Photochemistry of Vision PDF
Preview Photochemistry of Vision
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 machine or similar means, and storage in data banks. 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
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