VISION IN VERTEBRATES VISION IN VERTEBRATES M. A. Ali and M. A. Klyne Universite de Montreal Montreal, Quebec, Canada PLENUM PRESS • NEW YORK AND LONDON Library of Congress Cataloging in Publication Data Ali, M. A. (Mohamed Ather), 1932- Vision in vertebrates. Includes bibliographies and indexes. I. Vision. 2. Eye. 3. Vertebrates-Physiology. I. Klyne, M. A. II. Title. [DNLM: I. Eye-physiology. 2. Vertebrates. 3. Vision. WW 103 A398v) QP475.A45 1985 596'.01'823 85-12141 ISBN 978-1-4684-9131-9 ISBN 978-1-4684-9129-6 (eBook) DOl 10.1 007/978-1-4684-9129-6 ©1985 Plenum Press, New York Softcover reprint of the hardcover 1s t edition 1985 A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y. 10013 All rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher PREFACE When Dr. Katherine Tansley's "Vision in Vertebrates" appeared in 1965, it filled a real void that had hitherto existed. It did so by serving at once as a text-book: for an undergraduate course, a general introduction to the subject for post-graduate students embarking on research on some aspect of vision, and the interested non-specialists. Gordon Walls' "The Vertebrate Eye and It.s Adaptive Radiation" and A. Rochon-Duvigneaud's "Les Yeux et la Vision des Vertebres" have served as important sources of information on the subject and continue to do so even though it is 40 years since they appeared. However, they are essentially specialised reference works and are not easily accessible to boot. The genius of Katherine Tansley was to present in a succinct (132 pages) and lucid way a clear and an interesting survey of the matter. Everyone liked it, particularly the students because one could read it quickly and understand it. Thus, when it seemed that a new edition was desirable, especially in view of the enormous strides made and the vast literature that had accumulated in the past 20 years, one of us (MAA) asked Dr. Tansley if she would undertake the task. Since she is in retirement and her health not in a very satisfactory state both she and her son, John Lythgoe (himself a specialist of vision), asked us to take over the task. In view of the advances made and in view of the fact that it will virtually be impossible anymore to put everything in 100 to 150 pages, we decided to prepare an altogether new book, larger in size, inspiring ourselves however from Dr. Tansley's approach. We have illustrated the book abundantly and attempted to give as many references as possible, obviously putting emphasis on those that are reviews and books. There are a number of specialised works, such as the "Handbook of Sensory Physiology" series that serve particularly the specialist as references. Our aim is to attempt to v vi PREFACE present the subject in a concise way so that an under-graduate or a beginning graduate student is able to get an overall view of the way vertebrates see. We hope that we have mostly succeeded in doing this. We should welcome comments and criticisms from interested readers. We thank Madame Hoda Farid for assistance with the preparation of the illustrations, Monsieur Jean-Luc Verville for photographic help and Mademoiselle Francine Chatelois for pre- paring the index. We appreciate the encouragement we received from our editor, Mr. Kirk Jensen. Preparation of this book was also aided by an operating grant from the Natural Sciences and Engineering Council of Canada. Montreal, Spring 1985 M.A. Ali M. A. Klyne TABLE OF CONTENTS Preface v 1. Structure of the Vertebrate Eye 1 Cornea .... 4 Aqueous Humour 5 Iris . . . . . . 6 Ciliary Body . . 7 Crystalline Lens 7 Vitreous Body 8 Retina .... 8 Development 12 Eye Movements 15 2. Physiology of the Retina 19 Photoreceptors. . . 19 The Outer Segment 19 The Inner Segment . 23 The Outer Nuclear Layer 26 The Receptor Terminal. 26 General ......... . 28 Secondary {Intermediate} Neurones 29 Bipolar Cells . 29 Horizontal Cells 30 Amacrine Cells 30 Ganglion Cells 31 Electrophysiological Evidence of Retinal Char- acteristics ... 31 Applica tions . . . . 33 vii viii CONTENTS ERG ..... 33 Cone Potentials 34 S-Potentials. . 34 Ganglion Cells 35 Purkinje Shift . 36 Movement Perception 38 3. Visual Pigments . . . . . . 43 Biochemistry ..... 46 Methods of Study . . . . 48 Extraction Technique 50 Reflexion Technique . . . . 64 Microspectrophotometry (MSP) 65 Physiological Sign if icance 70 4. Accommodation . . . . . . 73 Fishes ........ . 77 Active Accommodation . 77 Inactive Accommodation 80 Amphibians 82 Reptiles and Birds 84 Reptiles •.. 84 Birds ..... 85 Active Accommodation 85 Inactive Accommodation 88 Mammals ....... . 91 Active Accommodation . 91 Inactive Accommodation 92 5. Adaptations to Light and Dimness 95 Regulation of Light Reaching the Visual Pigment 97 Pupil Size .....•......... 98 Retinomotor (PhotomechanicaI) Movements 98 Absorption by Visual Pigment 101 Neural Processing. . . . . . . . 104 6. Adaptations to Various Modes of Life 107 The Diurnal Habit. . . 107 Eye: Size and Shape 108 Pupil. . . . . . . 110 Intra-ocular Filters 111 Cornea and Lens. . 111 Oil Droplets. . . . 114 Retina ..... . 115 The Nocturnal Habit 119 Eye: Size and Shape 120 Pupil ...... . 121 CONTENTS ix Retina . .. . 123 Tapetum .... 125 The Arhythmic Habit 127 Summary ..... 129 7. Retinal Adaptations to Habitats 133 Aquatic Medium 134 Photic Qualities 137 Clear Waters 137 Turbid Waters . 141 Deep-Sea ... 145 Tide Pools 146 Marshes .• 147 Terresterial Environment 147 Temperature . 148 Summary ... 150 8. Acuity and Sensitivity 151 Acuity .. 153 Sensitivity 155 Summary. 160 9. Colour Vision 161 Vision of Monochromats 162 Vision of Dichromats • 164 Vision of Trichromats . 166 Defects in Colour Vision . • 168 Colour Vision in Animals . 171 Fishes . • 171 Amphibians 173 Reptiles . 173 Birds. • . 173 Mammals. .. . ... 174 Determination of Colour Vision 175 10. Visual Transduction . . . . .. 179 Calcium Hypothesis • • . . . 181 Negative Transmitter Hypothesis 183 Calcium and cGMP . . .. .• 186 11. Processing by the Central Nervous System . 191 Optic Nerve, Chiasma and Tract 191 Optic Tectum . • .. .• 193 Pretectal Area • . . • . . • . 196 Dorsal Thalamus • . • . . • . 197 Visual Centres in the Telencephalon 201 Evolution of the Mechanisms of Vision 202 x CONTENTS Binocular (Stereoscopic) Vision 204 Processing of Colour Vision . . 205 Cone Inputs to LG N Cells . 207 Relation to Visual Behaviour 210 Wavelength Discrimination. 212 Contrast and Similitude 213 Summary .... 214 12. Visual Ulusions .... 215 Size/Shape Distortion 215 Geometric Illusions 216 Ambiguous Forms. 219 Paradoxes . . . . 221 Movement Distortion 223 Brightness and Colour Distortions 226 Summary ...... . 228 13. Extraocular Photoreceptors 231 Pineal ....... . 232 Brain and Dermal Photoreceptors 236 Encephalic Photoreceptors 238 Dermal Photoreceptors 239 Summary. 240 References . . . 241 Systematic Index 257 Subject Index .. 261 1 STRUCTURE OF THE VERTEBRATE EYE The basic pattern of all vertebrate eyes is similar. The cross- section of the eyebaU can be represented by a circle with one-fifth of its circumference removed. Into this is fitted a clear segment which has a slightly smaller radius of curvature (cornea). The outer coat, which makes up the remaining four-fifths of the eyeball, is a tough fibrous structure whose opaque posterior part (sclera) is continuous with the strongly curved, transparent cornea (Fig. 1.I). The vertebrate eye may be compared to the camera, and this analogy is illustrated in Fig. 1.2. In terresterial animals good vision is largely dependent on the optical perfection of the anterior surface of the cornea, and since this surface is exposed it must be well protected. This is done by the lids and by the secretion of tear fluid. The eyelids are composed of compressed fibrous tissue containing muscles and glands. The eyelids close reflexly at the approach of a foreign body, e.g. if the cornea is touched or if the light is too intense. In addition, many animals (e.g. frogs, some birds) have a nictitating membrane or third eyelid composed of transparent and semi- transparent tissues which can be drawn horizontally across the eye between the other two eyelids. Some animals (e.g. snakes) do not have eyelids but possess a 'spectacle' instead - a covering of transparent skin continuous with the skin of the head. Further protection of the cornea is afforded by tear fluid secreted by the lacrimal and Harderian glands. The tear fluid, which varies in composition in different animals, serves to irrigate the anterior surface of the cornea and the inner surface of the eyelids, as well as to wash dust and other foreign particles out of the eye. In some aquatic mammals (e.g. seals) it protects the cornea from salt water.