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SYSTEM OF OPHTHALMOLOGY
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The scheme for the "System of Ophthalmology" is as follows, but its
division into different volumes is liable to alteration.
Vol. I. THE EYE IN EVOLUTION
Vol. II. THE ANATOMY OF THE VISUAL SYSTEM
Vol. III. NORMAL AND ABNORMAL DEVELOPMENTPt. I. EmbryologyPt. II. Congenital Deformities
Vol. IV. THE PHYSIOLOGY OF THE EYE AND OF VISION
Vol. V. OPHTHALMIC OPTICS AND REFRACTION
Vol. VI. OCULAR MOTILITY AND STRABISMUS
Vol. VII. THE FOUNDATIONS OF OPHTHALMOLOGYHeredity, Pathology, Methods of Diagnosis,General Therapeutics
Vol. VIII. DISEASES OF THE OUTER EYEPt. I. Conjunctiva
Pt. II. Cornea and Sclera
Vol. IX. DISEASES OF THE UVEAL TRACT
Vol. X. DISEASES OF THE RETINA
Vol. XL DISEASES OF THE LENS AND VITREOUS;GLAUCOMA AND HYPOTONY
Vol. XII. NEURO-OPHTHALMOLOGY
Vol. XIII. THE OCULAR ADNEXAnLids, Lacrimal Apparatus, Orbit and Para-orbital Structures
Vol. XIV. INJURIES
Vol. XV. INDEX OF GENERAL AND SYSTEMICOPHTHALMOLOGY
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SYSTEM OF OPHTHALMOLOGYEDITED BY
SIR STEWART DUKE-ELDERG.C.V.O., M.A., LL.D., Ph.D., D.Sc, M.D., D.M., F.R.C.S., F.R.C.S.E., F.A.C.S., F.R.A.C.S.
VOL. I
THE EYE IN EVOLUTIONBY
SIR STEWART DUKE-ELDER
WITH 902 ILLUSTRATIONS, 15 COLOURED PLATESAXD 3.')0 MARGINAL ILLUSTRATIONS
ST. LOUIS
THE C. V. MOSBY COMPANY1958
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@1958 by Henry Kimpton Publishers,7 Leighton Place,
Leighton Road,
London NWH
All rights reserved. No part of this publication maybe reproduced, stored in a retrieval system, or trans-
mitted, in any form or by any means, electronic,
mechanical, photocopying, recording or otherwise,
without the prior permission of the publishers.
Reprinted 1970, 1976
ISBN 85313 213 a
MADE AND PRINTED IN GREAT BRITAIN
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PREFACEThe reception accorded to my Textbook of Ophthalmology has per-
suaded me that there is a need for its continuation in a second edition. Theseven volumes of the Textbook took almost a quarter of a century to write,
a period unfortunately longer than it might have been owing to the exigencies
of war. The first four volumes have long been out of print—and inten-tionally so because they have long been out of date. It is to be rememberedthat the second volume was written before the suljjhonamides were intro-duced ; the third before the antibiotics revolutionized the therapeutics of
infective diseases ; both of them before the role of viruses in ocular diseasewas adequately appreciated ; the physiology of the eye of yesterday isunrecognizable when compared with that of today ; even the anatomy hasbeen transformed by more elaborate optical and chemical methods ofinvestigation and the advent of the electron microscope. The re-writing ofthe whole work if its com^^rehensive nature were to be retained would be animmense task occupying more time than I could reasonably expect to haveat my disposal. Moreover, tomorrow ^^•ill be different from today, and ifa work such as this is to be of any lasting value it would seem to me desirablethat a new edition be published at least every fifteen or twenty years
;
fortunately, ophthalmology is no static science.
It therefore seemed to me wise to sliare the task of re-writing theoriginal Textbook with my colleagues at the Institute of Ophthalmology inLondon. I am grateful that they have accepted this burden. For thisreason I have changed the name of the book to a ''System of Ophthalmology "
since it will necessarih^ be less personal.
This first volume in the new series is an extension of the first twentypages of Volume I of the old Textbook ; this I have %^Titten myself, largelybecause it is a subject in which I am particularly interested—and I wishedto write it. The subject-matter has never been gathered together in a singlebook before and it is my hope that it will interest ophthalmologists in sofar as it forms the basis of the science of vision ; and it may be that it will beof value also to those whose interest is biological rather than clinical.
;
The numerous marginal sketches are not usual in a book of this type.To the student of natural history they may seem superfluous, but to theophthalmologist some of the animals may be unfamiliar and the drawingsmay perchance add meaning to the zoological nomenclature and thus givethe text more life and interest. It is to be noted, however, that they aredrawn not to scale, but approximately to a standard size to fit into a 1-inchmargin,
Stewart Duke-Elder.Institute of Ophthalmology,London,1957.
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ACKNOWLEDGEMENTSIn the preparation of this book I have incurred a considerable amount of
indebtedness which is a pleasure to record.Many of the illustrations are borrowed, and in each the source is acknowledged.
There are, however, five sovirces from which I have liberally drawn, and these meritspecial thanks : Dr. Gordon Walls, for a number of his original drawings ; Masson etCie of Paris, who have allowed me to use some illustrations from Rochon-Duvigneaud'sclassical work, Les Yeux et la Vision des Vertebris ; Dr. Maurice Burton and hispublishers, the Elsevier Publishing Co. of Holland, for some illustrations from TheStory of Animal Life ; the Royal Society for permission to iise a large number ofLindsay Johnson's illustrations published in their Proceedings ; and Macmillan & Co.for giving free permission to copy a large number of the illustrations of animals in theCambridge Natural History in the form of inarginal sketches.
In preparing the illustrations I have had the willing co-operation of Dr. PeterHansen and the Department of Medical Illustration of the Institute of Ophthalmology,the assistance of which, particularly that of Mr. T. R. Tarrant, the Medical Artist, hasbeen invaluable. The Zoological Society of London has lent me a number of photo-graphs, as also has the Natural History Museum of London, together with specimensof various invertebrates. Professor Ida Mann has allowed me to use a large numberof her illustrations of the eyes of animals, and Dr. Kevin O'Day of Melbourne hasallowed me to use photographs and slides of the eyes of Monotremes and Marsupialswhich are unobtainable outside Australia ; while in this Institute Professor NormanAshton and Dr. Katharine Tansley have provided me with sections and photographsof the eyes of a number of animals.
In several instances my knowledge of zoology has been brought up to dateby the great kindness of Dr. Mary Whitear of the Zoology Department of UniversityCollege, London, who has read the proofs of those sections dealing with zoologicalclassification ; while Dr. Katharine Tansley and Dr. Robert Weale of this Institutehave given me most helpful criticism in some aspects of the visual problems discussed.Miss M. H. T. Yuille, Mr. A. J. B. Goldsmith and my wife have shared with me theonerous task of proof-reading.
It is difficult for me to express my indebtedness to my secretary. Miss RosamundSoley, who has borne much of the burden of the technical aspects of the production ofthis Volume. She has typed and iDrejDared the manuscript, corrected the proofs, andundertaken the immense and somewhat thankless task of verifying the bibliographies,prepared the Zoological Glossary and the Index, and drawn the 350 marginal sketches.
Finally, my indebtedness to my publishei's, Henry Kimpton, continues to beimmense. They have assisted me in every possible way. Why Mr. G. E. Deed con-tinues to put up with my inoods and vagaries after thirty years is to me quiteincomprehensible.
Stewart Duke -Elder.
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CONTENTS
VOLUME I
THE EYE IN EVOLUTION
Part I. The Effect of Light on Living Organisms
Chapter I
Introduction
The Scope of the Subject
The Responses of Organisms to Light Photosynthesis
Chapter II
The Effect of Light on Metabolism : Photoperiodism
MetaboHc Effects of Light .Photoperiodism in Plants
Photoperiodism in Animals .(a) Metabolic Activities .
(b) Sexual Cycle of Animals(c) Pigment Migration .(d) Bioluminescence
(e) Time-memory of Insects and Birds
7
9
13
13
16
19
21
22
Chapter III
The Effect of Light on Movement
Historical DevelopmentTypes of Motorial Responses
(a) Photokinesis
(i) Orthokinesis
(ii) Klinokinesis
(b) Phototropism .(c) Phototaxis
(i)
(ii)
(iii)
(iv)
(V)
(vi)
Klinotaxis
Tropotaxis
Telotaxis
Scototaxis
Menotaxis
Light-compass Reaction, 61 ; Navigational Sense in Birds,
63 ; Orientation to Polarized Light, 66 ; Orientation of
Insects Out-of-doors, 67 ; Orientation to a Visual Pat-tern, 73 ; Dorsal (Ventral) Light Reaction, 74
Mnemotaxis .........
27
31
33
34
34
38
42
47
52
55
60
60
78
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CONTENTS
Chapter IV
The Effect of Light on Pigmentation
The Types of Colour ChangeMechanism of Colour Changes
Chromatophores .Types of PigmentTypes of Response
Primary, 89 ; Secondary, 91 ; Indirect, 92
Central Organization of Pigmentary Changes, Nervous and Hormonal
Chapter VThe Emergence of Vision
Light-sensitiveness, the Light Sense and Vision ....
PAGE
82
85
85
87
89
92
102
Part II. The Evolution o! the Visual Apparatus
Chapter VI
The Morphology of Invertebrate Eyes
I. The Genesis of the Eye ....Dermal Photosensitivity.Specific Light-sensitive Cells .
Pigments .....Melanin, 118 ; Visual Pigments, 118 Ommochromes, 122
II. The Structure of Invertebrate Eyes1. Eye-spots : Stigmata
2. Light-sensitive Cells .
3. The Simple Eye(a) The Unicellular Eye .(6) The Multicellular Simple Eye
(i) The Subepithelial Eye(ii) The Epithelial Invaginated Eye
The Flat Eye, 136; the Cupulate Eye, 137; theVesicular Eye, 141
(iii) The Inverted Retina(c) Aggregate Eyes .....(d) Composite Ocelli .....
4. The Compound Eye ......(a) The Development of Ocelli and Compound Eyes(6) The Structure of the Compound Eye .
The Simple Ommatidial Eye, 159 ; the Composite Compound Eye, 160
(i) The Compound Eyes of Arachnids(ii) The Compound Eyes of Crustaceans
(iii) The Compound Eyes of Insects(c) The Optical System of the Compound Eye
The Appositional Eye, 173 ; the Superpositional Eye,174 ; the Analysis of Polarized Light, 174
113
114
115
117
126
125
127
129
130
132
132
135
146
151
152
154
156
157
160
163
166
170
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CONTENTS XI
Chapteb VII
The Systematic Anatomy of Invertebrate Eyes
The Structural Variability of Invertebrate Eyes
I. Protozoa ....II. Parazoa (Porifera : Sponges)
III. Invertebrate Metazoa .1. Coelenterata
(a) Cnidaria .
Hydrozoa ; Scyphozoa ; Anthozoa(b) Acnidaria : Ctenophora
2. Echinodermata .....Holothuroidea, 184 ; Echinoidea, 185 ; Asteroidea, 185
3. Worms ....(a) Unsegmented Worms
(i) Platyhelminthes
Turbellaria, 188 ; Trematoda, 189 ; Cestoda, 189
(ii) Nemertea(iii) Nematoda
(6) Segmented Worms : Annelida(i) Oligochpeta .
(ii) Polycheeta
(iii) Archiannelida
(iv) Hirudinea : Leeches
4. Chgetognatha : Arrow-worms6. Rotifera .
6. Polyzoa : Bryozoa
7. Brachiopoda : Lamp Shells8. Mollusca ...
(a) Placophora
(b) Solenogastres .
(c) Seaphopoda
(d) Gastropoda
(e) Lamellibranchiata
(/) Cephalopoda
9. Arthropoda
(a) Onychophora .Crustacea
.
MyriapodaArachnida
Scorpionidea, 211 ; Xiphosura, 212 ; Araneida, 213
Pseudoscorpionidea, 214 ; Pedipalpi, 214 ; Phalangida
215 ; Solifugae, 216 ; Acarina, 216 ; Pycnogonida, 21'
Insecta .......(i) The Stemmata of Larval or Pupal Forms
(ii) The Dorsal Ocelli of Adults .(iii) The Compound Eyes of Adults
(b)
(c)
(d)
{e)
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180
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186
187
188
189
190
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196
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217
222
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Chapter VIII
The Eyes of Proto-chordates
1. Hemichordata .......2. Tunicata : Urochordata......3. Cephalochordata : Lancelots .....
227
228
228
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Xll CONTENTS
Chapter IX
The Evolution of the Vertebrate Eye
The Vertebrate Phylum .....1
.
The Phylogeny of the Vertebrate Eye2. The Ontogeny of the Vertebrate Eye3. The Emergence of the Vertebrate Eye4. The General Structm-e of the Vertebrate Eye
PAGE
233
237
239
242
248
Chapter XThe Eyes of Cyclostomes
The Class of Cyclostomes1. The Ammoccete Eye
Light-sensitive Cells
2. The Lamprey Eye .
259
261
263
263
Chapter XI
The Eyes of Fishes
General Configviration of the Eye
.
The Class of FishesL The Selachian Eye .2. The Holocephalian Eye3. The Teleostean Eye4. The Dipnoan Eye5. The Coelacanth Eye6. The Chondrostean Eye7. The Holostean EyeAnomalies in the Eyes of Fishes
(a) The Tubular (Telescopic) Eye
(6) The Amphibious Eye(c) Stalked Eyes .(d) The Migratory Eye .
273
278
279
290
291
312
314
315
321
322
322
324
326
328
Chapter XII
The Eyes of Amphibians
The Class of AmphibiansGeneral Configuration of the Eye.
1. The Anuran Eye2. The Urodelan Eye .
333
334
334
346
Chapter XIII
The Eyes of Reptiles
The Class of Reptiles .General Configuration of the Eye
1. The Lacertilian Eye2. The Chelonian Eye .3. The Crocodilian Eye4. The Rhynchocephalian Eye5. The Ophidian V.ye .
353
353
355
368
375
379
383
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CONTENTS Xlll
Chapter XIV
The Eyes of Birds
The Class of BirdsGeneral Configuration of the Eye.
The Avian Eye
397
401
401
Chapter XVThe Eyes of ]\Iam>iaxs
The Class of Mammals1. The Monotreme Eye2. The Marsupial Eye .
The Sub-class of Placentals3. The Placental Eye .
Aquatic Adaptations
429
431
437
441
446
501
Chapter XVI
The Central Organization of Vision
General Principles
II.
The Nervous Control1. The Nerve-net2. Trunk-pathways3. The Ganglionic Nervous System
(a) The Nervous System of Worms(6) The Nervous System of Arthropods
.
(c) The Nervous System of Molluscs4. The Central Nervous System of Vertebrates
Hind-brain, 533 ; Mid-brain, 534 ; Diencephalon, 537
mus, 538 ; Telencephalon, 542
Evolution of the Visual Pathways and Centres
The Hormonal Control ......Hormones and Neuro -secretory Cells
(a) The Neuro-endocrme System of Crustaceans(b) The Neuro -endocrine System of Insects(c) The Neuro -endocrine System of Vertebrates
Optic Thala-
509
511
614
616
617
518
521
527
530
543
647
550
552
555
556
Part III. The Function of the Eyes of Animals
Chapter XVII
The Vision of Invertebrates
Methods of Investigation .....1. The Reactions of the Lower Invertebrates to Light
(a) Protozoa .....(b) Coelenterata.....(c) Echinodermata ....
567
670
570
571
571
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XIV CONTENTS
2. The Vision of Worms ....(a) Unsegmented Worms(6) Segmented Worms
3. The Vision of Molluscs ....(a) Gastropods and Lamellibranchs
(6) Cephalopods
4. The Vision of Arthropods(a) Onychophora
(6) Myriapods
(c) Crustaceans
(d) Arachnids
5. The Vision of Insects(a) The Larvse of Insects ....(b) The Dorsal Ocelli of Adults .(c) The Compound Eyes of Insects
(i) Behavioural Experiments(ii) Electro-physiological Characteristics
(iii) Spectral Sensitivity
(iv) Discrimination of Luminosity-differences
(v) Perception of Colour .
(vi) Perception of Form .(vii) Perception of Distance
(viii) Spatial Appreciation and LocalizationAccommodation in Invertebrates
PAGE572
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578
578
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681
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582
683
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588
589
589
590
Chapter XVIII
The Vision of Vertebrates
The Role of Vision in Vertebrate Life(a) Cyclostomes
(b) Fishes
(c) Amphibians{d) Reptiles
(e) Birds
(/) Mammals
I. The Perception of Light1. The Nocturnal Eye
(a) The Optical SystemThe Tapetum Lucidum
(b) The Organization of the Retina2. The Diurnal Eye ....3. The Arhythmic Eye
(a) Contractile Pupils
(6) Occlusible Tapeta .(c) Photo -mechanical Changes in the Retina(rf) The Static Organization of the Retina
4. Absolute Sensitivity to Light .
6. Discriminati of Variations in Intensity .
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698
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599
600
600
602
605
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606
609
611
612
612
612
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617
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CONTENTS XV
PAGEII. The Perception of Colour ......... 619
Objective Methods of Investigation ...... 621Subjective Methods of Investigation ...... 623
1. The Colour Vision of Cyclostomes ....... 6242. The Colour Vision of Fishes 6243. The Colour Vision of Amphibians ....... 6274. The Colour Vision of Reptiles ....... 6286, The Colour Vision of Birds 6296. The Colour Vision of Mammals ....... 632
III. The Perception of Form ......... 6371. Optical Factors 638
(a) The Refraction of Vertebrates ...... 638(6) Accommodation in Vertebrates ...... 640
(i) Static Devices ........ 640Stenopoeic Pupil, 641 ; Duplicated Optical System,
641 ; Interposition of Nictitating Membrane, 643 ;Duplicated Retina, 643 ; Ramp-retina, 643 ; Cor-
rugated Retina, 643 ; Length of Receptor Elements,643
(ii) DjTiamic Devices ....... 644(a) Movement of Lens as a ^^^^ole .... 644
Backward Movement, 644 ; Forward Movement,647
(^) Deformation of Lens ...... 649By Direct Ciliary Pressure, 649 ; by Capsular
Elasticity, 652
(iii) Accommodation in Amphibious Vertebrates . . . 654(c) Other Optical Factors determining Visual Acuity . . . 655
2. The Structure of the Retina 656(a) The Area Centralis ........ 657(b) The Fovea 658(c) The Degree of Summation ....... 659
3. The Visual Acuity of Vertebrates ....... 660(a) The Visual Acuity of Fishes 660(b) The Visual Acuity of Amphibians . . . . . .661(c) The Visual Acuity of Reptiles . ...... 661(d) The Visual Acuity of Birds 662(e) The Visual Acuity of Mammals ...... 663
rV. The Perception of Space1. The Visual Fields of Vertebrates
(a) The Uniocular Field
(6) The Binocular FieldCyclostomes, 678 ; Fishes, 678
682 ; Birds, 684 ; Mammals,2. The Ocular Movements .
(a) Involuntary Ocular Movements
(6) Voluntary Ocular MovementsFishes, 693 ; Amphibians, 694
Mammals, 696
Amphibians, 682
687
Reptiles,
666
669
669
672
689
690
692Reptiles, 694 ; Birds, 695
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XVI CONTENTS
The Perception of Space
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contd. page
3. Uniocular and Binocular Vision ....... 697Spatial Judgments . . . . . . . . .700
Fishes, 701 ; Amphibians and Reptiles, 702 ; Birds, 702 ;Manmials, 704
V. The Perception of Movement . . . . . . . .705
Part IV. Evolutionary By-ways
Chapter XIXMedian Eyes
1. Pineal and Parietal Organs . . . . . . . .. 711Cyclostomes, 713 ; Fishes, 713 ; Amphibians, 714 ; Reptiles, 715
(a) The Median Eye of the Lamprey . . . . . .716(6) The Median Eyes of Lizards and /S^/ienorfon . . . . .716
2. The Function of the Pineal and Parietal Organs . . . . .718
Chapter XXRudimentary Eyes
Habit and Regression . . . . . . . . . .7211. The Sedentary Habit 722
Molluscs, 722 ; Crustaceans, 722
2. The Abyssal Habit 722Molluscs, 723 ; Crustaceans, 723 ; Fishes, 723
3. The Cavernicolous or Limicoline Habit . . . . . .724Invertebrates, 724 ; Cave-fishes, 725 ; Amphibians, 726
4. The Fossorial or Burrowing Habit . . . . . . .728Invertebrates, 728 ; Amphibians, 730 ; Reptiles, 731 ; Mammals, 733
5. The Parasitic Habit 733Invertebrates, 733 ; Cyclostomes, 734 ; Fishes, 734
Chapter XXILuminous Organs
Bioluminescence .....1. The Occurrence of Bioluminescence .
The Biological Purpose of Bioluminescence2. The Biological Mechanism of Bioluminescence
Extracellular Bioluminescence
Intracellular Production of Bioluminescence
3. The Chemical Mechanism of Bioluminescence
736
737
741
744
745
746
747
Chapter XXII
Electric Organs
The Electric Organs of Fishes : Astroscopus
EPILOGUEAPPENDIX. Pala^ontological Table .Zoological Glossary ....Index ......
751
753
754
756
779
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PART I
THE EFFECT OF LIGHT ON LIVING ORGANISMS
Introduction
The Effect of Light on Metabolism
The Effect of Light on Movement
The Effect of Light on Pigmentation
The Emergence of Vision
S.O.—VOL. I.
SO_DE_V1_P1_C1.pdfSO_DE_V1_P1_C2.pdfSO_DE_V1_P1_C3.pdfSO_DE_V1_P1_C4.pdfSO_DE_V1_P1_C5.pdf
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PART II
THE EVOLUTION OF THE VISUAL APPARATUS
The Morphology of Invertebrate Eyes
The Systematic Anatomy of Invertebrate Eyes
The Eyes of Protochordates
The Evolution of the Vertebrate Eye
The Eyes of Cyclostomes
The Eyes of Fishes
The Eyes of Amphibians
The Eyes of Reptiles
The Eyes of Birds
The Eyes of Mammals
The Central Organization of Vision
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PART III
THE FUNCTION OF THE EYES OF ANIMALS
The Vision of Invertebrates
The Vision of Vertebrates
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PART IV
EVOLUTIONARY BY-WAYS
Median Eyes
Rudimentary Eyes
Luminous Organs
Electric Organs
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PortadaEsquema "System Ophthalmology"PrefacioReconocimientosContenidoParte I. Efectos de la Luz en los Organismos vivos1.- Introducción2.- Efectos de la luz en el metabolismo: FOTOPERIODISMO3.- Efectos de la luz en el Movimiento4.- Efectos de la luz en la Pigmentación5.- Aparición de la Visión
Parte II. La evolución del Aparato Visual 6.- La morfología del ojo de los Invertebrados 7.- Anatomía Sistemática del Ojo de los Invertebrados8.- El Ojo de los Protocordados 9.- Evolución del Ojo de los Vertebrados10.- El Ojo de los Ciclóstomos11.- El ojo de los Peces12.- El Ojo de los Anfibios13.- El Ojo de los Reptiles14.- El Ojo de los Pájaros15.- El Ojo de los Mamíferos16.- Organización Central de la Visión
Parte III. La función de los Ojos en los Animales17.- La Visión de los Invertebrados18.- La Visión de los Vertebrados
Parte IV. Otros Caminos Evolutivos19.- Ojo Medial20.- Ojos Rudimentarios21.- Órganos Luminosos22.- Órganos Eléctricos
EpílogoApéndiceGlosario de ZoologíaÍndice