Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-27T21:10:52.231Z Has data issue: false hasContentIssue false

Why different regions of the retina have different spectral sensitivities: A review of mechanisms and functional significance of intraretinal variability in spectral sensitivity in vertebrates

Published online by Cambridge University Press:  09 June 2011

S. E. TEMPLE*
Affiliation:
Sensory Neurobiology Group, School of Biomedical Sciences, The University of Queensland, St. Lucia, Queensland, Australia Ecology of Vision Laboratory, School of Biological Sciences, The University of Bristol, Bristol, UK
*
*Address correspondence and reprint requests to: S.E. Temple, Ecology of Vision Laboratory, School of Biological Sciences, The University of Bristol, Woodland Road, Bristol BS8 1UG, UK. E-mail: [email protected]

Abstract

Vision is used in nearly all aspects of animal behavior, from prey and predator detection to mate selection and parental care. However, the light environment typically is not uniform in every direction, and visual tasks may be specific to particular parts of an animal’s field of view. These spatial differences may explain the presence of several adaptations in the eyes of vertebrates that alter spectral sensitivity of the eye in different directions. Mechanisms that alter spectral sensitivity across the retina include (but are not limited to) variations in: corneal filters, oil droplets, macula lutea, tapeta, chromophore ratios, photoreceptor classes, and opsin expression. The resultant variations in spectral sensitivity across the retina are referred to as intraretinal variability in spectral sensitivity (IVSS). At first considered an obscure and rare phenomenon, it is becoming clear that IVSS is widespread among all vertebrates, and examples have been found from every major group. This review will describe the mechanisms mediating differences in spectral sensitivity, which are in general well understood, as well as explore the functional significance of intraretinal variability, which for the most part is unclear at best.

Type
Evolution and eye design
Copyright
Copyright © Cambridge University Press 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahnelt, P.K., Hokoc, J.N. & Rohlich, P. (1995). Photoreceptors in a primitive mammal, the South American opossum, Didelphis marsupialis aurita: Characterization with anti-opsin immunolabeling. Visual Neuroscience 12, 793804.CrossRefGoogle Scholar
Ahnelt, P.K. & Kolb, H. (2000). The mammalian photoreceptor mosaic-adaptive design. Progress in Retinal & Eye Research 19, 711777.Google Scholar
Ala-Laurila, P., Donner, K., Crouch, R.K. & Cornwall, M.C. (2007). Chromophore switch from 11-cis-dehydroretinal (A2) to 11-cis-retinal (A1) decreases dark noise in salamander red rods. The Journal of Physiology 585, 5774.CrossRefGoogle ScholarPubMed
Allison, W.T., Dann, S.G., Veldhoen, K.M. & Hawryshyn, C.W. (2006). Degeneration and regeneration of ultraviolet cone photoreceptors during development in rainbow trout. The Journal of Comparative Neurology 499, 702715.Google Scholar
Appleby, S.J. & Muntz, W.R.A. (1979). Occlusable yellow corneas in tetraodontidae. The Journal of Experimental Biology 83, 249259.CrossRefGoogle Scholar
Arnott, H.J., Maciolek, N.J. & Nicol, J.A. (1970). Retinal tapetum lucidum: A novel reflecting system in the eye of teoeosts. Science 169, 478480.Google Scholar
Arrese, C.A., Rodger, J., Beazley, L.D. & Shand, J. (2003). Topographies of retinal cone photoreceptors in two Australian marsupials. Visual Neuroscience 20, 307311.CrossRefGoogle ScholarPubMed
Arrese, C.A., Oddy, A.Y., Runham, P.B., Hart, N.S., Shand, J., Hunt, D.M. & Beazley, L.D. (2005). Cone topography and spectral sensitivity in two potentially trichromatic marsupials, the quokka (Setonix brachyurus) and quenda (Isoodon obesulus). Proceedings of the Royal Society of London. Series B, Biological Sciences 272, 791796.Google ScholarPubMed
Bailes, H.J., Robinson, S.R., Trezise, A.E. & Collin, S.P. (2006). Morphology, characterization, and distribution of retinal photoreceptors in the Australian lungfish Neoceratodus forsteri (Krefft, 1870). The Journal of Comparative Neurology 494, 381397.Google Scholar
Barlow, H.B. (1956). Retinal noise and absolute threshold. Journal of the Optical Society of America 46, 634639.Google Scholar
Beaudet, L., Browman, H.I. & Hawryshyn, C.W. (1993). Optic nerve response and retinal structure in rainbow trout of different sizes. Vision Research 33, 17391746.CrossRefGoogle ScholarPubMed
Best, A.C.G. & Nicol, J.A.C. (1980). Eyeshine in fishes. A review of ocular reflectors. Canadian Journal of Zoology 58, 945956.Google Scholar
Bone, R.A. (1980). The role of the macular pigment in the detection of polarized light. Vision Research 20, 213220.Google Scholar
Bone, R.A., Landrum, J.T. & Tarsis, S.L. (1985). Preliminary identification of the human macular pigment. Vision Research 25, 15311535.CrossRefGoogle ScholarPubMed
Boulton, M., Docchio, F., Dayhawbarker, P., Ramponi, R. & Cubeddu, R. (1990). Age-related changes in the morphology, absorption and fluorescence of melanosomes and lipofuscin granules of the retinal pigment epithelium. Vision Research 30, 12911303.Google Scholar
Bowmaker, J.K. (1977). The visual pigments, oil droplets and spectral sensitivity of the pigeon. Vision Research 17, 11291138.CrossRefGoogle ScholarPubMed
Bowmaker, J.K. (1991). The evolution of vertebrate visual pigments and photoreceptors. In Evolution of the Eye and Visual System, Vol. 2, ed. Cronly-Dillon, J.R. & Gregory, R.L., pp. 6381. Boca Raton, FL: CRC Press, Inc.Google Scholar
Bowmaker, J.K. (1998). Evolution of colour vision in vertebrates. Eye 12(Pt 3b), 541547.Google Scholar
Bowmaker, J.K. (2008). Evolution of vertebrate visual pigments. Vision Research 48, 20222041.CrossRefGoogle ScholarPubMed
Bowmaker, J.K. & Knowles, A. (1977). The visual pigments and oil droplets of the chicken retina. Vision Research 17, 755764.Google Scholar
Bowmaker, J.K., Loew, E.R. & Ott, M. (2005). The cone photoreceptors and visual pigments of chameleons. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 191, 925932.Google Scholar
Brenner, E., Spaan, J.P., Wortel, J.F. & Nuboer, J.F.W. (1983). Early color deprivation in the pigeon. Behavioural Brain Research 8, 343350.CrossRefGoogle ScholarPubMed
Bridges, C.D.B. (1982). Porphyropsin in retina of four-eyed fish Anableps anableps. Nature 300, 384.Google Scholar
Burkhardt, D.A., Gottesman, J., Levine, J.S. & MacNichol, E.F. (1983). Cellular mechanisms for color-coding in holostean retinas and the evolution of color vision. Vision Research 23, 10311041.CrossRefGoogle ScholarPubMed
Calderone, J.B. & Jacobs, G.H. (1995). Regional variations in the relative sensitivity to UV light in the mouse retina. Visual Neuroscience 12, 463468.Google Scholar
Calderone, J.B. & Jacobs, G.H. (2003). Spectral properties and retinal distribution of ferret cones. Visual Neuroscience 20, 1117.Google Scholar
Calderone, J.B., Reese, B.E. & Jacobs, G.H. (2003). Topography of photoreceptors and retinal ganglion cells in the spotted hyena (Crocuta crocuta). Brain, Behavior and Evolution 62, 182192.CrossRefGoogle ScholarPubMed
Carleton, K.L., Parry, J.W., Bowmaker, J.K., Hunt, D.M. & Seehausen, O. (2005). Colour vision and speciation in Lake Victoria cichlids of the genus Pundamilia. Molecular Ecology 14, 43414353.CrossRefGoogle Scholar
Cheng, C.L. & Novales Flamarique, I. (2004). Opsin expression: New mechanism for modulating colour vision. Nature 428, 279.Google Scholar
Christopher, C.C. & Barrett, G.W. (2006). Coexistence of white-footed mice (Peromyscus leucopus) and golden mice (Ochrotomys nuttalli) in a southeastern forest. Journal of Mammalogy 87, 102107.Google Scholar
Collin, S.P. & Shand, J. (2003). Retinal sampling and the visual field in fishes. In Sensory Processing in Aquatic Environments, ed.Collin, S.P. & Marshall, N.J., pp. 139169. New York: Springer-Verlag.CrossRefGoogle Scholar
de Monasterio, F.M., McCrane, E.P., Newlander, J.K. & Schein, S.J. (1985). Density profile of blue-sensitive cones along the horizontal meridian of macaque retina. Investigative Ophthalmology & Visual Science 26, 289302.Google Scholar
Denton, E.J. & Locket, N.A. (1989). Possible wavelength discrimination by multibank retinae in deep-sea fishes. Journal of the Marine Biological Association of the United Kingdom 69, 409435.CrossRefGoogle Scholar
Deutschlander, M.E., Greaves, D.K., Haimberger, T.J. & Hawryshyn, C.W. (2001). Functional mapping of ultraviolet photosensitivity during metamorphic transitions in a salmonid fish, Oncorhynchus mykiss. The Journal of Experimental Biology 204, 24012413.CrossRefGoogle Scholar
Dkhissi-Benyahya, O., Szel, A., Degrip, W.J. & Cooper, H.M. (2001). Short and mid-wavelength cone distribution in a nocturnal Strepsirrhine primate (Microcebus murinus). The Journal of Comparative Neurology 438, 490504.Google Scholar
Douglas, R.H. & Marshall, N.J. (1999). A review of vertebrate and invertebrate ocular filters. In Adaptive Mechanisms in the Ecology of Vision, ed. Archer, S.N., Djamgoz, M.B.A., Loew, E.R., Partridge, J.C. & Vallerga, S., pp. 95162. London: Kluwer Academic Publishers.Google Scholar
Douglas, R.H. & McGuigan, C.M. (1989). The spectral transmission of freshwater teleost ocular media - An interspecific comparison and a guide to potential ultraviolet sensitivity. Vision Research 29, 871879.CrossRefGoogle Scholar
Douglas, R.H. & Partridge, J.C. (1997). On the visual pigments of deep-sea fish. Journal of Fish Biology 50, 6885.Google Scholar
Douglas, R.H., Partridge, J.C. & Marshall, N.J. (1998). The eyes of deep-sea fish I: Lens pigmentation, tapeta and visual pigments. Progress in Retinal & Eye Research 17, 597636.CrossRefGoogle Scholar
Emond, M.P., McNeil, R., Cabana, T., Guerra, C.G. & Lachapelle, P. (2006). Comparing the retinal structures and functions in two species of gulls (Larus delawarensis and Larus modestus) with significant nocturnal behaviours. Vision Research 46, 29142925.CrossRefGoogle ScholarPubMed
Ferree, C.E. & Rand, G. (1919). Chromatic thresholds of sensation from center to periphery of the retina and their bearing on color theory. Psychological Review 26, 1641.CrossRefGoogle Scholar
Fröhlich, E., Negishi, K. & Wagner, H.J. (1995). The occurrence of dopaminergic interplexiform cells correlates with the presence of cones in the retinae of fish. Visual Neuroscience 12, 359369.Google Scholar
Gaillard, F., Kuny, S. & Sauve, Y. (2009). Topographic arrangement of S-cone photoreceptors in the retina of the diurnal Nile grass rat (Arvicanthis niloticus). Investigative Ophthalmology and Visual Science 50, 54265434.CrossRefGoogle ScholarPubMed
Gaten, E., Shelton, P.M.J. & Herring, P.J. (1992). Regional morphological variations in the compound eyes of certain mesopelagic shrimps in relation to their habitat. Journal of the Marine Biological Association of the United Kingdom 72, 6175.CrossRefGoogle Scholar
Glösmann, M., Steiner, M., Peichl, L. & Ahnelt, P.K. (2008). Cone photoreceptors and potential UV vision in a subterranean insectivore, the European mole. Journal of Vision 8, 23, 112.Google Scholar
Goldsmith, T.H. (1990). Optimization, constraint, and history in the evolution of eyes. The Quarterly Review of Biology 65, 281322.Google Scholar
Goldsmith, T.H., Collins, J.S. & Licht, S. (1984). The cone oil droplets of avian retinas. Vision Research 24, 16611671.CrossRefGoogle ScholarPubMed
Govardovskii, V.I., Fyhrquist, N., Reuter, T., Kuzmin, D.G. & Donner, K. (2000). In search of the visual pigment template. Visual Neuroscience 17, 509528.CrossRefGoogle ScholarPubMed
Hagstrom, S.A., Neitz, J. & Neitz, M. (1998). Variations in cone populations for red-green color vision examined by analysis of mRNA. Neuroreport 9, 19631967.Google Scholar
Hart, N.S. (2001). The visual ecology of avian photoreceptors. Progress in Retinal & Eye Research 20, 675703.Google Scholar
Hart, N.S., Lisney, T.J. & Collin, S.P. (2006). Cone photoreceptor oil droplet pigmentation is affected by ambient light intensity. The Journal of Experimental Biology 209, 47764787.Google Scholar
Heinermann, P.H. (1984). Yellow intraocular filters in fishes. Experimental Biology 43, 127147.Google ScholarPubMed
Hemenger, R.P. (1982). Dichroism of the macular pigment and Haidinger’s brushes. Journal of the Optical Society of America 72, 734737.CrossRefGoogle ScholarPubMed
Hemmi, J.M. & Grunert, U. (1999). Distribution of photoreceptor types in the retina of a marsupial, the tammar wallaby (Macropus eugenii). Visual Neuroscience 16, 291302.CrossRefGoogle ScholarPubMed
Hendrickson, A., Djajadi, H.R., Nakamura, L., Possin, D.E. & Sajuthi, D. (2000). Nocturnal tarsier retina has both short and long/medium-wavelength cones in an unusual topography. The Journal of Comparative Neurology 424, 718730.3.0.CO;2-Z>CrossRefGoogle Scholar
Hess, M., Melzer, R.R. & Smola, U. (1998). The photoreceptors of Muraena helena and Ariosoma balearicum - A comparison of multiple bank retinae in anguilliform eels (Teleostei). Zoologischer Anzeiger 237, 127137.Google Scholar
Hoke, K.L., Evans, B.I. & Fernald, R.D. (2006). Remodeling of the cone photoreceptor mosaic during metamorphosis of flounder (Pseudopleuronectes americanus). Brain, Behavior and Evolution 68, 241254.CrossRefGoogle ScholarPubMed
Hulke, J.W. (1867). On the retina of amphibia and reptiles. Journal of Anatomy & Physiology 1, 94-106, 378-101, 102, 115, 117, 119, & 378-121.Google Scholar
Jacobs, G.H. (2009). Evolution of colour vision in mammals. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 364, 29572967.Google Scholar
Jacobs, G.H., Williams, G.A., Cahill, H. & Nathans, J. (2007). Emergence of novel color vision in mice engineered to express a human cone opsin. Science 315, 17231725.Google Scholar
Jacobs, G.H., Williams, G.A. & Fenwick, J.A. (2004). Influence of cone pigment coexpression on spectral sensitivity and color vision in the mouse. Vision Research 44, 16151622.CrossRefGoogle ScholarPubMed
Juliusson, B., Bergstrom, A., Rohlich, P., Ehinger, B., Vanveen, T. & Szél, A. (1994). Complementary cone fields of the rabbit retina. Investigative Ophthalmology and Visual Science 35, 811818.Google Scholar
King-Smith, P.E. (1969). Absorption spectra and function of coloured oil drops in pigeon retina. Vision Research 9, 13911399.Google Scholar
Kirschfeld, K. (1982). Carotenoid pigments: Their possible role in protecting against photooxidation in eyes and photoreceptor cells. Proceedings of the Royal Society of London. Series B, Biological Sciences 216, 7185.Google ScholarPubMed
Knott, B., Berg, M.L., Morgan, E.R., Buchanan, K.L., Bowmaker, J.K. & Bennett, A.T.D. (2010). Avian retinal oil droplets: Dietary manipulation of colour vision? Proceedings of the Royal Society of London. Series B, Biological Sciences 277, 953962.Google ScholarPubMed
Knowles, A. & Dartnall, H.J.A. (1977). Habitat, habit and visual pigments. In The Eye, Vol. 2, ed. Davson, H., pp. 581649. London: Academic.Google Scholar
Kondrashev, S.L., Gamburtzeva, A.G., Gnjubkina, V.P., Orlov, O.J. & My, P.T. (1986). Coloration of corneas in fish: A list of species. Vision Research 26, 287290.Google Scholar
Land, M.F. & Nilsson, D.-E. (2002). Animal Eyes. Oxford: Oxford University Press.Google Scholar
Levine, J.S., MacNichol, E.F. Jr, Kraft, T. & Collins, B.A. (1979). Intraretinal distribution of cone pigments in certain teleost fishes. Science 204, 523526.CrossRefGoogle ScholarPubMed
Locket, N.A. (1977). Adaptations to the deep-sea environment. In The Visual System in Vertebrates in Handbook of Sensory Physiology, Vol. VII/5, ed. Crescitelli, F., pp. 67192. New York: Springer.Google Scholar
Loew, E.R. & Lythgoe, J.N. (1985). The ecology of colour vision. Endeavour 9, 170174.Google Scholar
Lythgoe, J.N. (1966). Visual pigments and underwater vision. In Light as an Ecological Factor, Vol. 6, ed. Bainbidge, R., Evans, C.C. & Rackham, D., pp. 375391. Oxford: Blackwell.Google Scholar
Lythgoe, J.N. (1979). The Ecology of Vision. Oxford: Clarendon Press.Google Scholar
Martin, P.R. & Grünert, U. (1999). Analysis of the short wavelength-sensitive (“blue”) cone mosaic in the primate retina: Comparison of New World and Old World monkeys. The Journal of Comparative Neurology 406, 114.Google Scholar
McFarland, W.N. & Munz, F.W. (1975). The visible spectrum during twilight and its implications to vision. In Light as an Ecological Factor (II) the 16th Symposium of the British Ecological Society, ed. Evans, G.C., Bainbridge, R. & Rackham, O., pp. 249270. Oxford: Blackwell Scientific Publications.Google Scholar
Misson, G.P. (2003). A Mueller matrix model of Haidinger’s brushes. Ophthalmic & Physiological Optics 23, 441447.Google Scholar
Munk, O. (1980). Retinal tapetum in the deep-sea teleost, Diretmus argenteus. Videnskabelige Meddelelser fra Dansk Naturhistorisk Forening 142, 179186.Google Scholar
Muntz, W.R.A. (1972). Inert absorbing and reflecting pigments. In Photochemistry of Vision (Handbook of Sensory Physiology), Vol. VII/1, ed. Dartnall, H.J.A., pp. 529565. New York: Springer.Google Scholar
Muntz, W.R.A. (1975). Visual pigments and the environment. In Vision in Fishes, ed. Ali, M.A., pp. 565577. New York: Plenium.Google Scholar
Muntz, W.R.A. & Northmore, D.P. (1971). Visual pigments from different parts of the retina in rudd and trout. Vision Research 11, 551561.Google Scholar
Munz, F.W. & McFarland, W.N. (1975). Part I: Presumptive cone pigments extracted from tropical marine fishes. Vision Research 15, 10451062.Google Scholar
Nuboer, J.F.W. & Wortel, J.F. (1985 a). A comparison of the spectral sensitivities of the chicken and the pigeon. Journal of Physiology 366, P13.Google Scholar
Nuboer, J.F.W. & Wortel, J.F. (1985 b). Wavelength discrimination in the lower and upper visual field of the pigeon. Journal of Physiology 366, P95P95.Google Scholar
O’Day, W.T. & Fernandez, H.R. (1976). Vision in lanternfish Stenobrachius leucopsarus (Myctophidae). Marine Biology 37, 187195.Google Scholar
Ollivier, F.J., Samuelson, D.A., Brooks, D.E., Lewis, P.A., Kallberg, M.E. & Komaromy, A.M. (2004). Comparative morphology of the tapetum lucidum (among selected species). Veterinary Ophthalmology 7, 1122.Google Scholar
Osorio, D. & Vorobyev, M. (1996). Colour vision as an adaptation to frugivory in primates. Proceedings of the Royal Society of London. Series B, Biological Sciences 263, 593599.Google Scholar
Osorio, D. & Vorobyev, M. (2008). A review of the evolution of animal colour vision and visual communication signals. Vision Research 48, 20422051.Google Scholar
Panorgias, A., Parry, N.R.A., McKeefry, D.J., Kulikowski, J.J. & Murray, I.J. (2009). Nasal-temporal differences in cone-opponency in the near peripheral retina. Ophthalmic and Physiological Optics 29, 375381.CrossRefGoogle ScholarPubMed
Parry, J.W., Carleton, K.L., Spady, T.C., Carboo, A., Hunt, D.M. & Bowmaker, J.K. (2005). Mix and match color vision: Tuning spectral sensitivity by differential opsin gene expression in lake Malawi cichlids. Current Biology 15, 17341739.Google Scholar
Partridge, J.C. (1989). The visual ecology of avian cone oil droplets. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 165, 415426.Google Scholar
Peichl, L. (2005). Diversity of mammalian photoreceptor properties: Adaptations to habitat and lifestyle? The Anatomical Record. Part A, Discoveries in Molecular, Cellular, and Evolutionary Biology 287A, 10011012.Google Scholar
Peichl, L., Chavez, A.E., Ocampo, A., Mena, W., Bozinovic, F. & Palacios, A.G. (2005). Eye and vision in the subterranean rodent cururo (Spalacopus cyanus, Octodontidae). The Journal of Comparative Neurology 486, 197208.CrossRefGoogle ScholarPubMed
Peichl, L., Künzle, H. & Vogel, P. (2000). Photoreceptor types and distributions in the retinae of insectivores. Visual Neuroscience 17, 937948.CrossRefGoogle ScholarPubMed
Peiponen, V.A. (1992). Color discrimination of two passerine bird species in the Munsell system. Ornis Scandinavica 23, 143151.CrossRefGoogle Scholar
Rahman, M.L., Aoyama, M. & Sugita, S. (2007). Number and density of retinal photoreceptor cells with emphasis on oil droplet distribution in the Mallard Duck (Anas platyrhynchos var. domesticus). Animal Science Journal 78, 639649.Google Scholar
Rahman, M.L., Yoshida, K., Maeda, I., Tanaka, H. & Sugita, S. (2010). Distribution of retinal cone photoreceptor oil droplets, and identification of associated carotenoids in crow (Corvus macrorhynchos). Zoological Science 27, 514521.Google Scholar
Remy, M. & Emmerton, J. (1989). Behavioral spectral sensitivities of different retinal areas in pigeons. Behavioral Neuroscience 103, 170177.Google Scholar
Reuter, T.E., White, R.H. & Wald, G. (1971). Rhodopsin and porphyropsin fields in the adult bullfrog retina. The Journal of General Physiology 58, 351371.CrossRefGoogle ScholarPubMed
Rocha, F.A.D., Ahnelt, P.K., Peichl, L., Saito, C.A., Silveira, L.C.L. & De Lima, S.M.A. (2009). The topography of cone photoreceptors in the retina of a diurnal rodent, the agouti (Dasyprocta aguti). Visual Neuroscience 26, 167175.CrossRefGoogle ScholarPubMed
Röhlich, P., van Veen, T. & Szél, A. (1994). Two different visual pigments in one retinal cone cell. Neuron 13, 11591166.CrossRefGoogle ScholarPubMed
Roorda, A. & Williams, D.R. (1999). The arrangement of the three cone classes in the living human eye. Nature 397, 520522.Google Scholar
Schiviz, A.N., Ruf, T., Kuebber-Heiss, A., Schubert, C. & Ahnelt, P.K. (2008). Retinal cone topography of artiodactyl mammals: Influence of body height and habitat. The Journal of Comparative Neurology 507, 13361350.Google Scholar
Shinozaki, A., Hosaka, Y., Imagawa, T. & Uehara, M. (2010). Topography of ganglion cells and photoreceptors in the sheep retina. The Journal of Comparative Neurology 518, 23052315.Google Scholar
Siebeck, U.E., Collin, S.P., Ghoddusi, M. & Marshall, N.J. (2003). Occlusable corneas in toadfishes: Light transmission, movement and ultrastruture of pigment during light- and dark-adaptation. The Journal of Experimental Biology 206, 21772190.Google Scholar
Siebeck, U.E. & Marshall, N.J. (2001). Ocular media transmission of coral reef fish: Can coral reef fish see ultraviolet light? Vision Research 41, 133149.Google Scholar
Stavenga, D.G. (2002). Colour in the eyes of insects. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 188, 337348.Google Scholar
Szél, A., Diamantstein, T. & Rohlich, P. (1988). Identification of the blue-sensitive cones in the mammalian retina by anti-visual pigment antibody. The Journal of Comparative Neurology 273, 593602.Google Scholar
Szél, A., Rohlich, P., Caffe, A.R., Juliusson, B., Aguirre, G. & van Veen, T. (1992). Unique topographic separation of two spectral classes of cones in the mouse retina. The Journal of Comparative Neurology 325, 327342.Google Scholar
Szél, A., Rohlich, P., Caffe, A.R. & van Veen, T. (1996). Distribution of cone photoreceptors in the mammalian retina. Microscopy Research and Technique 35, 445462.Google Scholar
Szél, A., van Veen, T. & Rohlich, P. (1994). Retinal cone differentiation. Nature 370, 336.Google Scholar
Takechi, M. & Kawamura, S. (2005). Temporal and spatial changes in the expression pattern of multiple red and green subtype opsin genes during zebrafish development. The Journal of Experimental Biology 208, 13371345.Google Scholar
Temple, S.E., Hart, N.S., Marshall, J. & Collin, S.P. (2010). A spitting image: Specializations in archerfish eyes for vision at the interface between air and water. Proceedings of the Royal Society of London. Series B, Biological Sciences 277, 26072615.Google Scholar
Temple, S.E., Plate, E.M., Ramsden, S., Haimberger, T.J., Roth, W.M. & Hawryshyn, C.W. (2006). Seasonal cycle in vitamin A1/A2-based visual pigment composition during the life history of coho salmon (Oncorhynchus kisutch). Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 192, 301313.Google Scholar
Temple, S.E., Ramsden, S.D., Haimberger, T.J., Veldhoen, K.M., Veldhoen, N.J., Carter, N.L., Roth, W.-M. & Hawryshyn, C.W. (2008 a). Effects of exogenous thyroid hormones on visual pigment composition in coho salmon (Oncorhynchus kisutch). The Journal of Experimental Biology 211, 21342143.Google Scholar
Temple, S.E., Veldhoen, K.M., Haimberger, T.J., Phelan, J.T., Veldhoen, N.J. & Hawryshyn, C.W. (2008 b). Ontogenetic changes in cone photoreceptor spectral absorption and opsin expression in coho salmon (Oncorhynchus kisutch). The Journal of Experimental Biology 211, 38793888.Google Scholar
Turner, J.R., White, E.M., Collins, M.A., Partridge, J.C. & Douglas, R.H. (2009). Vision in lanternfish (Myctophidae): Adaptations for viewing bioluminescence in the deep-sea. Deep-Sea Research Part I: Oceanographic Research Papers 56, 10031017.Google Scholar
Tyler, J.E. & Smith, R.C. (1970). Measurements of Spectral Irradiance Underwater. London: Gordon and Breach, Science Publishers, Inc.Google Scholar
Walls, G.L. (1942). The Vertebrate Eye and It’s Adaptive Radiation. Bloomfield Hills, MI: Cranbrook Press.Google Scholar
Walls, G.L. & Judd, H.D. (1933). The intra-ocular filters of vertebrates. The British Journal of Ophthalmology 17, 705725.CrossRefGoogle ScholarPubMed
Wang, Y.S., Macke, J.P., Merbs, S.L., Zack, D.J., Klaunberg, B., Bennett, J., Gearhart, J. & Nathans, J. (1992). A locus control region adjacent to the human red and green visual pigment genes. Neuron 9, 429440.Google Scholar
Wang, R.T., Nicol, J.A.C., Thurston, E.L. & McCants, M. (1980). Studies on the eyes of bigeyes (Teleostei Priacanthidae) with special reference to the tapetum lucidum. Proceedings of the Royal Society of London. Series B, Biological Sciences 210, 499512.Google Scholar
Warrant, E.J. & Nilsson, D.E. (1998). Absorption of white light in photoreceptors. Vision Research 38, 195207.Google Scholar
Weale, R.A. (1953). Spectral sensitivity and wave-length discrimination of the peripheral retina. Journal of Physiology 119, 170190.Google Scholar
Williams, G.A., Calderone, J.B. & Jacobs, G.H. (2005). Photoreceptors and photopigments in a subterranean rodent, the pocket gopher (Thomomys bottae). Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 191, 125134.Google Scholar
Willmer, E.N. & Wright, W.D. (1945). Colour sensitivity of the fovea centralis. Nature 156, 119121.Google Scholar
Wortel, J.F., Rugenbrink, H. & Nuboer, J.F.W. (1987). The photopic spectral sensitivity of the dorsal and ventral retinae of the chicken. Journal of Comparative Physiology. A, Sensory, Neural, and Behavioral Physiology 160, 151154.Google Scholar