I.P. Pavlov Journal of Higher Nervous ActivityI.P. Pavlov Journal of Higher Nervous ActivityЖурнал высшей нервной деятельности им. И.П. Павлова0044-46773034-5316The Russian Academy of Sciences65205210.31857/S0044467723010045GIWPTCФИЗИОЛОГИЧЕСКИЕ МЕХАНИЗМЫ ПОВЕДЕНИЯ ЖИВОТНЫХ: ВОСПРИЯТИЕ ВНЕШНИХ СТИМУЛОВ, ДВИГАТЕЛЬНАЯ АКТИВНОСТЬ, ОБУЧЕНИЕ И ПАМЯТЬФИЗИОЛОГИЧЕСКИЕ МЕХАНИЗМЫ ПОВЕДЕНИЯ ЖИВОТНЫХ: ВОСПРИЯТИЕ ВНЕШНИХ СТИМУЛОВ, ДВИГАТЕЛЬНАЯ АКТИВНОСТЬ, ОБУЧЕНИЕ И ПАМЯТЬCOLOR PERCEPTION AND ITS CODING IN SIMIAN NEOCORTEXВосприятие цвета и его кодирование в коре приматовAseyevN. A.АсеевН. А.aseyev@ihna.ruInstitute of Higher Nervous Activity and Neurophysiology of RASИнститут Высшей Нервной Деятельности и Нейрофизиологии РАН01012023731627502022025Copyright ©; 2023, Н.А. АсеевCopyright ©; 2023, Н.А. Асеев2023Н.А. АсеевН.А. Асеевhttps://innoscience.ru/0044-4677/article/view/652052

Perception of color by human and nonhuman primates is a complex problem, which is studied not only by neurophysiology, but also by neighboring fields of science such as psychophysiology, psycholinguistics, and even philosophy. With neurophysiology as a starting point, I review contributions of adjacent fields in understanding of the primates’ color space encoding. All known at the moment neurophysiologic mechanisms of color perception by primates are reviewed and a hypothetical way of color stimuli processing is proposed, suggesting at a final stage involvement of conceptual (gnostic) neurons encoding only colors of visual stimuli.

Восприятие цвета человеком и другими приматами – это комплексная задача, которую решают, помимо нейрофизиологии, и другие смежные науки, такие как психофизиология, психолингвистика и даже философия. В данном обзоре нейрофизиология зрения взята за отправную точку, рассматривается вклад всех смежных дисциплин в понимание того, как кодируется цветовое восприятие у приматов. Рассмотрены известные на данный момент нейрофизиологические механизмы восприятия цвета приматами и предлагается гипотетическая схема обработки цветовых стимулов в коре приматов, предполагающая на высшей стадии обработки стимула кодирование цвета концептуальными нейронами, отвечающими только за отражение параметра цветности зрительного стимула.

color visionperceptionprimatescodingqualianeocortexneuronцветовое зрениевосприятиекодированиеприматыквалиановая коранейронИзмайлов Ч.А., Соколов Е.Н., Черноризов А.М. Психофизиология цветового зрения. 1989, М.: Изд-во МГУ. 205 pp.Ноздрачев А.Д., Щербатых Ю.В. Физиология и психология – диалектика взаимодействия при решении психофизиологической проблемы. Рос. физиол. журн. им. И. М. Сеченова. 2021. 107 (2): 154–176.Abboud S., Hanassy S., Levy-Tzedek S., Maidenbaum S., Amedi A. EyeMusic: Introducing a “visual” colorful experience for the blind using auditory sensory substitution. Restorative Neurology and Neuroscience. 2014. 32 (2): 247–257.Afraz A., Hasantash M. Reply to Lev-Ari: Operational definition of “color perception”; which task represents the concept better? Proc Natl Acad Sci U S A. 2021. 118 (10).Arcaro M.J., Kastner S. Topographic organization of areas V3 and V4 and its relation to supra-areal organization of the primate visual system. Vis Neurosci. 2015. 32: E014.Baden T., Osorio D. The Retinal Basis of Vertebrate Color Vision. Annu Rev Vis Sci. 2019. 5: 177–200.Bannert M.M., Bartels A. Decoding the yellow of a gray banana. Curr Biol. 2013. 23 (22): 2268–2272.Bannert M.M., Bartels A. Human V4 Activity Patterns Predict Behavioral Performance in Imagery of Object Color. J Neurosci. 2018. 38 (15): 3657–3668.Berlin B., Kay P. Basic Color Terms: Their Universality and Evolution. 1969, Berkeley and Los Angeles.: University of California Press.Bird C.M., Berens S.C., Horner A.J., Franklin A. Categorical encoding of color in the brain. Proc Natl Acad Sci U S A. 2014. 111 (12): 4590–4595.Bohon K.S., Hermann K.L., Hansen T., Conway B.R. Representation of Perceptual Color Space in Macaque Posterior Inferior Temporal Cortex (the V4 Complex). eNeuro. 2016. 3 (4).Bosten J.M., Boehm A.E. Empirical evidence for unique hues? J Opt Soc Am A Opt Image Sci Vis. 2014. 31 (4): A385–393.Brainard D.H., Roorda A., Yamauchi Y., Calderone J.B., Metha A., Neitz M., Neitz J., Williams D.R., Jacobs G.H. Functional consequences of the relative numbers of L and M cones. J Opt Soc Am A Opt Image Sci Vis. 2000. 17 (3): 607–614.Brouwer G.J., Heeger D.J. Decoding and reconstructing color from responses in human visual cortex. J Neurosci. 2009. 29 (44): 13992–4003.Brouwer G.J., Heeger D.J. Categorical clustering of the neural representation of color. J Neurosci. 2013. 33 (39): 15454–15465.Buck S. L. Brown. Curr Biol. 2015. 25 (13): R536-7.Chang L., Tsao D.Y. The Code for Facial Identity in the Primate Brain. Cell. 2017. 169 (6): 1013–1028 e14.Collin S.P., Knight M.A., Davies W.L., Potter I.C., Hunt D.M., Trezise A.E. Ancient colour vision: multiple opsin genes in the ancestral vertebrates. Curr Biol. 2003. 13 (22): R864–865.Conway B.R. Color signals through dorsal and ventral visual pathways. Vis Neurosci. 2014. 31 (2): 197–209.Conway B.R. The Organization and Operation of Inferior Temporal Cortex. Annu Rev Vis Sci. 2018. 4: 381–402.Conway B.R., Hubel D.H., Livingstone M.S. Color contrast in macaque V1. Cereb Cortex. 2002. 12 (9): 915–925.Conway B.R., Livingstone M.S. Spatial and temporal properties of cone signals in alert macaque primary visual cortex. J Neurosci. 2006. 26 (42): 10 826–10 846.Conway B.R., Moeller S., Tsao D.Y. Specialized color modules in macaque extrastriate cortex. Neuron. 2007. 56 (3): 560–573.Conway B.R., Ratnasingam S., Jara-Ettinger J., Futrell R., Gibson E. Communication efficiency of color naming across languages provides a new framework for the evolution of color terms. Cognition. 2020. 195: 104086.Conway B.R., Tsao D.Y. Color-tuned neurons are spatially clustered according to color preference within alert macaque posterior inferior temporal cortex. Proc Natl Acad Sci U S A. 2009. 106 (42): 18034–18039.Cottaris N.P., De Valois R.L. Temporal dynamics of chromatic tuning in macaque primary visual cortex. Nature. 1998. 395 (6705): 896–900.Deeb S.S. Genetics of variation in human color vision and the retinal cone mosaic. Curr Opin Genet Dev. 2006. 16 (3): 301–307.Dijkstra N., Bosch S.E., van Gerven M.A.J. Shared Neural Mechanisms of Visual Perception and Imagery. Trends Cogn Sci. 2019. 23 (5): 423–434.Dumoulin S.O., Harvey B.M., Fracasso A., Zuiderbaan W., Luijten P.R., Wandell B.A., Petridou N. In vivo evidence of functional and anatomical stripe-based subdivisions in human V2 and V3. Sci Rep. 2017. 7(1): 733.Duyck M., Chang A.L.Y., Gruen T.J., Tello L.Y., Eastman S., Fuller-Deets J., Conway B.R. Color Tuning of Face-Selective Neurons in Macaque Inferior Temporal Cortex. eNeuro. 2021. 8 (2).Emery K.J., Kuppuswamy Parthasarathy M., Joyce D.S., Webster M.A. Color perception and compensation in color deficiencies assessed with hue scaling. Vision Res. 2021. 183: 1–15.Engel S., Zhang X., Wandell B. Colour tuning in human visual cortex measured with functional magnetic resonance imaging. Nature. 1997. 388 (6637): 68–71.Forder L., Bosten J., He X., Franklin A. A neural signature of the unique hues. Sci Rep. 2017. 7: 42364.Forder L., He X., Franklin A. Colour categories are reflected in sensory stages of colour perception when stimulus issues are resolved. PLoS One. 2017. 12 (5): e0178097–e0178097.Garg A.K., Li P., Rashid M.S., Callaway E.M. Color and orientation are jointly coded and spatially organized in primate primary visual cortex. Science. 2019. 364 (6447): 1275–1279.Gegenfurtner K.R., Kiper D.C., Levitt J.B. Functional properties of neurons in macaque area V3. J Neurophysiol. 1997. 77 (4): 1906–1923.Ghose G.M., Ts’o D.Y. Integration of color, orientation, and size functional domains in the ventral pathway. Neurophotonics. 2017. 4(3): 031216.Gross C.G. Genealogy of the “grandmother cell”. Neuroscientist. 2002. 8 (5): 512–518.Hadjidimitrakis K., Bakola S., Chaplin T.A., Yu H.H., Alanazi O., Chan J.M., Worthy K.H., Rosa M.G.P. Topographic Organization of the 'Third-Tier’ Dorsomedial Visual Cortex in the Macaque. J Neurosci. 2019. 39 (27): 5311–5325.Hasantash M., Afraz A. Richer color vocabulary is associated with better color memory but not color perception. Proceedings of the National Academy of Sciences. 2020. 117 (49): 31046.Hazama Y., Tamura R. Effects of self-locomotion on the activity of place cells in the hippocampus of a freely behaving monkey. Neurosci Lett. 2019. 701: 32–37.He H., Li J., Xiao Q., Jiang S., Yang Y., Zhi S. Language and Color Perception: Evidence From Mongolian and Chinese Speakers. Front Psychol. 2019. 10: 551.Hesse J.K., Tsao D.Y. A new no-report paradigm reveals that face cells encode both consciously perceived and suppressed stimuli. Elife. 2020. 9: e58360.Horwitz G.D., Hass C.A. Nonlinear analysis of macaque V1 color tuning reveals cardinal directions for cortical color processing. Nat Neurosci. 2012. 15 (6): 913–919.Isherwood Z.J., Joyce D.S., Parthasarathy M.K., Webster M.A. Plasticity in perception: insights from color vision deficiencies. Fac Rev. 2020. 9: 8.Izmailov C.A., Sokolov E.N. Spherical Model of Color and Brightness Discrimination. Psychological Science. 1991. 2 (4): 249–260.Jack B.N., Le Pelley M.E., Han N., Harris A.W.F., Spencer K.M., Whitford T.J. Inner speech is accompanied by a temporally-precise and content-specific corollary discharge. Neuroimage. 2019. 198: 170–180.Jacobs J., Weidemann C.T., Miller J.F., Solway A., Burke J.F., Wei X.X., Suthana N., Sperling M.R., Sharan A.D., Fried I., Kahana M.J. Direct recordings of grid-like neuronal activity in human spatial navigation. Nat Neurosci. 2013. 16 (9): 1188–1190.Jameson K.A., Highnote S.M., Wasserman L.M. Richer color experience in observers with multiple photopigment opsin genes. Psychon Bull Rev. 2001. 8 (2): 244–261.Jeffs J., Federer F., Ichida J.M., Angelucci A. High-resolution mapping of anatomical connections in marmoset extrastriate cortex reveals a complete representation of the visual field bordering dorsal V2. Cereb Cortex. 2013. 23 (5): 1126–47.Johnson E.N., Hawken M.J., Shapley R. The spatial transformation of color in the primary visual cortex of the macaque monkey. Nat Neurosci. 2001. 4 (4): 409–16.Josselyn S.A., Tonegawa S. Memory engrams: Recalling the past and imagining the future. Science. 2020. 367 (6473).Kay P., Berlin B., Maffi L., Merrifield WR., Cook R. The World Color Survey. 2009, Stanford: CSLI.Killian N.J., Jutras M.J., Buffalo E.A. A map of visual space in the primate entorhinal cortex. Nature. 2012. 491 (7426): 761–764.Kim I., Hong S. W., Shevell S.K., Shim W.M. Neural representations of perceptual color experience in the human ventral visual pathway. Proc Natl Acad Sci U S A. 2020. 117 (23): 13145–13150.Kiper D.C., Fenstemaker S.B., Gegenfurtner K.R. Chromatic properties of neurons in macaque area V2. Vis Neurosci. 1997. 14 (6): 1061–1072.Koch C., Massimini M., Boly M., Tononi G. Neural correlates of consciousness: progress and problems. Nat Rev Neurosci. 2016. 17 (5): 307–321.Koida K., Komatsu H. Effects of task demands on the responses of color-selective neurons in the inferior temporal cortex. Nat Neurosci. 2007. 10 (1): 108–116.Kusunoki M., Moutoussis K., Zeki S. Effect of background colors on the tuning of color-selective cells in monkey area V4. J Neurophysiol. 2006. 95 (5): 3047–3059.Lafer-Sousa R., Conway B.R. Parallel, multi-stage processing of colors, faces and shapes in macaque inferior temporal cortex. Nat Neurosci. 2013. 16 (12): 1870–1878.Lafer-Sousa R., Conway B.R., Kanwisher N.G. Color-Biased Regions of the Ventral Visual Pathway Lie between Face- and Place-Selective Regions in Humans, as in Macaques. J Neurosci. 2016. 36 (5): 1682–1697.Landisman C.E., Ts’o D.Y. Color processing in macaque striate cortex: electrophysiological properties. J Neurophysiol. 2002. 87 (6): 3138–3151.Lev-Ari S. Richer color vocabulary is correlated with color memory, but its relation to perception is unknown. Proceedings of the National Academy of Sciences. 2021. 118 (10): e2024682118.Li M., Liu F., Juusola M., Tang S. Perceptual color map in macaque visual area V4. J Neurosci. 2014. 34 (1): 202–217.Li Y., Luo H., Tian X. Mental operations in rhythm: Motor-to-sensory transformation mediates imagined singing. PLoS Biol. 2020. 18 (10): e3000504.Lim H., Wang Y., Xiao Y., Hu M., Felleman D.J. Organization of hue selectivity in macaque V2 thin stripes. J Neurophysiol. 2009. 102 (5): 2603–2615.Lindsey D.T., Brown A.M. Universality of color names. Proc Natl Acad Sci U S A. 2006. 103 (44): 16608–16613.Liu Y., Li M., Zhang X., Lu Y., Gong H., Yin J., Chen Z., Qian L., Yang Y., Andolina I.M., Shipp S., McLoughlin N., Tang S., Wang W. Hierarchical Representation for Chromatic Processing across Macaque V1, V2, and V4. Neuron. 2020. 108 (3): 538–550 e5.Martin K.A. The Pope and grandmother–a frog’s-eye view of theory. Nat Neurosci. 2000. 3 Suppl: 1169.Matsuno T., Kawai N., Matsuzawa T. Color classification by chimpanzees (Pan troglodytes) in a matching-to-sample task. Behav Brain Res. 2004. 148 (1–2): 157–165.Miller J.F., Neufang M., Solway A., Brandt A., Trippel M., Mader I., Hefft S., Merkow M., Polyn S.M., Jacobs J., Kahana M.J., Schulze-Bonhage A. Neural activity in human hippocampal formation reveals the spatial context of retrieved memories. Science. 2013. 342 (6162): 1111–1114.Mo L., Xu G., Kay P., Tan L.H. Electrophysiological evidence for the left-lateralized effect of language on preattentive categorical perception of color. Proc Natl Acad Sci USA. 2011. 108 (34): 14026–14030.Mollon J.D. Color vision: opsins and options. Proc Natl Acad Sci USA. 1999. 96 (9): 4743–4745.Mollon J.D. A neural basis for unique hues? Curr Biol. 2009. 19(11): R441-2; author reply R442-3.Morita T., Kochiyama T., Okada T., Yonekura Y., Matsumura M., Sadato N. The neural substrates of conscious color perception demonstrated using fMRI. Neuroimage. 2004. 21 (4): 1665–1673.Murphey D.K., Yoshor D., Beauchamp M.S. Perception matches selectivity in the human anterior color center. Curr Biol. 2008. 18 (3): 216–20.Nasr S., Polimeni J.R., Tootell R.B. Interdigitated Color- and Disparity-Selective Columns within Human Visual Cortical Areas V2 and V3. J Neurosci. 2016. 36 (6): 1841–1857.Nieder A. Neural constraints on human number concepts. Curr Opin Neurobiol. 2020. 60: 28–36.Nigam S., Pojoga S., Dragoi V. A distinct population of heterogeneously color-tuned neurons in macaque visual cortex. Sci Adv. 2021. 7 (8).Parkes L.M., Marsman J.B., Oxley D.C., Goulermas J.Y., Wuerger S.M. Multivoxel fMRI analysis of color tuning in human primary visual cortex. J Vis. 2009. 9 (1): 1 1–13.Persichetti A.S., Thompson-Schill S.L., Butt O.H., Brainard D.H., Aguirre G. K. Functional magnetic resonance imaging adaptation reveals a noncategorical representation of hue in early visual cortex. J Vis. 2015. 15 (6): 18.Rajaei N., Aoki N., Takahashi H.K., Miyaoka T., Kochiyama T., Ohka M., Sadato N., Kitada R. Brain networks underlying conscious tactile perception of textures as revealed using the velvet hand illusion. Hum Brain Mapp. 2018. 39 (12): 4787–4801.Rajendran S., Maule J., Franklin A., Webster M.A. Ensemble coding of color and luminance contrast. Atten Percept Psychophys. 2021. 83(3): 911–924.Regier T., Kay P. Language, thought, and color: Whorf was half right. Trends Cogn Sci. 2009. 13 (10): 439–446.Regier T., Kay P., Cook R.S. Focal colors are universal after all. Proc Natl Acad Sci USA. 2005. 102 (23): 8386–8391.Regier T., Xu Y. The Sapir-Whorf hypothesis and inference under uncertainty. Wiley Interdiscip Rev Cogn Sci. 2017. 8 (6).Rosenthal I.A., Singh S.R., Hermann K.L., Pantazis D., Conway B.R. Color Space Geometry Uncovered with Magnetoencephalography. Curr Biol. 2021. 31 (5): 1127–1128.Rowe M.H. Trichromatic color vision in primates. News Physiol Sci. 2002. 17: 93–98.Schein S.J., Desimone R. Spectral properties of V4 neurons in the macaque. J Neurosci. 1990. 10 (10): 3369–3389.Schrödinger E. What is life?: the physical aspects of the living cell (Repr. ed.). 2001: Cambridge Univ. Press.Sharpe L.T., Stockman A., Jagle H., Knau H., Klausen G., Reitner A., Nathans J. Red, green, and red-green hybrid pigments in the human retina: correlations between deduced protein sequences and psychophysically measured spectral sensitivities. J Neurosci. 1998. 18 (23): 10053–10069.Skelton A.E., Catchpole G., Abbott J.T., Bosten J.M., Franklin A. Biological origins of color categorization. Proc Natl Acad Sci U S A. 2017. 114 (21): 5545–5550.Stoughton C.M., Conway B.R. Neural basis for unique hues. Curr Biol. 2008. 18 (16): R698–699.Teichmann L., Grootswagers T., Moerel D., Carlson T.A., Rich A.N. Temporal dissociation of neural activity underlying synesthetic and perceptual colors. Proc Natl Acad Sci USA. 2021. 118(6).Thierry G., Athanasopoulos P., Wiggett A., Dering B., Kuipers J.R. Unconscious effects of language-specific terminology on preattentive color perception. Proc Natl Acad Sci U S A. 2009. 106 (11): 4567–4570.Tregillus K.E.M., Isherwood Z.J., Vanston J.E., Engel S.A., MacLeod D.I.A., Kuriki I., Webster M.A. Color Compensation in Anomalous Trichromats Assessed with fMRI. Curr Biol. 2021. 31 (5): 936–942 e4.Umbach G., Kantak P., Jacobs J., Kahana M., Pfeiffer B.E., Sperling M., Lega B. Time cells in the human hippocampus and entorhinal cortex support episodic memory. Proc Natl Acad Sci USA. 2020. 117 (45): 28463–28474.Vandenbroucke A.R.E., Fahrenfort J.J., Meuwese J.D.I., Scholte H.S., Lamme V.A.F. Prior Knowledge about Objects Determines Neural Color Representation in Human Visual Cortex. Cereb Cortex. 2016. 26 (4): 1401–1408.Vautin R.G., Dow B.M. Color cell groups in foveal striate cortex of the behaving macaque. J Neurophysiol. 1985. 54 (2): 273–292.Viénot F., Brettel H., Ott L., M’Barek A.B., Mollon J.D. What do colour-blind people see? Nature. 1995. 376 (6536): 127–128.Whitford T.J., Jack B.N., Pearson D., Griffiths O., Luque D., Harris A.W., Spencer K.M., Le Pelley M.E. Neurophysiological evidence of efference copies to inner speech. Elife. 2017. 6.Winawer J., Witthoft N., Frank M.C., Wu L., Wade A.R., Boroditsky L. Russian blues reveal effects of language on color discrimination. Proc Natl Acad Sci U S A. 2007. 104 (19): 7780–7785.Witthoft N., Winawer J., Eagleman D.M. Prevalence of learned grapheme-color pairings in a large online sample of synesthetes. PLoS One. 2015. 10(3): e0118996.Witzel C., Gegenfurtner K.R. Categorical perception for red and brown. J Exp Psychol Hum Percept Perform. 2016. 42 (4): 540–570.Witzel C., Maule J., Franklin A. Red, yellow, green, and blue are not particularly colorful. J Vis. 2019. 19 (14): 27.Wool L.E., Komban S.J., Kremkow J., Jansen M., Li X., Alonso J. M., Zaidi Q. Salience of unique hues and implications for color theory. J Vis. 2015. 15(2).Xiao Y., Casti A., Xiao J., Kaplan E. Hue maps in primate striate cortex. Neuroimage. 2007. 35 (2): 771–786.Xiao Y., Wang Y., Felleman D.J. A spatially organized representation of colour in macaque cortical area V2. Nature. 2003. 421 (6922): 535–9.Yang J., Kanazawa S., Yamaguchi M.K., Kuriki I. Cortical response to categorical color perception in infants investigated by near-infrared spectroscopy. Proc Natl Acad Sci USA. 2016. 113 (9): 2370–2375.Yasuda M., Banno T., Komatsu H. Color selectivity of neurons in the posterior inferior temporal cortex of the macaque monkey. Cereb Cortex. 2010. 20 (7): 1630–1646.Zaslavsky N., Kemp C., Regier T., Tishby N. Efficient compression in color naming and its evolution. Proc Natl Acad Sci USA. 2018. 115 (31): 7937–7942.Zeki S. The representation of colours in the cerebral cortex. Nature. 1980. 284 (5755): 412–418.