• 1990 (Vol.4)
  • 1989 (Vol.3)
  • 1988 (Vol.2)
  • 1987 (Vol.1)

What did adaptive optics give us for understanding the mechanisms of human color vision

© 2023 E. M. Maximova

Institute for Information Transmission Problems of the Russian Academy of Sciences (Kharkevich Institute) 127051 Moscow, B. Karetnyi pereulok, 14, Russia

Received 28 Sep 2022

Information on the color vision of animals and humans, the history and methods of its study is briefly presented. The results of fundamental research in this area obtained using adaptive optics and scanning laser ophthalmoscopy (AOSLO) in combination with densitometry, phase-sensitive optical coherence tomography (AO-PSOCT), and calcium imaging (Ca++ imaging) are described. These methods made it possible for the first time in vivo to see the mosaic of human retinal L, M, S cones, to build maps of the location of cones of three different types, to study color perception during stimulation of single cones.

Key words: color vision, L cones, M cones, S cones, adaptive optics, dichromasia, color coding

DOI: 10.31857/S0235009223010055  EDN: AUAGVN

Cite: Maximova E. M. Chto dala adaptivnaya optika dlya ponimaniya mekhanizmov tsvetovogo zreniya cheloveka [What did adaptive optics give us for understanding the mechanisms of human color vision]. Sensornye sistemy [Sensory systems]. 2023. V. 37(1). P. 17–34 (in Russian). doi: 10.31857/S0235009223010055

References:

  • Bongard M.M., Kolorimetriya na zhivotnykh [Colorimetry on animals] Doklady Akademii nauk SSSR [Reports of the Academy of Sciences of the USSR]. 1955. V. 103 (2). P. 239–242 (in Russian).
  • Bongard M.M., Smirnov M.S. Chetyrekhmernost’ tsvetovogo prostranstva cheloveka [Four-dimensionality of the human color space]. Doklady Akademii nauk SSSR [Reports of the Academy of Sciences of the USSR]. 1956. V. 108 (3). P. 447–449 (in Russian).
  • Bongard M.M., Smirnov M.S. Vizual’naya kolorimetriya metodom zameshcheniya (novaya sistema kolorimetra dlya issledovaniya tsvetovogo zreniya cheloveka) [The replacement method in visual colorimetry]. Biofizika [Biophysics]. 1957. V. 2 (1). P. 119–123 (in Russian).
  • Bongard M.M., Smirnov M.S. Krivye spektral’noi chuvstvitel’nosti priemnikov, svyazannykh s odinochnymi voloknami zritel’nogo nerva lyagushki [Spectral sensitivity curves of receptors connected with single optic nerve fibers in the frog]. Biofizika [Biophysics]. 1957. V. 2 (3). P. 336–342 (in Russian).
  • Bongard M.M., Smirnov M.S. O “kozhnom zrenii” R. Kuleshovoi [On “skin vision” of R. Kuleshova]. Biofizika [Biophysics]. 1965. V. 10 (1). P. 48–54 (in Russian).
  • Govardovskii V.I., Astakhova L.A., Firsov M.L. Spetsifika fiziologicheskikh i biokhimicheskikh mekhanizmov vozbuzhdeniya i adaptatsii kolbochek setchatki [Specifics of physiological and biochemical mechanisms of excitation and adaptation in retinal cones]. Sensornye sistemy [Sensory systems]. 2015. V. 29 (4). P. 296–308 (in Russian).
  • Kalamkarov G.R., Ostrovskii M.A. Molekulyarnye mekhanizmy zritel’noi retseptsii [Molecular mechanisms of visual reception]. Moscow. Nauka Publ, 2002. 279 p. (in Russian).
  • Kondrashev S.L., Orlov O.Yu. Kolorimetricheskoe izuchenie tsvetovogo zreniya travyanoi lyagushki [A colorimetrical study of colour vision in common frog]. Vestnik Moskovskogo universiteta. Seriya 6: biologiya, pochvovedenie [Bulletin of the Moscow University. Series 6: biology, soil science]. 1975. № 4. P. 107–110 (in Russian).
  • Maximova E.M., Aliper A.T., Damjanović I., Zaichikova A.A., Maximov P.V. Ganglioznye kletki s fonovoi aktivnost’yu setchatki ryb i ikh vozmozhnaya funktsiya v otsenke zritel’noi stseny [Ganglion Cells with Sustained Activity of the Fish Retina and Their Putative Function in Comprehension of the Visual Surround]. Rossiiskii fiziologicheskii zhurnal im. I.M. Sechenova [I.M. Sechenov Russian Journal of Physiology]. 2020. V. 106 (4). P. 486–503. https://doi.org/10.31857/S0869813920040044 (in Russian).
  • Mazohin-Porshnyakov G.A. Kolorimetricheskoe izuchenie svoistv zreniya strekoz (elektrofiziologicheskoe issledovanie) [Colorimetric study of colour vision in dragonfly]. Biofizika [Biophysics]. 1959. V. 4 (4). P. 427–436 (in Russian).
  • Mazohin-Porshnyakov G.A. Kolorimetricheskoe dokazatel’stvo trikhromazii pchelinykh (na primere shmelei) [Colorimetric evidence of trichromasia in bees (on the example of bumblebees)]. Biofizika [Biophysics]. 1962. V. 7 (2). P. 211–217 (in Russian).
  • Nyuberg N.D., Paradoksy tsvetnogo zreniya [Paradoxes of color vision]. Priroda [Nature]. 1960. No. 8. P. 53–59 (in Russian).
  • Ovchinnikov Yu.A., Abdulaev N.G., Feigina N.Yu., Artamonov I.D., Zolotarev A.S. Polnaya aminokislotnaya posledovatel’nost' zritel’nogo rodopsina [Complete amino acid sequence of visual rhodopsin]. Bioorganicheskaya. khimiya [Bioorganic Chemistry]. 1982. V. 8 (10). P. 1424–1427 (in Russian).
  • Orlov O.Yu. Fiziologicheskie osnovy tsvetovogo zreniya cheloveka [Physiological basis of human color vision]. Sb.: Klinicheskaya fiziologiya zreniya. Ocherki [Clinical physiology of vision. Essays]. 2006. Ed. A.M. Shamshinova, 3rd edition. Moscow. MBN. P. 298–340 (in Russian)
  • Orlov O.Yu., Byzov A.L. Kolorimetricheskoe issledovanie zreniya golovonogikh mollyuskov (Cephalopoda) [Colorimetric study of the vision of cephalopods (Cephalopoda)]. Doklady Akademii nauk SSSR [Reports of the Academy of Sciences of the USSR]. 1961. V. 139 (3). P. 723–725 (in Russian).
  • Orlov O.Yu., Maximova E.M. O roli vnutrikolbochkovykh svetofil’trov (mekhanizm TsZ yashcheritsy i cherepakhi) [On the role of intracone light filters (mechanism of color vision of lizards and turtles)]. Doklady Akademii nauk SSSR [Reports of the Academy of Sciences of the USSR]. 1964. V. 154 (2). P. 463–466 (in Russian).
  • Ostrovskii M.A., Govardovskii V.I. Mekhanizmy fotoretseptsii pozvonochnykh [Mechanisms of photoreception in vertebrates]. Fiziologiya zreniya [Vision physiology]. Moscow. Nauka, 1992. P. 5–59 (in Russian).
  • Podugolnikova T.A., Maximov V.V. Regulyarnost’ prostranstvennoi struktury retseptornogo i nervnykh sloev setchatki kostistykh ryb: svetovaya mikroskopiya [Regularity of spatial structure of receptor and neural layers in the retinae of bony fishes: light microscopy]. Zoologicheskii zhurnal [Zoological journal]. 1973. V. 52 (4), P. 541–551 (in Russian).
  • Podugolnikova T.A., Maximov V.V. Mozaika fotoretseptorov i nervnykh elementov setchatki ryb [Mosaic of photoreceptors and neural units in the fish retina]. Cbornik, Sensornye sistemy [Sensory systems]. 1977. P. 178–196 (in Russian).
  • Smirnov M.S. Measurement of the wave aberration in the human eye. Biofizika [Biophysics]. 1961. V. 6 (6). P. 687–703 (in Russian).
  • Ahnelt P.K., Kolb H. The mammalian photoreceptor mosaic-adaptive design. Prog Ret Eye Res. 2000. V. 19 (6). P. 711–777
  • Allison W.T., Barthel L.K., Skebo K.M., Takechi M., Kawamura S., Raymond P.A. Ontogeny of cone photoreceptor mosaics in zebrafish. J. Comp. Neurol. 2010. V. 518 (20). P. 4182–4195. https://doi.org/10.1002/cne.22447
  • Arrese C.A., Hart N.S., Thomas N., Beazley L.D., Shand J. Trichromacy in Australian marsupials. Curr. Biol. 2002. V. 12. P. 657–660. https://doi.org/10.1016/S0960-9822(02)00772-8
  • Arrese C.A., Beazley L.D., Neumeyer C. Behavioural evidence of marsupial trichromacy. Curr. Biol. 2006. V. 16. P. R193–R194. https://doi.org/10.1016/j.cub.2006.02.036
  • Baden T. Circuit mechanisms for colour vision in zebrafish. Review. Current Biology. 2021. V. 31. P. R807–R820. https://doi.org/10.1126/sciadv.abj6815
  • Baden T., Euler T., Berens P. Understanding the retinal basis of vision across species. Nat Rev Neurosci. 2020. V. 21 (1). P. 5–20. https://doi.org/10.1038/s41583-019-0242-1
  • Baden T., Osorio D. The retinal basis of vertebrate color vision. Annu Rev Vis Sci. 2019. V. 5. P. 177–200. https://doi.org/10.1146/annurev-vision-091718-014926
  • Baden T., Schubert T., Chang L., Wei T., Zaichuk M., Wissinger B., Euler T. A tale of two retinal domains: Near-Optimal sampling of achromatic contrasts in natural scenes through asymmetric photoreceptor distribution. Neuron. 2013. V. 80 (5). P. 1206–1217. https://doi.org/10.1016/j.neuron.2013.09.030
  • Baraas R.C., Carroll J., Gunther K.L., Chung M., Williams D.R., Foster D.H., Neitz M. Adaptive optics retinal imaging reveals S-cone dystrophy in tritan colorvision deficiency. J. Opt. Soc. Am. A. 2007. V. 24 (5). P. 1438–1447. https://doi.org/10.1364/josaa.24.001438
  • Bilotta J., Saszik S. The zebrafish as a model visual system. Int J Dev Neurosci. 2001. V. 19 (7). P. 621–629. https://doi.org/10.1016/s0736-5748(01)00050-8
  • Boycott B.B., Dowling J.E., Kolb H. Organization of the primate retina: light microscopy. Philos Trans R Soc Lond B Biol Sci. 1969. V. 255. P. 109–184. https://doi.org/10.1098/rstb.1969.0004
  • Bowmaker J.K., Dartnall H.J. Visual pigments of rods and cones in a human retina. J Physiol. 1980. V. 298. P. 501–511. https://doi.org/10.1113/jphysiol.1980.sp013097
  • Bowmaker J.K. Evolution of colour vision in vertebrates. Eye (Lond). 1998. V. 12. P. 541–547. https://doi.org/10.1038/eye.1998.143
  • Bowmaker J.K., Microspectrophotometry of vertebrate photoreceptors: A brief review. Vision Research. 1984. V. 24 (11). P. 1641–1650. https://doi.org/10.1016/0042-6989(84)90322-5
  • Campbell F.W. and Rushton W.A.H. Measurement of the scotopic pigment in the living human eye. J Physiol. 1955. V. 130 (1). P. 131–147. https://doi.org/10.1113/jphysiol.1955.sp005399
  • Carroll J., Neitz M., Hofer H., Neitz J., Williams D.R. Functional photoreceptor loss revealed with adaptive optics: An alternate cause of color blindness. PNAS. 2004. V. 101 (22). P. 8461–8466. https://doi.org/10.1073/pnas.0401440101
  • Collin S.P., Trezise A.E. The origins of colour vision in vertebrates. Clin Exp Optom. 2004. V. 87 (4–5). P. 217–223. https://doi.org/10.1111/j.1444-0938.2004.tb05051.x
  • Curcio C.A., Sloan K.R., Kalina R.E., Hendrickson A.E. Human photoreceptor topography. J. Comp Neurol. 1990. V. 292 (4). P. 497–523. https://doi.org/10.1002/cne.902920402
  • Curcio C.A., Allen K.A., Sloan K.R., Lerea C.L., Hurley J.B., Klock I.B., Milam A.H. Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. J. Comp Neurol. 1991. V. 312 (4). P. 610–624. https https://doi.org/10.1002/cne.903120411
  • Dacey D.M. Primate retina: cell types, circuits and color opponency. Prog Retin Eye Res.1999. V. 18 (6). P. 737–763. https://doi.org/10.1016/s1350-9462(98)00013-5
  • Dacey D.M. Parallel pathways for spectral coding in primate retina. Annu. Rev. Neurosci. 2000. V. 23. P. 743–775. https://doi.org/10.1146/annurev.neuro.23.1.743
  • Dacey D.M., Packer O.S. Colour coding in the primate retina: diverse cell types and cone-specific circuitry. Curr Opin Neurobiol. 2003.V. 13 (4). P. 421–427. https://doi.org/10.1016/s0959-4388(03)00103-x
  • Danilova M.V., Mollon J.D. Bongard and Smirnov on the tetrachromacy of extra-foveal vision. Vision Research. 2022. V. 195. P. 107952. https://doi.org/10.1016/j.visres.2021.08.007
  • Dartnall H.J.A., Bowmaker J.K., Mollon J.D. Human visual pigments: microspectrophotometric results from the eyes of seven persons. Proc. R. Soc. Lond. B. Biol. Sci. 1983. V. 220 (1218). P. 115–130. https://doi.org/10.1098/rspb.1983.0091
  • Dominy N.J., Lucas P.W. Ecological importance of trichromatic vision to primates. Nature. 2001. V. 410 (6826). P. 363–366. https://doi.org/10.1038/35066567
  • Dowling J.E., Boycott B.B. Organization of the primate retina: electron microscopy. Proc. R. Soc. Lond. B. Biol. Sci. 1966. V. 166 (1002). P. 80–111. https://doi.org/10.1098/rspb.1966.0086
  • Dulai K.S., von Dornum M., Mollon J.D., Hunt D.M. The evolution of trichromatic color vision by opsin gene duplication in New World and Old World primates. Genome Res. 1999. V. 9. P. 629–638. https://doi.org/10.1101/gr.9.7.629
  • Engstrom K. Cone Types and Cone Arrangement in the Retina of Some Cyprinids. Acta Zoologica. 1960. V. 41 (3). P. 277–295. https://doi.org/10.1111/j.1463-6395.1960.tb00481.x
  • Estévez O., Spekreijse H. The “silent substitution” method in visual research. Vision Research. 1982. V. 22. P. 681–69. https://doi.org/10.1016/0042-6989(82)90104-3
  • Field G.D., Gauthier J.L., Sher A., Greschner M., Machado T.A., Jepson L.H., Shlens J., Gunning D.E., Mathieson K., Dabrowski W., Paninski L., Litke A.M., Chichilnisky E.J. Functional connectivity in the retina at the resolution of photoreceptors. Nature. 2010. V. 467 (7316). P. 673–677. https://doi.org/10.1038/nature09424
  • Gehring W.J., Ikeo K. Pax 6: mastering eye morphogenesis and eye evolution. Trends in Genetics. 1999. V. 15 (9). P. 371–377. https://doi.org/10.1016/S0168-9525(99)01776-X
  • Gill J.S., Moosajee M., Dubis A.M. Cellular imaging of inherited retinal diseases using adaptive optics. Eye. 2019. V. 33. P. 1683–1698. https://doi.org/10.1038/s41433-019-0474-3
  • Govardovskii V.I., Fyhrquist N., Reuter T., Kuzmin D.G., Donner K. In search of the visual pigment template. Visual Neurosci. 2000. V. 17. P. 509–528. https://doi.org/10.1017/ S0952523800174036
  • Hampson K.M. Adaptive optics and vision. Journal of Modern Optics. 2008. V. 55. № 21. P. 3425–3467. https://doi.org/10.1080/09500340802541777
  • Hart N.S., Partridge J.C., Cuthill I.C., Bennett A.T. Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.) J. Comp. Physiol. A. 2000. V. 186 (4). P. 375–387. https://doi.org/10.1007/s003590050437
  • Hartridge H. Cluster formation by the foveal cones. J. Physiol. 1946. V. 15. P. 105.
  • Hendrickson A. Organization of the Adult Primate Fovea. Macular Degeneration. Penfold P.L., Provis J.M. (eds). Berlin, Heidelberg. Springer, 2005. https://doi.org/10.1007/3-540-26977-0_1
  • Henriques L.D., Hauzman E., Bonci D.M.O., Chang B.S.W., Muniz J.A.P.C., Souza G.S., Silveira L.C.L., Galvão O.F., Goulart P.R.K., Ventura D.F. Uniform trichromacy in Alouatta caraya and Alouatta seniculus: behavioural and genetic colour vision evaluation. Front Zool. 2021. V. 18. P. 36 (1–10). https://doi.org/10.1186/s12983-021-00421-0
  • Hillmann D., Spahr H., Pfäffle C., Sudkamp H., Franke G., Hüttmann G. In vivo optical imaging of physiological responses to photostimulation in human photoreceptors. PNAS. 2016. V. 113 (46). P. 13138–13143. https://doi.org/10.1073/pnas.1606428113
  • Hofer H., Carroll J., Neitz J., Neitz M., Williams D.R. Organization of the Human Trichromatic Cone Mosaic. J. Neurosci. 2005. V. 19 (42). P. 9669–9679. https://doi.org/10.1523/JNEUROSCI.2414-05.2005
  • Hunt D.M., Dulai K.S., Cowing J.A., Julliot C., Mollon J.D., Bowmaker J.K., Li W.-H., Hewett-Emmett D. Molecular evolution of trichromacy in primates. Vision Res. 1998. V. 38 (21). P. 3299–3306. https://doi.org/10.1016/s0042-6989(97)00443-4
  • Jacobs G.H., Neitz J., Deegan J.F. Retinal receptors in rodents maximally sensitive to ultraviolet light Nature. 1991. V. 353. P. 655–656. https://doi.org/10.1038/353655a0
  • Jacobs G.H. Evolution of colour vision in mammals. Phil. Trans. R. Soc. B. 2009. V. 364 (1531). P. 2957–2967. https://doi.org/10.1098/rstb.2009.0039
  • Jacobs G.H. Losses of functional opsin genes, short-wavelength cone photopigments, and color vision – a significant trend in the evolution of mammalian vision. Vis Neurosci. 2013. V. 30 (1–2). P. 39–53. https://doi.org/10.1017/S0952523812000429
  • Jacobs G.H., Neitz M., Neitz J. Mutations in S-cone pigment genes and the absence of colour vision in two species of nocturnal primate. Proc. R. Soc. Lond. B. 1996. V. 263 (1371). P. 705–710. https://doi.org/10.1098/rspb.1996.0105
  • Jacobs G.H., Deegan J.F.D.I. Uniformity of colour vision in Old World monkeys. Proc. Biol. Sci. 1999. V. 266 (1432). P. 2023–2028. https://doi.org/10.1098/rspb.1999.0881
  • Keeler C.R. The Ophthalmoscope in the Lifetime of Hermann von Helmholtz. Arch Ophthalmol. 2002. V. 120 (2). P. 194–201. https://doi.org/10.1001/archopht.120.2.194
  • Kling A., Field G.D., Brainard D.H., Chichilnisky E.J. Probing Computation in the Primate Visual System at Single-Cone Resolution. Annu. Rev. Neurosci. 2019. V. 42. P. 169–186. https://doi.org/10.1146/annurev-neuro-070918-050233
  • Lakowski R. Theory and practice of colour vision testing: A Review. Part 2. British Journal of Industrial Medicine. 1969. V. 26 (4). P. 265–288. https://doi.org/10.1136/oem.26.4.265
  • Lee B.B. Paths to colour in the retina. Clin. Exp.Optom. 2004. V. 87. P. 239–248. https://doi.org/10.1111/j.1444-0938.2004.tb05054.x
  • Levenson D.H., Ponganis P.J., Crognale M.A., Deegan J.F. 2nd, Dizon A., Jacobs G.H. Visual pigments of marine carnivores: pinnipeds, polar bear, and sea otter. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 2006. V. 192 (8). P. 833–843. https://doi.org/10.1007/s00359-006-0121-x
  • Li Y.N., Tsujimura T., Kawamura S., Dowling J.E. Bipolar cell-photoreceptor connectivity in the zebrafish (Danio rerio) retina. J. Comp. Neurol. 2012. V. 520 (16). P. 3786–3802. https://doi.org/10.1002/cne.23168
  • Li P.H., Field G.D., Greschner M., Ahn D., Gunning D.E., Mathieson K., Sher A., Litke A.M., Chichilnisky E.J. Retinal representation of the elementary visual signal. Neuron. 2014. V. 81 (1). P. 130–139. https://doi.org/10.1016/j.neuron.2013.10.043
  • Marc R.E. The structure of vertebrate retinas. The Retinal Basis of Vision. Toyoda J. (ed.). Amsterdam. Elsevier, 1999. P. 3–19.
  • Marks W.B. Visual pigments of single goldfish cones. J. Physiol. 1965. V. 178 (1). P. 14–32. https://doi.org/10.1113/jphysiol.1965.sp007611
  • Maximov V. Colour vision in early vertebrates. Iugoslav. Physiol. Pharmacol. Acta. 1998. V. 34 (2). P. 343–349.
  • Maximov V. Environmental factors which may have led to the appearance of colour vision. Phil. Trans. R. Soc. Lond. B. 2000. V. 355. P. 1239–1242. https://doi.org/10.1098/rstb.2000.0675
  • McGregor J.E., Yin L., Yang Q., Godat T., Huynh K.T., Zhang J., Williams D.R., Merigan W.H. Functional architecture of the foveola revealed in the living primate. PLOS ONE. 2018. V. 13 (11). P. e0207102. https://doi.org/10.1371/journal.pone.0207102
  • Merino D., Loza-Alvarez P. Adaptive optics scanning laser ophthalmoscope imaging: technology update. Clin Ophthalmol. 2016. V. 10. P. 743–755. https://doi.org/10.2147/OPTH.S64458
  • Mollon J.D., Bowmaker J.K. The spatial arrangement of cones in the primate fovea. Nature.1992. V. 360 (6405). P. 677–679. https://doi.org/10.1038/360677a0
  • Movshon A. Animal models for visual neuroscience. Journal of Vision. 2014. V. 14 (15). P. 8. https://doi.org/10.1167/14.15.8
  • Nathans J., Thomas D., Hogness D.S. Molecular genetics of human color vision: the genes encoding blue, green and red pigments. Science. 1986. V. 232 (4747). P. 193–202. https://doi.org/10.1126/science.2937147
  • Orlov O.Yu., Maximova E.M. S-potential sources as excitation pools. Vision res. 1965. V. 5. P. 573–582. https://doi.org/10.1016/0042-6989(65)90032-5
  • Peichl L., Behrmann G., Kröger R. For whales and seals the ocean is not blue: a visual pigment loss in marine mammals. Eur. J. Neurosci. 2001. V. 13. P. 1520–1528. https://doi.org/10.1046/j.0953-816x.2001.01533.x
  • Peichl L., Moutairou K. Absence of short-wavelength sensitive cones in the retinae of seals (Carnivora) and African giant rats (Rodentia). Eur. J. Neurosci. 1998. V. 10 (8). P. 2586–2594. https://doi.org/10.1046/j.1460-9568.1998.00265.x
  • Peichl L. Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? Anat Rec A Discov Mol Cell Evol Biol. 2005. V. 287 (1). P. 1001–1012. https://doi.org/10.1002/ar.a.20262
  • Polyak S.L. The Retina. Chicago, The Univercity of Chicago Press, 1941. 607 p.
  • Provis J.M., Dubis A.M., Maddess T., Carroll J. Adaptation of the central retina for high acuity vision: Cones, the fovea and the avascular zone. Prog Retin Eye Res. 2013. V. 35. P. 63–81. https://doi.org/10.1016/j.preteyeres.2013.01.005
  • Qiu Y., Zhao Z., Klindt D., Kautzky M., Szatko K.P., Schaeffel F., Rifai K., Franke K., Busse L., Euler T. Natural environment statistics in the upper and lower visual field are reflected in mouse retinal specializations. Curr Biol. 2021. V. 31 (15). P. 3233–3247. https://doi.org/10.1016/j.cub.2021.05.017
  • Ramon-Y-Cajal S. La rétine des vertébrés. Cellule. 1892. V. 9. P. 121–255.
  • Roorda A., Williams D.R. The arrangement of the three cone classes in the living human eye. Nature. 1999. V. 397 (6719). P. 520–522. https://doi.org/10.1038/17383
  • Roorda A., Metha A.B., Lennie P., Williams D.R. Packing arrangement of the three cone classes in primate retina. Vision Res. 2001. V. 41 (10–11). P. 1291–1306. https://doi.org/10.1016/s0042-6989(01)00043-8
  • Roorda A., Romero-Borja F., Donnelly W.J. III, Queener H., Hebert T.J., Campbell M. Adaptive optics scanning laser ophthalmoscopy. Opt Express. 2002. V. 10 (9). P. 405–412. https://doi.org/10.1364/OE.10.000405
  • Sabesan R., Hofer H.J., Roorda A. Characterizing the human cone photoreceptor mosaic via dynamic photopigment densitometry. PLoS One. 2015. V. 10 (12). P. e0144891. https://doi.org/10.1371/journal.pone.0144891
  • Sabesan R., Schmidt B.P., Tuten W.S., Roorda A. The elementary representation of spatial and color vision in the human retina. Sci Adv. 2016. V. 2 (9). P. e1600797. https://doi.org/10.1126/sciadv.1600797
  • Schmidt B.P., Sabesan R., Tuten W.S., Neitz J., Roorda A. Sensations from a single M-cone depend on the activity of surrounding S-cones. Scientific REPORTS. 2018. V. 8. P. 8561. https://doi.org/10.1038/s41598-018-26754-1
  • Silveira L.C.L., Saito C.A., Filho M. da S., Kremers J., Bowmaker J.K., Lee B.B. Alouatta trichromatic color vision: cone spectra and physiological responses studied with microspectrophotometry and single unit retinal electrophysiology. PLOS ONE. 2014. V. 9 (11). P. e113321. https://doi.org/10.1371/journal.pone.0113321
  • Sincich L.C., Zhang Y., Tiruveedhula P., Horton J.C., Roorda A. Resolving single cone inputs to visual receptive fields. Nat Neurosci. 2009. V. 12 (8). P. 967–969. https://doi.org/10.1038/nn.2352
  • Solomon S.G., Lennie P. The machinery of colour vision. Nat Rev Neurosci. 2007. V. 8. P. 276–286. https://doi.org/10.1038/nrn2094
  • Stieb S.M., de Busserolles F., Carleton K.L., Cortesi F., Chung W.-S., Dalton B.E., Hammond L.A., Marshall N.J. A detailed investigation of the visual system and visual ecology of the Barrier Reef anemonefish, Amphiprion akindynos. Sci Rep. 2019. V. 9. P. 16459. https://doi.org/10.1038/s41598-019-52297-0
  • Thoreson W.B., Dacey D.M. Diverse cell t`ypes, circuits, and mechanisms for color vision in the vertebrate retina. Physiol Rev. 2019. V. 99 (3). P. 1527–1573. https://doi.org/10.1152/physrev.00027.2018
  • Toomey M.B., Corbo J.C. Evolution, development and function of vertebrate cone oil droplets. Front Neural Circuits. 2017. V. 11. P. 97. https://doi.org/10.3389/fncir.2017.00097
  • Wagner-Schuman M., Neitz J., Rha J., Williams D.R., Neitz M., Carroll J. Color-deficient cone mosaics associated with Xq28 opsin mutations: A stop codon versus gene deletions. Vision Res. 2010. V. 50 (23). P. 2396–2402. https://doi.org/10.1016/j.visres.2010.09.015
  • Walls G.L. The Vertebrate Eye and Its Adaptive Radiation. Bloomfield hills, mich., cranbrook institute of science. 1942. 814 p. https://doi.org/10.5962/bhl.title.7369
  • Wikler K.C., Rakic P. Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates. J Neurosci. 1990. V. 10 (10). P. 3390–3401. https://doi.org/10.1523/JNEUROSCI.10-10-03390.1990
  • Williams D.R. Imaging single cells in the living retina. Vis. Res. 2011. V. 51 (13). P. 1379–1396. https://doi.org/10.1016/j.visres.2011.05.002
  • Williams D.R., Sekiguchi N., Haake W., Brainard D, Packer O. The cost of trichromacy for spatial vision. From Pigments to Perception: Advances in Understanding Visual Processes. Eds. Valberg A., Lee B.B. New York. Plenum Press, 1991. P. 11–22. https://doi.org/10.1007/978-1-4615-3718-2_2
  • Wilkie D., Hunt D.M., Bowmaker J.K. Visual pigments and oil droplets in the retina of a passerine bird, the canary Serinus canaria: microspectrophotometry and opsin sequences. Vis. Res. 1999. V. 39 (17). P. 2801–2815. https://doi.org/10.1016/s0042-6989(99)00023-1
  • Wiesel T.N., Hubel D.H. Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. J Neurophysiol. 1966. V. 29 (6). P. 1115–1156. https://doi.org/10.1152/jn.1966.29.6.1115
  • Yin L., Masella B., Dalkara D., Zhang J., Flannery J.G., Schaffer D.V., Williams D.R., Merigan W.H. Imaging light responses of foveal ganglion cells in the living macaque eye. J. Neurosci. 2014. V. 34 (19). P. 6596–6605. https://doi.org/10.1523/JNEUROSCI.4438-13.2014
  • Yokoyama S., Yokoyama R. Adaptive evolution of photoreceptors and visual pigments in vertebrates. Ann Rev Ecol Sys. 1996. V. 27 (1). P. 543–567. https://doi.org/10.1146/annurev.ecolsys.27.1.543
  • Yokoyama S. Molecular evolution of vertebrate visual pigments. Prog Retin Eye Res. 2000. V. 19 (4). P. 385–419. https://doi.org/10.1016/s1350-9462(00)00002-1
  • Yokoyama S. Molecular evolution of color vision in vertebrates. Gene2002. V. 300 (1–2). P. 69–78. https://doi.org/10.1016/s0378-1119(02)00845-4
  • Zeki S. and Marini L. Three cortical stages of colour processing in the human brain. Brain. 1998. V. 121. P. 1669–1685. https://doi.org/10.1093/brain/121.9.1669
  • Zhang F., Kurokawa K., Lassoued A., Crowell J.A., Miller D.T. Cone photoreceptor classification in the living human eye from photostimulation-induced phase dynamics. PNAS. 2019. V. 116(16). P. 7951–7956. https://doi.org/10.1371/journal.pone.0207102
  • Zhang F., Kurokawa K., Bernucci M.T., Jung H.W., Lassoued A., Crowell J.A., Neitz J., Neitz M., and Miller D.T. Revealing how color vision phenotype and genotype manifest in individual cone cells. Invest. Ophthalmol. Vis. Sci. 2021. V. 62 (2). Art. 8. https://doi.org/10.1167/iovs.62.2.8