Photochemistry of Vision

840 Pages·1972·23.9 MB·English

by  J., E. W. Abrahamson, Ch. Baumann, C. D. B. Bridges, F. Crescitelli, H. J. A. Dartnall, R. M. Eakin, G. Falk, P. Fatt, T. H. Goldsmith, R. Hara, T. Hara, S. M. Japar, P. A. Liebman, J. N. Lythgoe, R. A. Morton, W. R. A. Muntz, W. A. H. Rushton, T. I. Shaw

Handbook
of
Sensory Physiology
Volume VII / 1
Editorial Board
H. Autrum . R. Jung . W. R. Loewenstein
D. M. MacKay· H. 1. Teuber
Photochemistry
of Vision
By
E. W. Abrahamson' Ch. Baumann' C. D. B. Bridges
F. Crescitelli . R. J. A. Dartnall . R. M. Eakin
G. Falk . P. Fatt . T. R. Goldsmith· R. Rara
T. Rara . S. M. Japar . P. A. Liebman' J. N. Lythgoe
R. A. Morton' W. R. A. Muntz· W. A. R. Rushton
T. I. Shaw' J. R. Wiesenfeld . T. Yoshizawa
Edited by
Herbert J. A. Dartnall
With 296 Figures
Springer-Verlag Berlin· Heidelberg· New York 1972
ISBN-13: 978-3-642-65068-0 e-ISBN-13: 978-3-642-65066-6
001: 10.1007/978-3-642-65066-6
This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned,
specifically those of translation, reprinting, re-use of illustrations, broadcasting, reproduction by photocopying
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Under § 54 of the German Copyright Law where copies are made for other than private use, a fee is payable to
the publisher, the amount of the fee to be determined by agreement with the publisher. © by Springer-Verlag,
Berlin' Heidelberg 1972. Library of Congress Catalog Card Number 71-182440.
Softcover reprint of the hardcover 1st edition 1972
The use of general descriptive names, trade names, trade marks, etc. in this publication, even if the former are
not especially identified, is not to be taken as a sign that such names, as understood by the Trade Marks and
Merchandise Marks Act, may accordingly be used freely by anyone_
Preface
Radiation can only affect matter if absorbed by it. Within the broad range of
300-1000 nm, which we call "the visible", light quanta are energetic enough to
produce excited electronic states in the atoms and molecules that absorb them. In
these states the molecules may have quite different properties from those in their
dormant condition, and reactions that would not otherwise occur become possible.
About 80 % of the radiant energy emitted by our sun lies in this fertile band,
and so long as the sun's surface temperature is maintained at about 6000° C this
state of affairs will continue. This and the transparency of our atmosphere and
waters have allowed the generation and evolution of life. Before life began the
atmosphere probably also transmitted much of the solar short-wave radiation, but
with the rise of vegetation a new product - oxygen - appeared and this, by a
photochemical reaction in the upper atmosphere, led to the ozone layer that now
protects us from the energetic "short-wave" quanta that once, perhaps, took part
in the generation of life-molecules.
Light is an ideal sensory stimulus. It travels in straight lines at great speed
and, consequently, can be made to form an image from which an animal can make
"true", continuous and immediate assessments of present and impending events.
It is no surprise then that the visual sense is found in nearly every division of the
animal kingdom - from the hawk to the jumping spider, from man to blow-fly
maggot, from the octopus to the rotifer.
In the visual apparatus an image of the environment is focused by the eye on
a sensitive surface made up of photoreceptive cells - the rods and cones of
vertebrates, and the retinulae of invertebrates. These cells contain photosensitive
pigments whose prime function is to absorb light. The spectral regions visible to
an animal are, indeed, determined by the light.absorbing properties of its visual
pigments. Some insects, for example, are equipped with an ultraviolet-absorbing
visual pigment by which they see honey-guide markings in certain flowers that
to us seem of a uniform hue. Fishes of freshwaters having light climates biased
towards the red, possess pigments absorbing in that spectral region. Deep-sea
fishes, on the other hand, have blue-sensitive visual pigments, thus making good
use of the dim, slim band of solar radiation that filters down to them. Some animals
change their visual pigments on changing their habitat, as the amphibia do when
they metamorphose to live on land, and as the migratory fishes do when they
switch from the river to the sea, or vice versa, on their spawning runs. Changes in
visual pigments can even occur in some sedentary species of freshwater fishes,
presumably in response to seasonal variation in their light environment.
In spite of these differing situations, severally calling for visual sensitivity to
any part of the spectrum from the near ultraviolet to the near infrared, all known
visual pigments are built to a common molecular pattern. Whether derived from
vertebrates or invertebrates, they are photosensitive chromoproteins consisting
of a chromophoric group, based on vitamin A, that is intimately joined to one of
a family of proteins called opsins. Moreover, so far as is known, the chromophoric
group is always in the ll-cis conformation, and the photochemical change that
VI Preface
occurs on absorption of a photon is the mere isomerisation of this group from the
cis to the trans form. But the consequences of this simple change are momentous.
Released in this way from the embrace of its chromophoric group, the protein
moiety relaxes to expose the hitherto concealed active groups. These initiate in
the visual cells the electrical changes that are transmitted to the higher visual
centres.
The theme of this volume - The Photochemistry of Vision - has been inter-
preted in a catholic sense, and the Contributors come from many different disciplines.
A substantial part of the account is, indeed, directly concerned with the chemistry
and photochemistry of the visual pigments. - What is the nature of the linkage
between chromophoric group and opsin?: - How can such a variety of light-
absorptive properties be reconciled with such apparently homogeneous chemical
and photochemical properties? : - What is the nature of the photochemical change
and what is its quantum efficiency?: - How many stages are there in the cascade
of thermal reactions that follows the photochemical event - and which of them is
the visual trigger?: - How do these reactions differ in vertebrates and inverte-
brates - and why?: - How is the visual pigment molecule reconstituted after
bleaching? 'The answers to these and many other questions are attempted.
But in addition to this photochemical approach the subject is also treated on
the broader basis of photobiology. A description of the visual pigments and of the
cells containing them is given for the whole animal kingdom from invertebrates to
vertebrates, and treated from both taxonomic and ecological standpoints. Here
the reader will find attempts to answer such questions as - What is the ancestral
photoreceptor?: - How long does it take for a species to evolve a new visual
pigment? : - Can a visual pigment help to decide an animal's taxonomic position?
Supporting data for the ecological approach is provided by descriptions of the
light climate in such diverse situations as the open land at sea-level, underneath a
canopy of vegetation, below the surface in rivers, lakes, estuaries and coastal
waters, and at various depths of the open seas. Peripheral data relevant to the
quality of light reaching the visual pigments, namely, the optical properties of oil
droplets and other pre-retinal media, and of tapeta, are given and, likewise, the
spectral qualities of bioluminescence - frequently more intense than the attenuated
light of the sun at quite moderate depths in murky coastal waters, and the only
source of light in the abyssal depths of the oceans.
The study of visual pigments prepared by extractive procedures has provided
much information about the scotopic pigments but has not been very successful
with cone pigments. Here the methods of retinal densitometry and, more recently,
of microspectrophotometry have helped to provide some of the missing information.
Apart from the satisfaction of bringing together such a diverse assortment of
material, this volume has been produced with two main objects: to seduce the
honours graduate into a study of vision, and to provide a source book for the
research worker. With the latter in mind, the contributors have not hesitated to
quote their unpublished material, to speculate, and to draw attention to neglected
areas that could be fruitful. These parts of the text are duly logged in the subject
index under "Problems, unsolved".
Falmer, November, 1971 H. J. A. DARTNALL
Contents
Chapter 1 Principles of the Interaction of Light and Matter.
By E. W. ABRAHAMSON and S. M. JAPAR.
With 15 Figures ......... . 1
Chapter 2 The Chemistry of the Visual Pigments.
By R. A. MORTON. With 12 Figures ....... 33
Chapter 3 The Structure, Spectra, and Reactivity of Visual
Pigments. By E. W. ABRAHAMSON and J. R. WIESEN-
FELD. With 18 Figures . . . . . . . . . . . . . . 69
Chapter 4 Photosensitivity. By H. J. A. DARTNALL.
With 8 Figures ................. 122
Chapter 5 The Behaviour of Visual Pigments at Low Temperatures.
By T. YOSHIZAWA. With 19 Figures ........ 146
Chapter 6 The Circular Dichroism and Optical Rotatory
Dispersion of Visual Pigments. By T. 1. SHAW.
With 6 Figures ............. . 180
Chapter 7 Physical Changes Induced by Light in the Rod Outer
Segment of Vertebrates. By G. FALK and P. FATT.
With 3 Figures ................. 200
Chapter 8 The Visual Cells and Visual Pigments of the Vertebrate
Eye. By F. CRESCITELLI. With 30 Figures .... 245
Chapter 9 Visual Pigments in Man. By W. A. H. RUSHTON.
With 12 Figures . . . . . . . . . . . . . . . 364
Chapter lO The Regeneration and Renewal of Visual Pigment in
Vertebrates. By CH. BAUMANN. With 5 Figures. 395
Chapter 11 The Rhodopsin-Porphyropsin Visual System.
By C. D. B. BRIDGES. With 37 Figures . . 417
Chapter 12 Microspectrophotometry of Photoreceptors.
By P. A. LIEBMAN. With 14 Figures . . 481
Chapter 13 Inert Absorbing and Reflecting Pigments.
By W. R. A. MUNTZ. With 16 Figures 529
Chapter 14 The Adaptation of Visual Pigments to the Photic
Environment. By J. N. LYTHGOE. With 18 Figures . . 566
Chapter 15 List of Vertebrate Visual Pigments. By J. N. LYTHGOE 604
Chapter 16 Structure of Invertebrate Photoreceptors.
By R. M. EAKIN. With 59 Figures ......... 625
Chapter 17 The Natural History of Invertebrate Visual Pigments.
By T. H. GOLDSMITH. With 9 Figures ........ 685
Chapter 18 Cephalopod Retinochrome. By T. HARA and R. HARA.
With 15 Figures 720
Author Index 747
Subject Index 771
Acknowledgments
Many of the illustrations in this volume have been reproduced from the
Literature. Where practicable the permissions of the Authors have been obtained,
and also of the Editors and/or Proprietors of the relevant Journals and Books.
Acknowledgment to the authors is given in each figure or table caption, and the
reference lists at the end of each Chapter give the full titles and particulars of the
sources. In addition, the following formal acknowledgments are made.
Journals
Vision Research (Pergamon Press Ltd.);
Figs. 7, 8 and Table 1, Chapter 4; Fig. 3, Chapter 6; Figs. 2, 3, Chapter 9; Figs. 5-8, 14,
22-33,36 and Tables 1,6-8, Chapter 11; Figs. 5, 11, Chapter 12; Figs. 2, 4, Chapter 13;
Figs. 14, 16, 18, Chapter 14.
Nature, London (Macmillan Journals Ltd.);
Fig. 3, Chapter 2; Fig. 3, Chapter 3; Figs. 5, 7, 9, 18, 19 and Table 1, Chapter 5; Fig. 4,
Chapter 6; Fig. 6, Chapter 9; Fig. 4, Chapter 10; Figs. 19,35, Chapter 11; Figs. 54, 55,
Chapter 16; Figs. 1, 5, 7, 9-14, Chapter 18
Zeitschrift fUr Zelliorschung und mikroskopische Anatomie (Springer Verlag);
Figs. 4, 23, 27, 28, 30, 36, 38-40, 46---49, 51, 53, Chapter 16
Publications of the American Chemical Society;
1. Biochemistry
Figs. 4-8, 15-17, Chapter 3; Fig. 2, Chapter 11
2. Journal of the American Chemical Society
Fig. 10, Chapter 1; Figs. 5-7, Chapter 2; Fig. 6, Chapter 6
3. Analytical Chemistry
Fig. 9, Chapter 1
Journal of Ultrastructure Research (Academic Press Inc.);
Fig. 2, Chapter 8; Figs. 8, 29, 31, 41, 45, 52, 57, 58, Chapter 16
Journal of the Optical Society of America (American Institute of Physics);
Fig. 3, Chapter 12; Figs. 1, 2, 6, 11 and Table 2, Chapter 14
Journal of General Physiology (The Rockefeller Institute Press);
Fig. 23, Chapter 8; Figs. 1-3, Chapter 10; Fig. 1, Chapter 17
Proceedings of the National Academy of Sciences of the U.S.A. (National Academy of Sciences,
Washington) ;
Figs. 1,2,5, Chapter 6; Fig. 5, Chapter 16
Journal of Physiology (The Physiological Society, published by Cambridge University Press);
Fig. 2, Chapter 7; Figs. 4, 5, 10, Chapter 9
Photochemistry and Photobiology (Pergamon Press Ltd.);
Fig. 13, Chapter 3; Figs. 9, 11, 12, Chapter 9
Journal of Cell Biology (The Rockefeller University Press);
Figs. 10, 18, 33, Chapter 16
Acknowledgments IX
Quarterly Journal of Microscopical Science (The Company of Biolog ists Ltd.):
Figs. 9, 20, 50, Chapter 16
Journal of Cellular and Comparative Physiology (The Wistar Institute of Anatomy and
Biology):
Figs. 24-26, Chapter 16
Canadian Journal of Zoology (National Research Council of Canada, Ottawa):
Figs. 16-18, Chapter II
Biochemical Journal (Cambridge University Press):
Figs I, 2, 4, Chapter 2
Helvetica Chimica Acta:
Fig. 8 and Tables 3, 4, Chapter 2
Zeitschrift fUr Vergleichende Physiologie (Springer-Verlag):
Figs. 3, 5, 6, Chapter 17
Bulletin of the Johns Hopkins Hospital:
Figs. 9, 10, Chapter 3 and Fig. 19, Chapter 16 (from H. V. Zonana's article "Fine structure
of the Squid Retina" in Vol. 109, Number 5 (1961) pages 185-205. © The Johns Hopkins
Press)
Annals of the New York Academy of Sciences:
Figs. 7, 8, Chapter 9
Acta Zoologica:
Figs. 7, 8, Chapter 8
Protistologica (Centre Nationale de la Recherche Scientifique, Paris):
Figs. 43, 56, Chapter 16
Journal of Cell Science (Cambridge University Press):
Figs. 2, 3, Chapter 16
Japanese Journal of Ophthalmology (University of Tokyo):
Fig. 6, Chapter 18
Biochimica et Biophysica Acta (Elsevier):
Table 2, Chapter 3
Progress in Biophysics and Molecular Biology (Pergamon Press Ltd.):
Table 7, Chapter 3
Archiv fiir Mikrobiologie (Springer-Verlag):
Fig. II, Chapter 16
Experimental Cell Research (International Society for Cell Biology: Academic Press Inc.):
Fig. 6, Chapter 13
Journal of Experimental Biology (Cambridge University Press):
Fig. 9, Chapter 17
British Medical Bulletin (Medical Department, The British Council) :
Fig. 1, Chapter II
Advances in Electronics and Electron Physics (Academic Press Inc.):
Fig. 3, Chapter 14
Ecology:
Fig. 5, Chapter 14
x Acknowledgments
Journal of the Marine Biological Association (U.K.) (Cambridge University Press):
Fig. 9, Chapter 14
Izvestiya Akadamii nauk SSSR (Geofiz.), Leningrad:
Fig. 12, Chapter 14
Compte Rendu de l'Academie des Sciences (Institut de France, Academie des Sciences):
Fig. 7, Chapter 16
Science (American Association for the Advancement of Science):
Fig. 12, Chapter 2
Optica Acta:
Fig. 5, Chapter 10
Books
Comprehensive Biochemistry (Eds. FLORKIN,M. and STOTZ,E.H.). Vol. 27, Photobiology,
Ionizing Radiations. Amsterdam-London-New York: Elsevier 1965.
(Fig. 9, Chapter 2; Fig. 3, Chapter 11 from article by BRIDGES,C.D.B. entitled "Bio-
chemistry of Visual Processes")
The Visual Pigments by DARTNALL,H.J.A. London: Methuen and Co. Ltd, New York: John
Wiley & Sons Inc. 1957.
(Fig. 1, Chapter 4)
The Functional Organization of the Compound Eye (Ed. BERNHARD,C.G.). Symposium
Publications Division, Oxford-London-Edinburgh-New York-Toronto-Sydney-Paris-Braun-
schweig: Pergamon Press 1966.
(Fig. 22, Chapter 16, from article by EGUCHI, E. and WATERMAN, T. H. entitled "Fine
Structure Patterns in Crustacean Rhabdoms"; Figs. 2, 7, Chapter 17, from article by
GOLDSMITH, T.H. and FERNANDEZ,H.R. entitled "Some Photochemical and Physiological
Aspects of Visual Excitation in Compound Eyes")
Fundamentals of Limnology by RUTTNER,R. (Trans. FREy,D.G. and F.E.J.). Toronto:
University of Toronto Press, 1953.
(Fig. 10, Chapter 11)
Evolutionary Biology, Vol. II (Eds. DOBZHANSKY,T., HECHT,M.K., STEERE,W.C.). New
York: Appleton-Century-Crofts 1968.
(Fig. 37, Chapter 16, from article by EAKIN,R.M. entitled "Evolution of Photoreceptors").
Molecular Bases of Biological Functions (Biophysics, Vol. 6). Kyoto: Yoshioka 1965.
(Fig. 4, Chapter 18, from article by HARA, T. entitled "Vision and Rhodopsin")
Visual Problems of Colour, Vol. 1. National Physical Laboratory Symposium No.8. London:
Her Majesty's Stationery Office, 1958.
(Figs. 4 and 5, Chapter 4)
The Vertebrate Eye and its Adaptive Radiation by WALLS, G. L. New York-London: Hafner
Publishing Co. 1963.
(Fig. 5, Chapter 13)
Color Science: Concepts and Methods, Quantitative Data and Formulas by WYSZECKI,G. and
STILES, W.S. New York-London-Sydney: John Wiley & Sons, Inc. 1967.
(Table 1, Chapter 4; Fig. 14, Chapter 13)
Optical Oceanography by JERLOv,N.G. Amsterdam-London-Ncw York: Elsevier 1968.
(Figs. 7, 8, 10 and Table 4, Chapter 14)
Acknowledgments XI
The Retina. Morphology, Function and Clinical Characteristics (Eds. STRAATSMA,B.R., HALL,
M.O., ALLEN,R.A., CRESCITELLI,F.), U.C.L.A. Forum in Medical Sciences No.8. Berkeley
and Los Angeles: University of California Press 1969.
(Figs. 1, 2, Chapter 3, from article by COHEN,A.I. entitled "Rods, Cones and Visual
Excitation". Permission to reprint granted by The Regents of the University of California)
Cold Spring Harbor Symposia on Quantitative Biology, Vol. 30. Published by The Long Island
Biological Association, New York, 1965.
(Fig. 10, Chapter 2, from article by WALD,G. and BROWN,P.K. entitled "Human Vision
and Colour Blindness": Figs. 12,20 and Table 5 from article by BRIDGES,C.D.E. entitled
"Absorption Properties, Interconversions and Environmental Adaptation of Pigments
from Fish Photoreceptors")
Advances in Comparative Physiology, Vol. 1. (Ed. LOWENSTEIN,O.). Academic Press Inc.,
1962.
(Fig. 4, Chapter 14, from article by NrcoL,J.A. C. entitled "Animal Luminescence",
pp. 217-273)
Persons
The following persons have kindly donated original material or supplied unpublished
information used as indicated.
R. DUNN From Ph. D. Thesis, University of California, Los Angeles (1965) entitled
"Electron Microscopy Studies on the Photoreceptor Cells of the Gecko,
Coleonyx variegatu8."
(Fig. 18, Chapter 8)
J. M. CULLEN (Fig. 10 and Table 3, Chapter 13)
P. E. KING-SMITH (Fig. 12, Chapter 13)
R. NISmOKA (Fig. 35, Chapter 16)
C. GREUET (Fig. 42, Chapter 16)
Editor's Acknowledgments
I record my appreciation of the support given and forbearance shown to me
by the Contributors - of the cheerful industry of my secretary, Mrs Patricia
Chatfield - and of the courtesy and uncomplaining efficiency of the Staff of
Springer-Verlag.
H. J. A. DARTNALL