Abstract
Despite their large brains, vertebrates extensively filter visual information with numerous adaptations within their eyes, simplifying the stream of neuronal traffic sent centrally and protecting retinal structures from photodamage. Each filtering mechanism can be considered ‘matched’ in the sense that it removes a particular component of incoming light. In this chapter, we consider these peripheral sensory filters of vertebrate eyes. While such eyes are built on a conserved design, they nevertheless incorporate a huge diversity of specialisations, including pigment filters, tuned visual pigments, optical adjustments and retinal sampling variations, all of which enhance the speed and utility of visual perception and simultaneously reduce the energetic cost of vision. Unlike invertebrates, many of whom figuratively re-engineer eye design from the ground up to favour particular visual tasks, vertebrates show enormous plasticity founded on a single fundamental design. This plasticity ranges among species, habitats and even seasons in some species, giving vertebrates as a group the ability to function in any location on earth that provides at least a few photons on which vision can be based.
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Beebe W (1935) Half mile down. The Bodley Head, London
Bernstein PS, Khachik F, Carvalho LS, Muir GJ, Zhao D-Y, Katz NB (2001) Identification and quantitation of carotenoids and their metabolites in the tissues of the human eye. Exp Eye Res 72:215–223
Bowmaker JK (2008) Evolution of vertebrate visual pigments. Vis Res 48:2022–2041
Bowmaker JK, Dartnall HJA, Herring PJ (1988) Longwave-sensitive visual pigments in some deep sea fishes: segregation of ‘paired’ rhodopsins and porphyropsins. J Comp Phys A 163:685–698
Bowmaker JK, Thorpe A, Douglas RH (1991a) Ultraviolet-sensitive cones in the goldfish. Vis Res 31:349–352
Bowmaker JK, Astell S, Hunt D, Mollon J (1991b) Photosensitive and photostable pigments in the retinae of old world monkeys. J Exp Biol 156:1–19
Carvalho LS, Knott B, Berg ML, Bennett ATD, Hunt DM (2011) Ultraviolet-sensitive vision in long-lived birds. Proc R Soc Lond B 278:107–114
Clarke GL, Denton EJ (1962) Light and animal life. In: Hill MN (ed) The sea. Wiley, New York, pp 456–468
Cochran WW, Mouritsen H, Wikelski M (2004) Migrating songbirds recalibrate their magnetic compasses daily from twilight cues. Science 304:405–408
Collin SP (1999) Behavioural ecology and retinal cell topography. In: Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S (eds) Adaptive mechanisms in the ecology of vision. Kluwer Academic Publishers, Dordrecht, pp 509–535
Collin SP, Shand J (2003) Retinal sampling and the visual field in fishes. In: Collin SP, Marshall NJ (eds) Sensory processing in aquatic environments. Springer, Berlin, pp p139–p169
Collin SP, Hoskins RV, Partridge JC (1997) Tubular eyes of deep-sea fishes: a comparative study of retinal topography. Brain Behav Evol 50:335–357
Collin SP, Hart NS, Shand J, Potter IC (2003) Morphology and spectral absorption characteristics of retinal photoreceptors in the southern hemisphere lamprey (Geotria australis). Vis Neurosci 20:119–130
Collin SP, Davies WL, Hart NS, Hunt DM (2009) The evolution of early vertebrate photoreceptors. Phil Trans R Soc Lond B 364:2925–2940
Cronin TW, Järvilehto M, Weckström M, Lall AB (2000) Tuning of photoreceptor spectral sensitivity in fireflies (Coleoptera: Lampyridae). J Comp Phys A 186:1–12
Cronin TW, Johnsen S, Marshall NJ, Warrant EJ (2014) Visual ecology. Princeton University Press, Princeton
Dawson WW, Schroeder JP, Sharpe SN (1987) Corneal surface properties of two marine mammal species. Mar Mamm Sci 3:186–197
Denton EJ (1990) Light and vision at depths greater than 200m. In: Herring PJ, Campbell AK, Whitfield M, Maddock L (eds) Light and life in the sea. Cambridge University Press, Cambridge, pp 127–148
Denton EJ, Gilpin-Brown JB, Wright PG (1970) On the ‘filters’ in the photophores of mesopelagic fish and on a fish emitting red light and especially sensitive to red light. J Physiol Lond 208:72–73P
Denton EJ, Herring PJ, Widder EA, Latz MF, Case JF (1985) The roles of filters in the photophores of oceanic animals and their relation to vision in the oceanic environment. Proc R Soc Lond B 225:63–97
Douglas RH (1989) The spectral transmission of the lens and cornea of the brown trout (Salmo trutta) and goldfish (Carassius auratus) – effect of age and implications for ultraviolet vision. Vision Res 29(7):861–869
Douglas RH (2001) The ecology of teleost fish visual pigments: a good example of sensory adaptation to the environment? In: Barth FG, Schmidt A (eds) Ecology of sensing. Springer, Berlin, pp 215–235
Douglas RH, Jeffery G (2014) The spectral transmission of ocular media suggest ultraviolet sensitivity is widespread among mammals. Proc R Soc Lond B 281:20132995
Douglas RH, Marshall NJ (1999) A review of vertebrate and invertebrate ocular filters. In: Archer SN, Djamgoz MBA, Loew ER, Partridge JC, Vallerga S (eds) Adaptive mechanisms in the ecology of vision. Kluwer Academic Publishers, Dordrecht, pp 95–162
Douglas RH, Thorpe A (1992) Short wave absorbing pigments in the ocular lenses of deep-sea teleosts. J Mar Biol Assoc UK 72:93–112
Douglas RH, Partridge JC, Marshall NJ (1998a) The eyes of deep-sea fish I: lens pigmentation, tapeta and visual pigments. Prog Retin Eye Res 17:597–636
Douglas RH, Partridge JC, Dulai K, Hunt D, Mullineaux CW, Tauber A, Hynninen PH (1998b) Dragon fish see using chlorophyll. Nature 393:423–424
Douglas RH, Harper RD, Case JF (1998c) The pupil response of a teleost fish, Porichthys notatus: description and comparison to other species. Vis Res 38:2697–2710
Douglas RH, Partridge JC, Dulai KS, Hunt DM, Mullineaux CW, Hynninen PH (1999) Enhanced retinal longwave sensitivity using a chlorophyll-derived photosensitiser in Malacosteus niger, a deep-sea dragon fish with far red bioluminescence. Vis Res 39:2817–2832
Douglas RH, Bowmaker JK, Mullineaux CW (2002a) A possible retinal longwave detecting system in a myctophid fish without far-red bioluminescence; evidence for a sensory arms race in the deep-sea. In: Stanley PE, Kricka LJ (eds) Bioluminescence and chemiluminescence; progress and current applications. World Scientific, River Edge, pp 391–394
Douglas RH, Collin SP, Corrigan J (2002b) The eyes of suckermouth armoured catfish (Loricariidae, subfamily Hypostomus): pupil response, lenticular longitudinal spherical aberration and retinal topography. J Exp Biol 205:3425–3433
Douglas RH, Hunt DM, Bowmaker JK (2003) Spectral sensitivity tuning in the deep-sea. In: Collin SP, Marshall NJ (eds) Sensory processing in aquatic environments. Springer, New York, pp 323–342
Ellingson JM, Fleishman LJ, Loew ER (1995) Visual pigments and spectral sensitivity of the diurnal gecko Gonatodes albogularis. J Comp Phys A 177:559–567
Fasick JL, Robinson PR (2000) Spectral-tuning mechanisms of marine mammal rhodopsins and correlations with foraging depth. Vis Neurosci 17:781–788
Fineran BA, Nichol JAC (1978) Studies on the photoreceptors of Anchoa mitchilli and A. hepsetus (Engraulidae) with particular reference to the cones. Phil Trans R Soc Lond B 283:25–60
Fleishman LJ, Howland HC, Howland MJ, Rand AS, Davenport ML (1988) Crocodiles don’t focus underwater. J Comp Phys A 163:441–443
Gislen A, Dacke M, Kröger RHH, Abrahamsson M, Nilsson DE, Warrant EJ (2003) Superior underwater vision in a human population of sea gypsies. Curr Biol 13:33–836
Gislen A, Warrant EJ, Dacke M, Kröger RHH (2006) Visual training improves underwater vision in children. Vis Res 48:3443–3450
Glickstein M, Millodot M (1970) Retinoscopy and eye size. Science 168:605–606
Haddock SHD, Moline MA, Case JF (2010) Bioluminescence in the sea. Ann Rev Mar Sci 2:443–493
Hanke FD, Dehnhardt G, Schaeffel F, Hanke W (2006) Corneal topography, refractive state, and accommodation in harbour seals (Phoca vitulina). Vis Res 46:837–847
Hart NS (2001) The visual ecology of avian photoreceptors. Prog Retin Eye Res 20:675–703
Hart NS, Vorobyev M (2005) Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors. J Comp Phys A 191:381–392
Hart NS, Bailes HJ, Vorobyev M, Marshall NJ, Collin SP (2008) Visual ecology of the Australian lungfish (Neoceratodus forsteri). BMC Ecol 8:21. doi:10.1186/1472-6785-8-21
Hasegawa E, Sawada K, Abe K, Watanabe K, Uchikawa K, Okazaki Y, Toyama M, Douglas RH (2008) The visual pigments of a deep-sea myctophid fish Myctophum nitidulum (Garman); an HPLC and spectroscopic description of a non-paired rhodopsin–porphyropsin system. J Fish Biol 72:937–945
Henze MJ, Shaeffel F, Ott M (2004) Variations in the off-axis refractive state in the eye of the Vietnamese leaf turtle (Geoemyda spengleri). J Comp Phys A 190:131–137
Hodos W, Erichsen JT (1990) Lower-field myopia in birds: an adaptation that keeps the ground in focus. Vis Res 30:653–657
Hogg C, Neveu M, Stokkan K-A, Folkow L, Cottril P, Douglas RH, Hunt DM, Jeffery G (2011) Arctic reindeer extend their visual range into the ultraviolet. J Exp Biol 214:2014–2019
Horváth G, Varjú D (2004) Polarized light in animal vision. Springer, Berlin
Howland HC, Howland M, Murphy CJ (1993) Refractive state of the rhinoceros. Vis Res 33:2649–2651
Jordan TM, Roberts NW, Partridge JC (2012) An omnidirectional broadband mirror design inspired by biological multilayer reflectors. Proc SPIE 8339:83390G
Katzir G, Howland HC (2003) Corneal power and underwater accommodation in great cormorants (Phalacrocorax carbo sinensis). J Exp Biol 206:833–841
Kondrashev SL (2008) Long-wave sensitivity in the masked greenling (Hexagrammos octogrammus), a shallow-water marine fish. Vis Res 48:2269–2274
Kröger RHH (2013) Optical plasticity in fish lenses. Prog Retin Eye Res 34:78–88
Kröger RHH, Campbell MCW, Fernald RD, Wagner HJ (1999) Multifocal lenses compensate for chromatic defocus in vertebrate eyes. J Comp Phys A 184:36–369
Lamb TD, Pugh EN (2004) Dark adaptation and the retinoid cycle of vision. Prog Retin Eye Res 23:307–380
Land MF (2009) Biological optics: deep reflections. Curr Biol 19:R78–R80
Land MF, Nilsson D-E (2012) Animal eyes, 2nd edn. Oxford University Press, Oxford
Lind O, Mitkus M, Olsson P, Kelber A (2014) Ultraviolet vision in birds: the importance of transparent eye media. Proc R Soc Lond B 281:20132209
Lluch S, Lopez-Fuster MJ, Ventura J (2003) Giant mitochondria in the retina cone inner segments of shrews of genus Sorex (Insectivora, Soricidae). Anat Rec Part A 272A:484–490
Locket NA (1977) Adaptations to the deep-sea environment. In: Crescitelli F (ed) Handbook of sensory physiology VII/5; the visual system of vertebrates. Springer, New York, pp 67–192
Locket NA (2000) On the lens pad of Benthalbella infans, a scopelarchid deep-sea teleost. Phil Trans R Soc Lond B 355:1167–1169
Loew ER, Govardovskii VI (2001) Photoreceptors and visual pigments in the red-eared turtle, Trachemys scripta elegans. Vis Neurosci 18:753–757
Loew ER, Fleishman LJ, Foster RG, Provencio I (2002) Visual pigments and oil droplets in diurnal lizards: a comparative study of Caribbean anoles. J Exp Biol 205:927–938
Losey GS, McFarland WN, Loew ER, Zamzow JP, Nelson PA, Marshall NJ (2003) Visual biology of Hawaiian coral reef fishes. 1. Ocular transmission and visual pigments. Copeia 2003:433–454
Lythgoe JN (1971) Iridescent corneas is fish. Nature 233:205–207
Lythgoe JN (1972) The adaptation of visual pigments to the photic environment. In: Dartnall HJA (ed) Handbook of sensory physiology VII/1; photochemistry of vision. Springer, Berlin, pp 566–624
Lythgoe JN (1979) The ecology of vision. Clarendon Press, Oxford
Mass AM, Supin AY, Severtov AN (1986) Topographic representation of sizes and density of ganglion cells in the retina of a Porpoise, Phocoena phocoena. Aquat Mamm 12:95–102
Meredith RW, Gatesy J, Emerling CA, York VM, Springer MS (2013) Rod monochromacy and the evolution of cetacean retinal opsins. PLoS Genet 9:e1003432
Muheim R (2011) Behavioural and physiological mechanisms of polarized light sensitivity in birds. Phil Trans R Soc Lond B 366:763–771
Muheim R, Phillips JB, Akesson S (2006) Polarized light cues underlie compass calibration in migratory songbirds. Science 313:837–839
Munk O (1966) Ocular anatomy of some deep-sea teleosts. Dana Rep 70:1–71
Munk O (1970) On the occurrence and significance of horizontal band-shaped retinal areas in teleosts. Vidensk Medd Dan Naturhist Foren 133:85–120
Muntz WRA (1976a) The visual consequences of yellow filtering pigments. In: Evans GC, Bainbridge R, Rackham O (eds) Light as an ecological factor: II. Blackwell Scientific Publications, Oxford, pp 271–287
Muntz WRA (1976b) On yellow lenses in mesopelagic animals. J Mar Biol Assoc UK 56:963–976
Murphy CJ, Howland HC (1991) The functional significance of crescent-shaped pupils and multiple pupillary apertures. J Exp Zool Suppl 5:22–28
Murphy CJ, Bellhorn RW, Williams T, Burns MS, Schaeffel F, Howland HC (1990) Refractive state, ocular anatomy, and accommodative range of the sea otter (Enhydra lutris). Vis Res 30:23–32
Nelson PA, Zamzow JP, Losey GS (2001) Ultraviolet blocking in the ocular humors of the teleost fish Acanthocybium solandri (Scombridae). Can J Zool 79:1714–1718
Nicol JAC (1981) Tapeta lucida of vertebrates. In: Enoch JM, Tobey FL (eds) Vertebrate photoreceptor optics. Springer, Berlin, pp 401–431
Novales-Flamarique I, Hárosi F (2000) Photoreceptors, visual pigments, and ellipsosomes in the killifish, Fundulus heteroclitus: a microspectrophotometric and histological study. Vis Neurosci 17:403–420
Ollivier FJ, Samuelson DA, Brooks DE, Lewis PA, Kallberg ME, Komáromy AM (2004) Comparative morphology of the tapetum lucidum (among selected species). Vet Ophthalmol 7:11–22
Ott M (2006) Visual accommodation in vertebrates: mechanisms, physiological response and stimuli. J Comp Phys A 192:97–111
Ott M, Schaffel F, Krimse W (1998) Binocular vision and accommodation in prey-catching chameleons. J Comp Phys A 182:319–330
Partridge JC, Douglas RH, Marshall NJ, Chung W-S, Jordan TM, Wagner HJ (2014) Reflecting optics in the diverticular eye of a deep-sea barreleye fish (Rhynchohyalus natalensis). Proc R Soc Lond B 281:20133223
Peichl L, Behrmann G, Kröger RHH (2001) For whales and seals the ocean is not blue: a visual pigment loss in marine mammals. Eur J Neurosci 13:1520–1528
Perlman I, Normann A (1998) Light adaptation and sensitivity controlling mechanisms in vertebrate photoreceptors. Prog Retin Eye Res 17:523–563
Phillips JB, Waldvogel JA (1988) Celestial polarized patterns as a calibration reference for sun compass of homing pigeons. J Theor Biol 131:55–67
Phillips JB, Deutschlander ME, Freake MJ, Borland SC (2001) The role of extraocular photoreceptors in newt magnetic compass orientation: parallels between light-dependent magnetoreception and polarized light detection. J Exp Biol 204:2543–2552
Phillips JB, Muheim R, Jorge PE (2010) A behavioral perspective on the biophysics of the light-dependent magnetic compass: a link between directional and spatial perception? J Exp Biol 213:3247–3255
Porter ML, McCready R, Kingston A, Cameron E, Hofmann C, Suarez L, Olsen GH, Cronin TW, Robinson PR (2014) Visual pigments, oil droplets, lens, and cornea characterization in the whooping crane (Grus americana). J Exp Biol 217:3883–3890
Quiroga RQ, Reddy L, Kreiman G, Koch C, Fried I (2005) Invariant visual representation by single neurons in the human brain. Nature 435:1102–1107
Roberts NW, Porter ML, Cronin TW (2011) The molecular basis of mechanisms underlying polarization vision. Phil Trans R Soc Lond B 366:627–637
Robinson SR (1994) Early vertebrate colour vision. Nature 367:121
Schaeffel F, Hagel G, Eikermann J, Collett T (1994) Lower-field myopia and astigmatism in amphibians and chickens. J Opt Soc Am A 11:487–497
Siebeck UE, Marshall NJ (2000) Transmission of ocular media in labrid fishes. Phil Trans R Soc Lond B 355:1257–1261
Siebeck UE, Marshall NJ (2001) Ocular media transmission of coral reef fish – can coral reef fish see ultraviolet light? Vis Res 41:133–149
Siebeck UE, Collin SP, Ghoddusi M, Marshall NJ (2003) Occlusable corneas in toadfishes: light transmission, movement and ultrastructure of pigment during light- and dark-adaptation. J Exp Biol 206:2177–2190
Sivak JG (1980) Accommodation in vertebrates. In: Zadunaisky JA, Davson H (eds) Current topics in eye research. Academic, New York, pp p281–p330
Sivak JG (1991) Elasmobranch visual optics. J Exp Zool Suppl 5:13–21
Sivak JG, Hildebrand T, Lebert C (1985) Magnitude and rate of accommodation in diving and nondiving birds. Vis Res 25:925–933
Sivak J, Howland HC, McGill-Harelstad P (1987) Vision in the Humboldt penguin (Spheniscus humboldti) in air and water. Proc R Soc Lond B 229:467–472
Sivak JG, Howland HC, West J, Weerheim J (1989) The eye of the hooded seal, Crystophora cristata, in air and water. J Comp Phys A 165:771–777
Solovei I, Kreysing M, Lanctot C, Kosem S, Peichl L, Cremer T, Guck J, Joffe B (2009) Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution. Cell 137:356–368
Somiya H (1976) Functional significance of the yellow lens in the eyes of Argyropelecus affinis. Mar Biol 34:93–99
Somiya H (1982) “Yellow lens” eyes of a stomiatoid deep-sea fish Malacosteus niger. Proc R Soc Lond B 215:481–489
Stokkan K-A, Folkow L, Dukes J, Neveu M, Hogg C, Siefken S, Dakin SC, Jeffery G (2013) Shifting mirrors: adaptive changes in retinal reflections to winter darkness in Arctic reindeer. Proc Roy Soc Lond B 280:20132451
Tarboush R, Novales-Flamarique I, Chapman GB, Connaughton VP (2014) Variability in mitochondria of zebrafish photoreceptor ellipsoids. Vis Neurosci 31:11–23
Temple S, Hart NS, Marshall NJ, Collin SP (2010) A spitting image: specializations in archerfish eyes for vision at the interface between air and water. Proc R Soc Lond B 277:2607–2615
Thorpe A, Douglas RH, Truscott RJW (1993) Spectral transmission and short-wave absorbing pigments in the fish lens. I Phylogenetic distribution and identity. Vis Res 33:289–300
Turner JR, White EM, Collins MA, Partridge JC, Douglas RH (2009) Vision in lanternfish (Myctophidae): adaptations for viewing bioluminescence in the deep-sea. Deep-Sea Res Pt I 56:1003–1017
Tyler NJC, Jeffery G, Hogg CR, Stokkan K-A (2014) Ultraviolet vision may enhance the ability of reindeer to discriminate plants in snow. Arctic 67:159–166
van Norren D, Gorgels TGMF (2011) The action spectrum of photochemical damage to the retina: a review of monochromatic threshold data. Photochem Photobiol 87:747–753
Vorobyev M (2003) Coloured oil droplets enhance colour discrimination. Proc R Soc Lond B 270:1255–1261
Wagner HJ, Fröhlich E, Negishi K, Collin SP (1998) The eyes of deep-sea fishes II functional morphology of the retina. Prog Retin Eye Res 17:637–685
Wagner HJ, Douglas RH, Frank TM, Roberts NW, Partridge JC (2009) A novel vertebrate eye using both reflective and refractive optics. Curr Biol 19:108–114
Walls GL (1931) The occurrence of coloured lenses in the eyes of snakes and squirrels, and their probable significance. Copeia 1931:125–127
Walls GL (1963) The vertebrate eye and its adaptive radiation. Hafner Publishing Co, New York
Wang RT, Nicol JAC (1974) The tapetum lucidum of gars (Lepisosteidae) and its role as a reflector. Can J Zool 52:1523–1530
Warrant EJ, Collin SP, Locket NA (2003) Eye design and vision in deep-sea fishes. In: Collin SP, Marshall NJ (eds) Sensory processing in aquatic environments. Springer, New York, pp 303–322
Wehner R (1987) ‘Matched filters’ – neural models of the external world. J Comp Physiol A 161:511–531
Whitehead AJ, Mares JA, Danis RP (2006) Macular pigment: a review of current knowledge. Arch Ophthalmol 124:1038–1045
Widder EA (2010) Bioluminescence in the ocean: origins of biological, chemical and ecological diversity. Science 328:704–708
Widder EA, Latz MI, Herring PJ, Case JF (1984) Far red bioluminescence from two deep-sea fishes. Science 225:512–514
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Douglas, R.H., Cronin, T.W. (2016). Visual Matched Filtering in Vertebrates. In: von der Emde, G., Warrant, E. (eds) The Ecology of Animal Senses. Springer, Cham. https://doi.org/10.1007/978-3-319-25492-0_7
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