categorically that
nocturnality, wherever it is characteristic of a large taxomic group, has
always been adopted secondarily by the ancestral form of the group.
Even more certainly, any nocturnal member of an otherwise diurnal
group has become nocturnal independently. We can be sure that all
vertebrate species would be diurnal if they could 'get away with it'.

The original chordates were bright-light animals. The early fishes
invented rods in order to extend their day and to be able to venture
from the surface to depths where they were safer, but where the lessened
illumination made necessary greater ocular sensitivity. The first land
animals were quite without predaceous enemies and were able to enjoy
the benefits of sunshine by becoming diurnal and heliothermic. But
increasing competition on land drove some forms into the cavern of
nocturnality to escape their enemies and to be able to feed in compara-
tive peace. These nocturnal amphibians and reptiles were the better off,
the smaller their bodies and the less they were dependent upon the sun
for the maintenance of rapid metabolism. The advent of small-bodied
descendants of the massive stegocephalians made nocturnality desirable
for the reduction of water-loss; and the small animal, being able to be
more active at a given environmental temperature, suffered no disad-
vantage from the change in habits.

Upon the invention of 'warm-bloodedness', independence of the sun
became greater. The mammals for the most part proceeded to become
crepuscular and nocturnal. The defenseless plant-eaters then found
greater safety in feeding, which is in them an almost continuous and
decidedly noisy process which places the animal at a real auditory dis-
advantage. Predators were forced into nocturnality by the paucity of
diurnal prey. The birds, however, were mostly prevented from aban-
doning diurnality by the high requirements imposed upon visual acuity
by the habit of flight. The ability to fly, in itself, served as a compensa-
tory defense against most predators, for birds are most vulnerable in the
form of eggs and young, as easily captured at one time of day as another.
The most conspicuously nocturnal birds, the owls, trace their ancestry
from diurnal birds through the crepuscular goat-suckers and frog-mouths.
They had no trouble in becoming nocturnal, for with their size and
roundheadedness, there was abundance of room in their heads for eyes
large enough to combine fair resolution with super-sensitivity.

Though nocturnality is something of a sanctuary from predators and
carries with it a coincidental improvement of audition and olfaction

ADVANTAGES, LIMITATIONS; LIGHTLESS HABITATS 209

(available also, of course, to the nocturnal predator) it imposes some
restrictions on diet. Tiny food objects cannot so easily be discerned, and
we find nocturnal animals to be relatively gross feeders, cropping vege-
tation which they have located by scent, rather than pecking at seeds,
and seizing large, unaware prey or motionless nestlings rather than
running down minute insects. Where insects do constitute the food, they
are not usually caught individually after visual location, but are 'trawled'
in numbers, as by the sticky tongue of an ant-eater. Seeds are sought in
numbers also— the rodents proverbially prefer their seeds in bunches,
as in a head of wheat or an ear of maize.

The superior visual acuity of the diurnal vertebrate often enables him
to maintain an enormous disparity between his armament and the de-
fenses of his prey — as when a hawk seizes a garter-snake or a kingbird
catches a fly. The nocturnal carnivore must have superior weapons, for
he must usually fight on more nearly equal terms with relatively much
larger prey. He prefers to catch nocturnal prey at a disadvantage in the
daytime, and it is not surprising that carnivorous forms are as often
twenty-four-hour animals as strictly nocturnal ones. The very strictest
of nocturnality is seen among those preyed-upon animals which are so
defenseless that they dare not come out of their hidey-holes even to bask.
In this category fall most of the legions of rodents.

Lightless Habitats and their Conquest — At this point we should
give a moment's attention to the fact that in addition to nocturnality
Ijy the clock', there are several other dim-light habits of vertebrates
which might seem to call for the same ocular modifications : the fossorial
habit (as exhibited by the mole, as opposed to forms like the woodchuck
which live in a burrow but use it only as a home) ; the cave-dwelling
habit (as developed by the permanent residents of caves in contrast to
such animals as the bats, which use caves only temporarily; the intern-
ally-parasitic habit; the deep-sea habit; and the occupation of very mud-
dy waters.

The habitats involved here are practically or entirely lightless, and
the animals which have adopted them have, for the most part, given
up any attempt to see and have allowed the eye to degenerate to a tiny,
even microscopic vestige, or to vanish altogether (see also pp. 387-405,
and Fig. 133). Well-developed eyes, adapted for dim-light vision, are
found only in those forms which occasionally venture into one of these
habitats for purposes other than mere temporary concealment; and out-

210 ADAPTATIONS TO NOCTURNAL ACTIVITY

side of the vertically-wandering fishes and whales these are very few
indeed. There are many other exceptions constituted by the deep-sea
fishes, most of which have enormous eyes whose retention and perfection
we can safely attribute to the timely invention of light-producing organs
by deep-sea animals. There is some point to a retention of a sense of light
and darkness by subterranean forms so that they may be aware when
their burrows have been broken into by the weather or by other animals.
Such animals, like the moles, marsupial moles, Spalax, and the fossorial
reptiles always have enough of an eye to make this much Vision' possible.
But the strictly cavernicolous vertebrates, all of them fishes or salaman-
ders, have only microscopic, completely non-functional eyes. Of the two
dozen or more cave-dwelling species of fishes, only two or three ever (as
individual variations) exhibit useful eyes, and in only one of these (the
Mexican Anoptichthys jordani) do the eyes vary from zero to complete
normality. The same degree of degeneracy as in cave fishes is seen in the
parasitic hag-fishes, which 'burrow' — in the bodies of their prey!

As for the muddy-water problem: several kinds of gobies and at
least one mammal (the fresh-water dolphin Platanista gangetica, swim-
ming through the roiled waters of the great Indian rivers), have given
it up as an impossible job. The eye of Platanista has 'gone bad' in a
unique way — this is the only vertebrate with a macroscopic eye which
lacks all traces of a lens. In such limicolous gobies as Austrolethops and
Trypauchen, and in the sole Typhlachirus, the entire eye is minute or
quite obsolescent. In general, the fishes of silty rivers, as in our Great
Plains, have somewhat undersized eyes which are useful only close to
the surface, where alone there is adequate light. The fishes of the peculiar
Lake Balaton have however made a valiant effort to cling to vision
despite the quasi-opacity of the water in which they swim (see p. 236).

The Eye as a Whole — It was hinted earlier (p. 172) that nocturnal
animals, as well as diurnal ones, have a special need for a large eye. The
need is a very direct one in the case of a diurnal eye: to enlarge the
image. The reason why large eyes are desirable for a nocturnal animal is
a little more complicated. It is not at all for the improvement of resolving
power — a whale eye the size of a baseball has but 2% of the resolving
power of the human eye, due to its tremendous retinal summation.

If we could be watching an animal in the process of evolving nocturn-
ality, we might feel impelled to advise him to enlarge his eyes "so more
light can enter them." But on second thought we should realize that this

THE NOCTURNAL EYE 211

would only tend to dim the image on the retina. Doubling the diameter
of the eye will double the diameter of the retinal image. This will reduce
the illumination per unit area of that image to one-fourth. But suppose
the pupil enlarges in proportion to the whole eye. Doubling its diameter
will increase, by four times, the amount of light it admits. The illum-
ination of the retina will thus have the same strength in any and all
eyes whose proportions are exactly the same, regardless of their abso-
lute sizes.

An eye which is simply larger will not, then, have brighter images and
greater overall sensitivity in dim light. But enlarging the pupil more yet,
out of proportion to the size of the eye, will brighten the image. If the
pupil is enlarged the lens must be broadened too, if spherical aberration
is not to be increased. A broader iris (to make room for a larger pupil)
and a broader (and proportionately thicker) lens will, in themselves, call
for an increase in the absolute size of the eye if it is to remain mechan-
ically and biologically in balance. We have arrived, by a rather devious
route, at a justification for advising our nocturnally-inclined animal to
enlarge his eyes — and to enlarge them in a disharmonic manner.

Enlarging the lens 'out of proportion' to the eye moves the optical
center of the cornea-lens apparatus backward (Fig. 71, p. 173). When the
curvature of the cornea, lens, or both is now sharpened to keep the image
from receding behind the retina, we find that the anterior chamber has
deepened and the image has shrunk. This shrinkage of the image is fine
up to a certain point, for it accomplishes what was wished : that bright-
ening of the image which lets the eye operate in dimmer light. The retina
of such an animal being poor in cones, visual acuity is low enough in all
conscience already, but it may suffer too much unless now the eye is en-
larged harmonically still further, to spread the image without detracting
from its brightness. That species is fortunate which has head-room for
the development of sensitivity through eye size alone. The cat has a
large eye for its size, but a proportionately small retinal image — only
38% of the diameter of that of the horse, whereas the diameter of the
eyeball is 50% of that of the horse. The human ocular axis is only 1.19
times that of the cat, but man's retinal image is 1.37 times as broad as the
cat's. Some small, small-eyed animals have had to do the whole job by
making the lens spherical, the cornea perhaps remaining broadly curved
since the lens has more to do with pulling backward, into the eye, the
optical center whose distance from the retina determines the size of the
image. The large-eyed carnivores such as the cats have greatly sharpened

212 ADAPTATIONS TO NOCTURNAL ACTIVITY

the curvature of the cornea and thus have been able to keep the lens
from becoming so large and so round as to increase spherical aberration
to any disastrous extent.

The end result of the juggling of these factors is an eye which, as
compared with a diurnal eye such as that of man, is :

1. Relatively large for the size of the animal, and absolutely large if
there is room for it in the head — even altered in shape ('tubular' eyes —
v.i.) if there is not space enough for an orthodox eye.

2. Provided with a relatively large anterior segment, making room
for a large-opening pupil and a proportionately large lens, which is :

3. More nearly or even quite spherical and set far back from the
cornea (which where convenient is less sharply curved), so that the
anterior chamber is often deepened and:

4. The optical center is far back within the eye, resulting in a smaller
and brighter retinal image.

'Tubular' Eyes — There are certain interesting consequences of these
changes which, in themselves, add nothing to the capacity of the eye for
operation in dim light. Whereas the diurnal eye tends to have a small
anterior segment and a large fundus, the nocturnal eye tends to have a
large anterior segment and, the image being small, would gain nothing
from having a posterior segment proportioned to it as in a diurnal eye.
The result is a relatively small fundus, rendering the eye somewhat
tubular in some species in which the anterior segment has become enor-
mous. This is true of the owls and their relative Podargus, some lemu-
roids, and a majority of the deep-sea fishes which have kept their eyes.
These forms, so to say, have ballooned the eye to the point where there
is barely room for it in the head (Fig. 84), and have continued to en-
large the anterior segment so that the effect is produced of the useless
equatorial region of the globe having been cut away (Fig. 136b, p. 400).
The eye of the deep-sea fish bears the same relation to a standard-shaped
fish eye of the same axial length as does the part of an apple, removed
by a cylindrical coring tool, to the intact apple.

The small size of the retina in tubular nocturnal eyes tends to make
more narrow the angle which embraces the visual field outside of the
eye. This demands considerable rotability of the eyeball in the orbit, in
order that the animal shall be able to see about him through a safely
wide angle. But, these tubular eyes have become so large that they are

'TUBULAR' EYES; SPHERICAL LENSES 213

locked in a close-fitting orbit and cannot be turned. Even though the
oculomotor muscles are present in owls, the eye of an owl cannot be
moved in the orbit by force. In consequence, the owls and the lowest
primates (e.g., Tarsius) have evolved an extraordinary rotability of the
head upon the axis of the body. The neck in all birds is notoriously
flexible — even the strictly diurnal hawks can rotate the head about 180 ;
but the owls can revolve theirs through 270° or more. To explore their
surroundings visually, the deep-sea fishes, lacking a neck, must turn the
whole body, or bend the trunk if they are slim enough to do so.

Spherical Lenses — Where the eyes of small nocturnal animals have
remained spherical and not enlarged unreasonably, the lens is always
even larger in proportion than in tubular eyes. In fact, when the lens

Fig. 84 — Tubular (miscalled 'telescopic' ) eyes.

a, owl, Bubo sp. x 1. After Putter, b, prosimian, Galago crassicaudatus garnetti. x2.46.
After Franz, c, deep-sea fish, Argyropelecus sp. Redrawn from Hesse.

swells (through evolution) in size it swells also in shape, so to say, and
tends toward a sphere (Fig. 71, p. 173). When it has attained this shape,
as in small bats, most rodents, and the rodent-like opossums, an advan-
tage is gained in connection with the need for voluntary eye movements
— the latter can be allowed to diminish or even to disappear. Part of the
reason for this is the absence of an area centralis, owing either to its dis-
appearance or to a failure to evolve one. Since there is no reason to aim
any particular retinal spot at the object under scrutiny, there is no reason
for aiming the eye at all. Largely, however, the diminution of eye move-
ment is due to the periscopic action of a spherical lens when associated
with a concentric or nearly concentric retina. Such a lens casts an image
which is small, but is equally good from whatever direction the object

214 ADAPTATIONS TO NOCTURNAL ACTIVITY

is imaged. Hence the eye with a spherical lens sees its object about as
well in the periphery of the retina as in the fundus. A moving object can
therefore travel farther alongside or around the head of the animal be-
fore the latter need make any movements to keep it in good view. The
only extra requirement is a wide cornea, and the net result is a widened
visual field.

Broad Cornece — The eflFect of an extensive cornea — and some, like
that of the house-mouse, cover about half the surface of the eyeball —
like that of large ocular size as such, is easily misunderstood. As has
been made clear, it is not true that a unit retinal area is more brightly
illuminated in a large eye {ceteris paribus) than in a small one. This
does become true only when the lens and pupil are disproportionately
large. Neither does a large cornea let in more light, as is commonly
supposed. It is the pupil which regulates the amount of light that reaches
the retina. The cornea would not need to be any larger than the fully
dilated pupil, if the iris were right against the cornea. To let light
rays hit the front part of the retina and increase the periscopy of the
eye, however, the cornea must be broader than the pupil; and the more
so, the farther the iris and lens are from the cornea. Since nocturnal
eyes tend to have deep anterior segments for the reasons given above, we
can see that their relatively broad corneas (compare lynx and man in Fig.
71, p. 173) are a consequence of these other ocular changes, and do not
in themselves promote sensitivity to light. The recession of the optical
center into the eye, in strongly nocturnal forms, cannot be wholly com-
pensated for by a broad cornea. The deeper the optical center within the
eyeball, the smaller and brighter the image will be; but the farther back
the center is from the pupil, the larger the pupil and the cornea must
become in order to maintain a wide-angled visual field. Despite all efforts
of pupil and cornea, the nocturnal eye tends dangerously toward 'tube
vision' — that restriction of visual field which we experience in looking
through an aperture located before the eye. The nocturnal animal, there-
fore, dares not rely solely upon increasing the objective intensity of the
image, by manipulating its relative size through mere gross changes in
ocular morphology and optics. He must keep the need for such changes
minimal (since they inevitably detract from visual acuity and visual
angle) by promoting the response to whatever light is available. This
necessarily means increasing the sensitivity of the retina itself.

BROAD CORNER; ROD-TO-CONE RATIOS 215

(B) The Nocturnal Retina

Rod'.Cone Ratios — We expect to find rods greatly predominating in
nocturnal retinae; and we are never disappointed. However, pure-rod
retinas are not as common among strictly nocturnal animals as pure-cone
retinae are among strictly diurnal ones. Fabulous though the cat's ability
may be for "seeing in the dark," she has a very respectable number of
cones — about a third as many as we ourselves, who are marooned among
the strongly diurnal animals when our artificial lights are taken away
from us.

This persistence of cones in nocturnal retinae calls for a Uttle special
explanation, for it has served some people as a sufficient excuse for
rejecting the Duplicity Theory entirely. The first prominent opponent
of the theory — Wilhelm Krause, a contemporary of its formulator. Max
Schultze — saw more cones than there really were in many nocturnal
forms, and drew incorrect conclusions from other animals through im-
perfect knowledge of their habits. Several modern investigators (par-
ticularly Mile. Verrier) have apparently thought that if there is any-
thing to the Duplicity Theory, then cats and owls should have no cones
whatever.

This view fails to take accoimt of the fact that whereas a diurnal
lizard never gets out of bed for a midnight snack, a cat may appreciate
a sun-bath at high noon. The nocturnal animal which wishes (as most
do) to be able to come out sometimes in daylight, is wise to retain some
cones for the improvement of form-sense, for he is otherwise at a great
disadvantage if taken by surprise by a diurnal enemy.

If this interpretation seems weak, we can surrender any positive argu-
ment in favor of a nocturnal animal's keeping cones, and still believe the
Duplicity Theory to be well founded. The only pure-rod retinae are in
nocturnal animals, and the proportion of cones in such animals is never
very high. Where there are so few as to seem utterly useless, as in the
opossum or the rat, it may be pointed out that unneeded cones are
probably harder to get rid of than are unwanted rods. The vertebrate
eye, like the brain, is so delicately-balanced an organ that it very rarely
contains anything useless. The eye is comparable to a machinery-crammed
submarine — if there is no proper niche for a thing, it is almost certain
to be in the way. In a strictly diurnal eye, even a few rods can detract
very immediately from resolving power, and they are completely elimi-
nated from every good area centralis. But cones, as we have learned, keep

216 ADAPTATIONS TO NOCTURNAL ACTIVITY

to themselves in the matter of their nerve-ceil connections, and ten cones
scattered among a thousand rods cannot cost the retina as much in
sensitivity as ten rods, scattered among a thousand cones and hooked
up to a single optic nerve fiber, would cost it in resolving power. There
is consequently simply not the urgency for getting rid of cones in noc-
turnal animals, that there is for weeding out rods in diurnal forms.
This is quite apart from any greater usefulness of 'even a few' cones
than of 'only a few' rods. The turtles are conspicuously exceptional in
having only a very few rods scattered in an almost pure-cone retina —
but even these may be useful since they are more numerous in light-
shunning forms such as Chelydra, and in the nocturnal Pseudemys.

Pure-Rod Animals — A pure-rod retina is automatically obtained
where, as in some lizards (geckoes, etc.) and snakes (Hypsiglena, Phyl-
lorhynchus) it has been manufactured by transmuting all of the single
and double cones of an ancestral pure-cone retina into single and double
rods. Transmutation has left so very few unchanged cones in Sphenodon
that in an entire section of its very large eye, never more than twenty
can be found. Aside from these forms, absolutely cone-free retinse which
once were duplex, and have lost their cones, are known for a certainty
to occur only in deep-sea fishes, the bats, and the armadillo. Some others
probably have only rods — all but one or two elasmobranchs, Lepidosiren
among the lungfishes, caecilians, the hedge-hog, the guinea-pig, the whales
and seals, most lemuroids and Aotus — but all of these need addi-
tional histological study (since most of these were last studied, micro-
technical methods have improved enormously) . Still others, like the rat
and other nocturnal rodents, are widely believed to have no cones but
do indeed have a few. One ridiculous statement often seen is that rats
and owls "have a few rudimentary cones." In a duplex retina, no visual
cell is ever rudimentary, though one population of visual cells may be so
scant as to deserve the term, like the cones of Sphenodon or the rods of
turtles. As a matter of fact, owls have enough cones so that they are
able to see more acutely by day than by night. Rochon-Duvigneaud once
picketed a Bubo bubo in an open field, and found that it could detect
an approaching hawk which was flying so high as to be invisible, at that
moment, to humans.

Summation — In nocturnal animals the rods tend to be very slender as
well as very numerous, causing the outer nuclear layer to thicken greatly
(Fig. 72, p. 177). In lungfishes and amphibians, however, the rods are

PURE-ROD ANIMALS; SUMMATION 217

bulky and exceed the cones in total volume as well as in actual numbers
(Fig. 64, p. 148) — just as in most teleosts the huge cones outweigh the
more numerous, tiny rods (Fig. 94, p. 237). The difference in acuity-
performance of bulky cones versus slender ones is obviously very great,
for the retinal limit of resolving power is set by the distance on centers
between the cones. It is not so easily apparent why nocturnal animals
should have slender rods and other animals not only fewer but plumper
ones. The slenderness of a rat's rods has not been produced for its own
sake. The distance between centers of adjacent rods has nothing to do
with the overall sensitivity of the rod population — but the number of rods
which can conveniently be hooked to a bipolar cell (this being pro-
moted by slenderness and close aggregation) has everything to do with
it. In amphibians and lungfishes not only the visual cells but most
somatic cell-types are notoriously huge. It makes an interesting specu-
lation: did the unknown factor which made their cells so large doom
the amphibians forever to low visual acuity because their cones are
usually bulky, and to a not particularly high sensitivity also, because
their rods are so big?

The thick outer nuclear layer resulting from the slenderness of noctur-
nal rods (the tiger holds the record here!) is pretty well counterbalanced
by the thinning of all other retinal layers due to the great extent of sum-
mation of visual cells in bipolars, and of these in ganglion cells, for the
sake of sensitivity and at a tremendous sacrifice in resolving ability. Noc-
turnal animals, on the whole, have thinner retinae than diurnal groups,
and have much more slender optic nerves. It is not at all unusual for
several thousand rods to be summated in one optic nerve fiber. The reti-
nal adaptations for sensitivity, both within the visual cells themselves and
in their relationship to optic nerve fibers, render the receptive tissue of a
nocturnal animal so extraordinarily sensitive to light that it cries out for
protection from any light stronger than that of the moon. We go on now
to consider how this protection has been obtained.

(C) The Slit Pupil

The elementary discussion of pupil mobility in section C of Chapter 7
was based upon the commonest form of the aperture — the circle. There
are a number of departures from this primitive shape, the most wide-
spread one being the slit, which in land animals, at least, is most com-
monly vertically oriented, for which a reason is given later (see p. 428).

218

ADAPTATIONS TO NOCTURNAL ACTIVITY

Value of the Slit Form — The slit pupil, like nearly all pupils, dilates
in dim light to a perfect or almost perfect circle. Very many years ago, a
generalization had already been found possible, to the effect that the slit
pupil is associated with nocturnal habits. Yet under nocturnal conditions
the slit pupil becomes as round as any. Obviously it has nothing to do
with vision in dim light; what then does it accomplish?

The broadly oval pupil of a frog can contract to a diameter which is
one-third of its fully dilated size; but to bring about this degree of con-
traction, the intensity of light must be increased 200 times. We have

Fig. 85 — Diagrams of mammalian iris musculatures.

a, round pupil of diurnal and strictly nocturnal forms, showing simple sphincter (solid
lines) and symmetrical dilatator (broken lines).

b, vertical slit (of cat), characteristic of nocturnal forms which bask. Part of the sphincter
surrounds the pupil, but two bundles which cross above and below and continue to the
periphery have a scissor-aciion upon the pupil, compressing it laterally. The dilatator
(broken lines) is quite symmetrical — contrast Figure 88, page 223. Redrawn from Raselli.

c, horizontal pupil (of horse), characteristic of ungulates, some whales, and other species.
Some sphincter fibers are oriented radially and are anchored in connective-tissue sectors
(stippled) which are devoid of dilatator fibers (broken lines). The pupil can expand to a
circle; but when the sphinaer fibers contract, the terminal ones force the pupil to become
a horizontal rectangle, indented by the corpora nigra (white). Based upon drawings and
descriptions of Eversbusch.

already noted that the frog is more dependent upon the photomechanical
changes of its retina for avoiding dazzlement in bright light. His pupil
cannot cope with the situation; but for that matter, neither can any pupil
whose closure depends upon a ring-shaped, sphincter muscle. We our-
selves can easily be dazzled even when our pupils are closed as far as they
will go. True, a lizard or a garter-snake is comfortable in even brighter
light despite the practical immobility of the pupil — but these forms have
only the relatively insensitive cones in their retinae.

Where the rods are very much in the ascendant, the circular pupil
ceases to be adequately protective. The sphincter may contract fully, but

THE SLIT PUPIL

219

even then it has considerable length, for it cannot eliminate itself entirely.
The arrangement of the iris muscles around a slit pupil, however, is such
as to make it easy for the slit to be closed without any impossible degrees
of muscle contraction — closed entirely in some instances, or in any case
to so small an area that the pupil is far better able to keep pace with
intensity-changes than it is in the frog or even in ourselves. (Fig. 85a, b) .
The slit pupil is hence in a sense paradoxical, for though it is an adap-
tation to nocturnaUty it has nothing whatever to do with seeing in dim
light. Hosts of nocturnal species do not have such a pupil, and are well
able to see under scotopic conditions. They get along with a circular
pupil because they are content to stay out of bright light. Any strongly
nocturnal, rod-rich animal which cares or dares to venture out in the sun,
— whether a cat stalking the barnyard sparrow, a gecko seeking flies, a

Fig. 86 — Pupil shades in mammals. After Lindsay Johnson.

a, 'umbraculum' (operculum) of hyrax, Procavia (an analogous structure occurs in many
whales), b, corpora nigra of Gazella dorcas. c, corpora nigra of camel.

snake seeking warmth, or a shark basking at the surface — needs a slit
pupil and will be found to have one.

Even some diurnal and arhythmic animals have devices for shielding
the pupil from intense glare coming directly downward or reflected up-
ward from the ground. Among such devices are the pigmentation of the
upper cornea in surface-loving needle-fishes and in Torpedo, the expan-
sible pupillary opercula of some fishes and whales (Fig. 65, p. 158), the
(voluntarily?) expansible 'umbraculum' above the pupil of the hyrax,
and 'corpora nigra' along the pupil margins of ungulates (Figs. 85c, 86).

Distribution and Meanings of Pupil Shapes — Phylogenetically, the
slit pupil is first met with in the elasmobranchs (Table VI, next page),
the only group of fishes whose pupils have much contractile excursion.
Most sharks have practically circular pupils, and a slit is characteristic

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222 ADAPTATIONS TO NOCTURNAL ACTIVITY

only of those forms which come frequently to the surface or into shallow
water — Scylliorbinus, Lamna, Selache, etc. Most of the elasmobranchs
whose eyes aim strongly upward are among the Batoidei — the skate-ray-
torpedo group. With the exception of the mantas, the batoids have oper-
cula (Fig. 65a, b; p. 158), which slope downward and slightly outward
over the pupil, and expand in bright light to block the aperture. The oper-
cular margin may be serrated, as in Raja, or smooth as in Dasyatis. It is
not unusual for rays to bask at the surface in summer, and they are then
exposed to especially strong light, considering the fact that their retinas
are pure-rod. The monk-fish (Squatina, a sort of imitation ray which is
really a shark) and the electric ray Torpedo have slits — horizontal in the
latter as in Selache and Sphyrna, diagonal in Squatina as in Scy