Normal human colour vision depends on three types of cone photoreceptors (short-, medium- and long-wavelength sensitive — S, M and L) that have different but overlapping spectral sensitivities.
Genes that code for the photosensitive pigments in L- and M-cones are juxtaposed on the X-chromosome, and are vulnerable to alteration or loss, resulting in impaired colour vision, particularly in men.
S-cones constitute 5–10% of the total number of cones; proportions of L- and M-cones vary widely among individuals, although L-cones generally predominate. Cones of the different types are randomly distributed in the mosaic, and large clusters of L- or M-cones are common.
Signals from different types of cones are combined in the retina to form cone-opponent pathways that project to the cortex, one opposing L- and M-cone signals, and others carrying strong S-cone signals variably opposed by L- and M-cone signals.
Signals regarding colour are substantially transformed on entry to the primary visual cortex, where most neurons respond weakly or not at all to pure colour variation. Neurons that respond well to colour variation have distinctive receptive fields that lack a spatially antagonistic organization.
The detection of contour and texture in coloured surfaces requires a receptive field that contains spatially distinct regions which are chromatically opponent. Neurons with such 'double-opponent' receptive fields are seldom found in the primary visual cortex, and might be more common in higher cortical areas.
Although neurons that respond well to coloured stimuli are found in multiple visual cortical areas, there is at present little evidence for a pathway that is specialized for the transmission of information about colour.
Some fundamental principles of colour vision, deduced from perceptual studies, have been understood for a long time. Physiological studies have confirmed the existence of three classes of cone photoreceptors, and of colour-opponent neurons that compare the signals from cones, but modern work has drawn attention to unexpected complexities of early organization: the proportions of cones of different types vary widely among individuals, without great effect on colour vision; the arrangement of different types of cones in the mosaic seems to be random, making it hard to optimize the connections to colour-opponent mechanisms; and new forms of colour-opponent mechanisms have recently been discovered. At a higher level, in the primary visual cortex, recent studies have revealed a simpler organization than had earlier been supposed, and in some respects have made it easier to reconcile physiological and perceptual findings.
This is a preview of subscription content, access via your institution
Open Access articles citing this article.
Brightness perception under photopic conditions: experiments and modeling with contributions of S-cone and ipRGC
Scientific Reports Open Access 04 September 2023
Zeitschrift für Arbeitswissenschaft Open Access 02 December 2022
B cell-dependent EAE induces visual deficits in the mouse with similarities to human autoimmune demyelinating diseases
Journal of Neuroinflammation Open Access 23 February 2022
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Rent or buy this article
Prices vary by article type
Prices may be subject to local taxes which are calculated during checkout
Young, T. On theory of light and colours. Phil. Trans. R. Soc. 92, 12–48 (1802).
Hering, E. Outlines of a Theory of the Light Sense (Harvard Univ. Press, Cambridge, Massachusetts, 1874/1964).
Krauskopf, J. & Gegenfurtner, K. R. Color discrimination and adaptation. Vision Res. 32, 2165–2175 (1992).
Rushton, W. A. H. Pigments and signals in colour vision. J. Physiol. 220, 1–31 (1972).
Jacobs, G. H., Deegan, J. F., Neitz, J., Crognale, M. A. & Neitz, M. Photopigments and color vision in the nocturnal monkey, Aotus. Vision Res. 33, 1773–1783 (1993).
Wald, G. The receptors of human color vision. Science 145, 1007–1016 (1964).
Neitz, M., Neitz, J. & Jacobs, G. H. Spectral tuning of pigments underlying red–green color vision. Science 252, 971–973 (1991).
Nathans, J. The evolution and physiology of human color vision: insights from molecular genetic studies of visual pigments. Neuron 24, 299–312 (1999).
Jacobs, G. H. & Rowe, M. P. Evolution of vertebrate colour vision. Clin. Exp. Optom. 87, 206–216 (2004).
Hayashi, T., Motulsky, A. G. & Deeb, S. S. Position of a 'green–red' hybrid gene in the visual pigment array determines colour-vision phenotype. Nature Genet. 22, 90–93 (1999).
Nathans, J., Thomas, D. & Hogness, D. S. Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. Science 232, 193–202 (1986). A genetic analysis of human photopigments that underpins our knowledge of the evolution of colour vision.
Neitz, J., Neitz, M., He, J. C. & Shevell, S. K. Trichromatic color vision with only two spectrally distinct photopigments. Nature Neurosci. 2, 884–888 (1999).
Carroll, J., Neitz, M., Hofer, H., Neitz, J. & Williams, D. R. Functional photoreceptor loss revealed with adaptive optics: an alternate cause of color blindness. Proc. Natl Acad. Sci. USA 101, 8461–8466 (2004).
Kremers, J., Usui, T., Scholl, H. P. & Sharpe, L. T. Cone signal contributions to electroretinograms [correction of electrograms] in dichromats and trichromats. Invest. Ophthalmol. Vis. Sci. 40, 920–930 (1999).
Jagla, W. M., Jagle, H., Hayashi, T., Sharpe, L. T. & Deeb, S. S. The molecular basis of dichromatic color vision in males with multiple red and green visual pigment genes. Hum. Mol. Genet. 11, 23–32 (2002).
Neitz, M. et al. Variety of genotypes in males diagnosed as dichromatic on a conventional clinical anomaloscope. Vis. Neurosci. 21, 205–216 (2004).
Carroll, J., Neitz, J. & Neitz, M. Estimates of L:M cone ratio from ERG flicker photometry and genetics. J. Vis. 2, 531–542 (2002).
Hofer, H., Carroll, J., Neitz, J., Neitz, M. & Williams, D. R. Organization of the human trichromatic cone mosaic. J. Neurosci. 25, 9669–9679 (2005).
Neitz, J., Carroll, J., Yamauchi, Y., Neitz, M. & Williams, D. R. Color perception is mediated by a plastic neural mechanism that is adjustable in adults. Neuron 35, 783–792 (2002). An elegant experiment showing the dependence of colour sensation on experience, and its independence from the proportions of different classes of receptors in the cone mosaic.
Berson, D. M. Strange vision: ganglion cells as circadian photoreceptors. Trends Neurosci. 26, 314–320 (2003).
Gooley, J. J., Lu, J., Fischer, D. & Saper, C. B. A broad role for melanopsin in nonvisual photoreception. J. Neurosci. 23, 7093–7106 (2003).
Dacey, D. M. et al. Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN. Nature 433, 749–754 (2005).
Curcio, C. A. et al. Distribution and morphology of human cone photoreceptors stained with anti-blue opsin. J. Comp. Neurol. 312, 610–624 (1991).
de Monasterio, F. M., Schein, S. J. & McCrane, E. P. Staining of blue-sensitive cones of the macaque retina by a fluorescent dye. Science 213, 1278–1281 (1981).
Martin, P. R. & Grunert, U. Analysis of the short wavelength-sensitive ('blue') cone mosaic in the primate retina: comparison of New World and Old World monkeys. J. Comp. Neurol. 406, 1–14 (1999).
Mollon, J. D. & Bowmaker, J. K. The spatial arrangement of cones in the primate fovea. Nature 360, 677–679 (1992).
Packer, O. S., Williams, D. R. & Bensinger, D. G. Photopigment transmittance imaging of the primate photoreceptor mosaic. J. Neurosci. 16, 2251–2260 (1996).
Roorda, A. & Williams, D. R. The arrangement of the three cone classes in the living human eye. Nature 397, 520–522 (1999). An important technical innovation — adaptive optics — allows for ultra-high resolution in vivo imaging of the photoreceptor mosaic.
Roorda, A., Metha, A. B., Lennie, P. & Williams, D. R. Packing arrangement of the three cone classes in primate retina. Vision Res. 41, 1291–1306 (2001).
Bowmaker, J. K., Parry, J. W. L. & Mollon, J. D. in Normal and Defective Colour Vision (eds Mollon, J. D., Pokorny, J. & Knoblauch, K.) 39–50 (Oxford Univ. Press, New York, 2003).
Deeb, S. S., Diller, L. C., Williams, D. R. & Dacey, D. M. Interindividual and topographical variation of L:M cone ratios in monkey retinas. J. Opt. Soc. Am. A 17, 538–544 (2000).
Hagstrom, S. A., Neitz, J. & Neitz, M. Variations in cone populations for red–green color vision examined by analysis of mRNA. Neuroreport 9, 1963–1967 (1998).
Neitz, M., Balding, S. D., McMahon, C., Sjoberg, S. A. & Neitz, J. Topography of long- and middle-wavelength sensitive cone opsin gene expression in human and Old World monkey retina. Vis. Neurosci 23, 379–385 (2006).
Hofer, H., Singer, B. & Williams, D. R. Different sensations from cones with the same photopigment. J. Vis. 5, 444–454 (2005).
Krauskopf, J. Color appearance of small stimuli and the spatial distribution of color receptors. J. Opt. Soc. Am. 54, 1171–1178 (1964).
Hurvich, L. M. & Jameson, D. An opponent-process theory of color vision. Psychol. Rev. 64, 384–404 (1957).
De Valois, R. L., Abramov, I. & Jacobs, G. H. Analysis of response patterns of LGN cells. J. Opt. Soc. Am. 56, 966–977 (1966). The first physiological study of colour opponency in neurons of the macaque LGN highlights mechanisms of the kind postulated by Hering.
Hubel, D. H. & Wiesel, T. N. Effects of varying stimulus size and color on single lateral geniculate cells in Rhesus monkeys. Proc. Natl Acad. Sci. USA 55, 1345–1346 (1966).
Derrington, A. M., Krauskopf, J. & Lennie, P. Chromatic mechanisms in lateral geniculate nucleus of macaque. J. Physiol. 357, 241–265 (1984). A quantitative analysis of responses of LGN neurons to chromatic modulation shows two distinct chromatically opponent groups.
Lankheet, M. J., Lennie, P. & Krauskopf, J. Distinctive characteristics of subclasses of red–green P-cells in LGN of macaque. Vis. Neurosci. 15, 37–46 (1998).
Smith, V. C., Lee, B. B., Pokorny, J., Martin, P. R. & Valberg, A. Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights. J. Physiol. 458, 191–221 (1992).
Rodieck, R. W. in Comparative Primate Biology Volume 4: Neurosciences (eds. Steklis, H. D. & Erwin, J.) 203–278 (Alan R. Liss, New York, 1988).
Calkins, D. J. & Sterling, P. Evidence that circuits for spatial and color vision segregate at the first retinal synapse. Neuron 24, 313–321 (1999).
Lennie, P. Parallel visual pathways: a review. Vision Res. 20, 561–594 (1980).
Paulus, W. & Kröger-Paulus, A. A new concept of retinal colour coding. Vision Res. 23, 529–540 (1983).
Shapley, R. M. & Perry, V. H. Cat and monkey retinal ganglion cells and their visual functional roles. Trends Neurosci. 9, 229–235 (1986).
Ingling, C. R. Jr & Martinez-Uriegas, E. The relationship between spectral sensitivity and spatial sensitivity for the primate r-g X-channel. Vision Res. 23, 1495–1500 (1983).
Dreher, B., Fukada, Y. & Rodieck, R. W. Identification, classification and anatomical segregation of cells with X-like and Y-like properties in the lateral geniculate nucleus of Old World primates. J. Physiol. 258, 433–452 (1976).
Mullen, K. T. & Kingdom, F. A. A. Losses in peripheral colour sensitivity predicted from 'hit and miss' post-receptoral cone connections. Vision Res. 36, 1995–2000 (1996).
Mullen, K. T. & Kingdom, F. A. Differential distributions of red-green and blue-yellow cone opponency across the visual field. Vis. Neurosci. 19, 109–118 (2002).
Calkins, D. J. & Sterling, P. Absence of spectrally specific lateral inputs to midget ganglion cells in primate retina. Nature 381, 613–615 (1996).
Dacey, D. M., Lee, B. B., Stafford, D. K., Pokorny, J. & Smith, V. C. Horizontal cells of the primate retina: cone specificity without spectral opponency. Science 271, 656–659 (1996).
Jusuf, P. R., Martin, P. R. & Grunert, U. Synaptic connectivity in the midget-parvocellular pathway of primate central retina. J. Comp. Neurol. 494, 260–274 (2006).
Dacey, D. M. Parallel pathways for spectral coding in primate retina. Ann. Rev. Neurosci. 23, 743–775 (2000).
Dacey, D. M. et al. Center-surround receptive field structure of cone bipolar cells in primate retina. Vision Res. 40, 1801–1811 (2000).
McMahon, M. J., Lankheet, M. J., Lennie, P. & Williams, D. R. Fine structure of parvocellular receptive fields in the primate fovea revealed by laser interferometry. J. Neurosci. 20, 2043–2053 (2000).
Polyak, S. L. The Retina (Univ. Chicago Press, Chicago, 1941).
Reid, R. C. & Shapley, R. M. Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus. J. Neurosci. 22, 6158–6175 (2002).
Lankheet, M. J., Lennie, P. & Krauskopf, J. Temporal–chromatic interactions in LGN P-cells. Vis. Neurosci. 15, 47–54 (1998).
Lee, B. B. & Yeh, T. Receptive fields of primate retinal ganglion cells studied with a novel technique. Vis. Neurosci. 15, 161–175 (1998).
Solomon, S. G., Lee, B. B., White, A. J., Ruttiger, L. & Martin, P. R. Chromatic organization of ganglion cell receptive fields in the peripheral retina. J. Neurosci. 25, 4527–4539 (2005).
Buzas, P., Blessing, E. M., Szmajda, B. A. & Martin, P. R. Specificity of M and L cone inputs to receptive fields in the parvocellular pathway: random wiring with functional bias. J. Neurosci. 26, 11148–11161 (2006).
Diller, L. et al. L and M cone contributions to the midget and parasol ganglion cell receptive fields of macaque monkey retina. J. Neurosci. 24, 1079–1088 (2004).
Martin, P. R., Lee, B. B., White, A. J., Solomon, S. G. & Ruttiger, L. Chromatic sensitivity of ganglion cells in the peripheral primate retina. Nature 410, 933–936 (2001).
Kouyama, N. & Marshak, D. W. Bipolar cells specific for blue cones in the macaque retina. J. Neurosci. 12, 1233–1252 (1992).
Mariani, A. P. Bipolar cells in monkey retina selective for the cones likely to be blue-sensitive. Nature 308, 184–186 (1984).
Ghosh, K. K., Martin, P. R. & Grünert, U. Morphological analysis of the blue cone pathway in the retina of a New World monkey, the marmoset Callithrix jacchus. J. Comp. Neurol. 379, 211–225 (1997).
Haverkamp, S. et al. The primordial, blue-cone color system of the mouse retina. J. Neurosci. 25, 5438–5445 (2005).
Mollon, J. D. “Tho' she kneel'd in that place where they grew...” The uses and origins of primate color vision. J. Exp. Biol 146, 21–38 (1989).
Dacey, D. M. & Lee, B. B. The 'blue-on' opponent pathway in primate retina originates from a distinct bistratified ganglion cell type. Nature 367, 731–735 (1994). The first intracellular recordings from macaque retinal ganglion cells showed that different morphological types have different chromatic properties.
Dacey, D. M., Peterson, B. B., Robinson, F. R. & Gamlin, P. D. Fireworks in the primate retina: in vitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 37, 15–27 (2003).
Hendry, S. H. C. & Reid, R. C. The koniocellular pathway in primate vision. Ann. Rev. Neurosci. 23, 127–153 (2000).
Martin, P. R., White, A. J. R., Goodchild, A. K., Wilder, H. D. & Sefton, A. E. Evidence that blue-on cells are part of the third geniculocortical pathway in primates. Eur. J. Neurosci. 9, 1536–1541 (1997).
Chatterjee, S. & Callaway, E. M. Parallel colour-opponent pathways to primary visual cortex. Nature 426, 668–671 (2003). Afferents from the LGN are recorded in V1, revealing a strict segregation of chromatic properties in the inputs to each layer.
Solomon, S. G. Striate cortex in dichromatic and trichromatic marmosets: neurochemical compartmentalization and geniculate input. J. Comp. Neurol. 450, 366–381 (2002).
Hendry, S. H. C. & Yoshioka, T. A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. Science 264, 575–577 (1994).
Derrington, A. M. & Lennie, P. Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. J. Physiol. 357, 219–240 (1984).
Chichilnisky, E. J. & Baylor, D. A. Receptive-field microstructure of blue–yellow ganglion cells in primate retina. Nature Neurosci. 2, 889–893 (1999).
Tailby, C., Solomon, S. G. & Lennie, P. Multiple S-cone pathways in the macaque visual system. COSYNE, 20 (2006).
Forte, J. D., Hashemi-Nezhad, M., Dobbie, W. J., Dreher, B. & Martin, P. R. Spatial coding and response redundancy in parallel visual pathways of the marmoset Callithrix jacchus. Vis. Neurosci. 22, 479–491 (2005).
Dacey, D. M. & Packer, O. S. Colour coding in the primate retina: diverse cell types and cone-specific circuitry. Curr. Opin. Neurobiol. 13, 421–427 (2003).
Klug, K., Herr, S., Ngo, I. T., Sterling, P. & Schein, S. Macaque retina contains an S-cone OFF midget pathway. J. Neurosci. 23, 9881–9887 (2003).
Lee, S. C., Telkes, I. & Grunert, U. S-cones do not contribute to the OFF-midget pathway in the retina of the marmoset, Callithrix jacchus. Eur. J. Neurosci. 22, 437–447 (2005).
Solomon, S. G. & Lennie, P. Chromatic gain controls in visual cortical neurons. J. Neurosci. 25, 4779–4792 (2005).
Chatterjee, S. & Callaway, E. M. S cone contributions to the magnocellular visual pathway in macaque monkey. Neuron 35, 1135–1146 (2002).
Sun, H., Smithson, H. E., Zaidi, Q. & Lee, B. B. Specificity of cone inputs to macaque retinal ganglion cells. J. Neurophysiol. 95, 837–849 (2006).
Sun, H., Smithson, H. E., Zaidi, Q. & Lee, B. B. Do magnocellular and parvocellular ganglion cells avoid short-wavelength cone input? Vis. Neurosci. 23, 441–446 (2006).
De Valois, R. L., Cottaris, N. P., Elfar, S. D., Mahon, L. E. & Wilson, J. A. Some transformations of color information from lateral geniculate nucleus to striate cortex. Proc. Natl Acad. Sci. USA 97, 4997–5002 (2000).
Valberg, A., Lee, B. B. & Tigwell, D. A. Neurones with strong inhibitory S-cone inputs in the macaque lateral geniculate nucleus. Vision Res. 26, 1061–1064 (1986).
Lennie, P., Krauskopf, J. & Sclar, G. Chromatic mechanisms in striate cortex of macaque. J. Neurosci. 10, 649–669 (1990). A comparison of chromatic properties of V1 neurons with those in the LGN, showing how colour signals are transformed.
Conway, B. R. Spatial structure of cone inputs to color cells in alert macaque primary visual cortex (V-1). J. Neurosci. 21, 2768–2783 (2001).
Conway, B. R., Hubel, D. H. & Livingstone, M. S. Color contrast in macaque V1. Cereb. Cortex 12, 915–925 (2002).
Cottaris, N. P. & De Valois, R. L. Temporal dynamics of chromatic tuning in macaque primary visual cortex. Nature 395, 896–900 (1998).
Conway, B. R. & Livingstone, M. S. Spatial and temporal properties of cone signals in alert macaque primary visual cortex. J. Neurosci. 26, 10826–10846 (2006).
Horwitz, G. D., Chichilnisky, E. J. & Albright, T. D. Blue–yellow signals are enhanced by spatiotemporal luminance contrast in macaque V1. J. Neurophysiol. 93, 2263–2278 (2005).
Johnson, E. N., Hawken, M. J. & Shapley, R. Cone inputs in macaque primary visual cortex. J. Neurophysiol. 91, 2501–2514 (2004).
Vidyasagar, T. R., Kulikowski, J. J., Lipnicki, D. M. & Dreher, B. Convergence of parvocellular and magnocellular information channels in the primary visual cortex of the macaque. Eur. J. Neurosci. 16, 945–956 (2002).
Angelucci, A. & Sainsbury, K. Contribution of feedforward thalamic afferents and corticogeniculate feedback to the spatial summation area of macaque V1 and LGN. J. Comp. Neurol. 498, 330–351 (2006).
Lennie, P. & D'Zmura, M. Mechanisms of color vision. Crit. Rev. Neurobiol. 3, 333–400 (1988).
Johnson, E. N., Hawken, M. J. & Shapley, R. The spatial transformation of color in the primary visual cortex of the macaque monkey. Nature Neurosci. 4, 409–416 (2001). An analysis of the spatial and chromatic properties of different types of receptive fields in V1.
Solomon, S. G., Peirce, J. W. & Lennie, P. The impact of suppressive surrounds on chromatic properties of cortical neurons. J. Neurosci. 24, 148–160 (2004).
Thorell, L. G., De Valois, R. L. & Albrecht, D. G. Spatial mapping of monkey V1 cells with pure color and luminance stimuli. Vision Res. 24, 751–769 (1984).
De Valois, R. L. & De Valois, K. K. A multi-stage color model. Vision Res. 33, 1053–1065 (1993). Reviews the discrepancies between known physiology and colour perception, and presents a plausible model to reconcile them.
De Valois, R. L., De Valois, K. K. & Mahon, L. E. Contribution of S opponent cells to color appearance. Proc. Natl Acad. Sci. USA 97, 512–517 (2000).
Krauskopf, J., Williams, D. R. & Heeley, D. W. Cardinal directions of color space. Vision Res. 22, 1123–1131 (1982). A seminal study that reveals through habituation three mechanisms that have a fundamental input to colour vision; the subsequent paper shows that these three mechanisms must be complemented by other, less fundamental ones.
Krauskopf, J., Williams, D. R., Mandler, M. B. & Brown, A. M. Higher order color mechanisms. Vision Res. 26, 23–32 (1986).
Carandini, M., Movshon, J. A. & Ferster, D. Pattern adaptation and cross-orientation interactions in the primary visual cortex. Neuropharmacology 37, 501–511 (1998).
Tailby, C., Solomon, S. G., Dhruv, N. T., Majaj, N. J. & Lennie, P. Habituation reveals cardinal chromatic mechanisms in striate cortex of macaque. J. Vis. 5, 80a (2005).
Solomon, S. G., Peirce, J. W., Dhruv, N. T. & Lennie, P. Profound contrast adaptation early in the visual pathway. Neuron 42, 155–162 (2004).
Cardinal, K. S. & Kiper, D. C. The detection of colored Glass patterns. J. Vis. 3, 199–208 (2003).
Mandelli, M. J. & Kiper, D. C. The local and global processing of chromatic Glass patterns. J. Vis 5, 405–416 (2005).
Bradley, A., Switkes, E. & De Valois, K. Orientation and spatial frequency selectivity of adaptation to color and luminance gratings. Vision Res. 28, 841–856 (1988).
Clifford, C. W., Spehar, B., Solomon, S. G., Martin, P. R. & Zaidi, Q. Interactions between color and luminance in the perception of orientation. J. Vis 3, 106–115 (2003).
Forte, J. D. & Clifford, C. W. Inter-ocular transfer of the tilt illusion shows that monocular orientation mechanisms are colour selective. Vision Res. 45, 2715–2721 (2005).
Daw, N. W. Goldfish retina: organization for simultaneous color contrast. Science 158, 942–944 (1967).
Livingstone, M. S. & Hubel, D. H. Anatomy and physiology of a color system in the primate visual cortex. J. Neurosci. 4, 309–356 (1984).
Desimone, R., Schein, S. J., Moran, J. & Ungerleider, L. G. Contour, color and shape analysis beyond the striate cortex. Vision Res. 25, 441–452 (1985).
Schein, S. J. & Desimone, R. Spectral properties of V4 neurons in the macaque. J. Neurosci. 10, 3369–3389 (1990).
Wachtler, T., Sejnowski, T. J. & Albright, T. D. Representation of color stimuli in awake macaque primary visual cortex. Neuron 37, 681–691 (2003).
Zeki, S. M. Colour coding in the cerebral cortex: the reaction of cells in monkey visual cortex to wavelengths and colours. Neuroscience 9, 741–765 (1983).
Zeki, S. M. Colour coding in the cerebral cortex: the responses of wavelength-selective and colour-coded cells in monkey visual cortex to changes in wavelength composition. Neuroscience 9, 767–781 (1983).
Livingstone, M. & Hubel, D. Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240, 740–749 (1988).
Shapley, R. & Hawken, M. Neural mechanisms for color perception in the primary visual cortex. Curr. Opin. Neurobiol. 12, 426–432 (2002).
Ts'o, D. Y. & Gilbert, C. D. The organization of chromatic and spatial interactions in the primate striate cortex. J. Neurosci. 8, 1712–1727 (1988).
Gegenfurtner, K. R., Kiper, D. C. & Fenstemaker, S. B. Processing of color, form, and motion in macaque area V2. Vis. Neurosci 13, 161–172 (1996).
Gegenfurtner, K. R., Kiper, D. C. & Levitt, J. B. Functional properties of neurons in macaque area V3. J. Neurophysiol. 77, 1906–1923 (1997).
Kiper, D. C., Fenstemaker, S. B. & Gegenfurtner, K. R. Chromatic properties of neurons in macaque area V2. Vis. Neurosci. 14, 1061–1072 (1997).
Moutoussis, K. & Zeki, S. Responses of spectrally selective cells in macaque area V2 to wavelengths and colors. J. Neurophysiol. 87, 2104–2112 (2002).
Kusunoki, M., Moutoussis, K. & Zeki, S. Effect of background colors on the tuning of color-selective cells in monkey area V4. J. Neurophysiol. 95, 3047–3059 (2006).
Friedman, H. S., Zhou, H. & Von Der Heydt, R. The coding of uniform colour figures in monkey visual cortex. J. Physiol. 548, 593–613 (2003).
Leventhal, A. G., Thompson, K. G., Liu, D., Zhou, Y. & Ault, S. J. Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex. J. Neurosci. 15, 1808–1818 (1995).
Hubel, D. H. & Livingstone, M. S. Segregation of form, color, and stereopsis in primate area 18. J. Neurosci. 7, 3378–3415 (1987).
Horton, J. C. & Hubel, D. H. Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762–764 (1981).
Livingstone, M. & Hubel, D. H. Thalamic inputs to cytochrome oxidase-rich regions in monkey visual cortex. Proc. Natl Acad. Sci. USA 79, 6098–6101 (1982).
Landisman, C. E. & Ts'o, D. Y. Color processing in macaque striate cortex: relationships to ocular dominance, cytochrome oxidase, and orientation. J. Neurophysiol. 87, 3126–3137 (2002).
Landisman, C. E. & Ts'o, D. Y. Color processing in macaque striate cortex: electrophysiological properties. J. Neurophysiol. 87, 3138–3151 (2002).
Kingdom, F. A. & Simmons, D. R. Stereoacuity and colour contrast. Vision Res. 36, 1311–1319 (1996).
Krauskopf, J. & Forte, J. D. Influence of chromaticity on vernier and stereo acuity. J. Vis. 2, 645–652 (2002).
Livingstone, M. S. & Hubel, D. H. Psychophysical evidence for separate channels for the perception of form, color, movement, and depth. J. Neurosci. 7, 3416–3468 (1987). Outlines the strong hypothesis of vision as a serial, parallel and hierarchical process.
Ikeda, M. & Nakashima, Y. Wavelength difference limit for binocular color fusion. Vision Res. 20, 693–697 (1980).
Simmons, D. R. The binocular combination of chromatic contrast. Perception 34, 1035–1042 (2005).
Peirce, J. W., Solomon, S. G., Forte, J., Krauskopf, J. & Lennie, P. Chromatic tuning of binocular neurons in early visual cortex. J. Vis. 3, 24a (2003).
Cumming, B. G. & DeAngelis, G. C. The physiology of stereopsis. Ann. Rev. Neurosci. 24, 203–238 (2001).
Gur, M. & Snodderly, D. M. A dissociation between brain activity and perception: chromatically opponent cortical neurons signal chromatic flicker that is not perceived. Vision Res. 37, 377–382 (1997).
Shady, S. & MacLeod, D. I. Color from invisible patterns. Nature Neurosci. 5, 729–730 (2002).
Shady, S., MacLeod, D. I. & Fisher, H. S. Adaptation from invisible flicker. Proc. Natl Acad. Sci. USA 101, 5170–5173 (2004).
Gallant, J. L., Braun, J. & Van Essen, D. C. Selectivity for polar, hyperbolic, and Cartesian gratings in macaque visual cortex. Science 259, 100–103 (1993).
Tootell, R. B., Nelissen, K., Vanduffel, W. & Orban, G. A. Search for color 'center(s)' in macaque visual cortex. Cereb. Cortex 14, 353–363 (2004).
Bouvier, S. E. & Engel, S. A. Behavioral deficits and cortical damage loci in cerebral achromatopsia. Cereb. Cortex 16, 183–191 (2006).
Damasio, A., Yamada, T., Damasio, H., Corbett, J. & McKee, J. Central achromatopsia: behavioral, anatomic, and physiologic aspects. Neurology 30, 1064–1071 (1980).
Ruttiger, L. et al. Selective color constancy deficits after circumscribed unilateral brain lesions. J. Neurosci. 19, 3094–3106 (1999).
Zeki, S. A century of cerebral achromatopsia. Brain 113, 1721–1777 (1990).
Brewer, A. A., Liu, J., Wade, A. R. & Wandell, B. A. Visual field maps and stimulus selectivity in human ventral occipital cortex. Nature Neurosci. 8, 1102–1109 (2005). A convincing analysis of the functional specialization of early extrastriate cortical areas.
Hadjikhani, N., Liu, A. K., Dale, A. M., Cavanagh, P. & Tootell, R. B. Retinotopy and color sensitivity in human visual cortical area V8. Nature Neurosci. 1, 235–241 (1998).
McKeefry, D. J. & Zeki, S. The position and topography of the human colour centre as revealed by functional magnetic resonance imaging. Brain 120, 2229–2242 (1997).
Engel, S. A. & Furmanski, C. S. Selective adaptation to color contrast in human primary visual cortex. J. Neurosci. 21, 3949–3954 (2001).
Engel, S. A. Adaptation of oriented and unoriented color-selective neurons in human visual areas. Neuron 45, 613–623 (2005).
Liu, J. & Wandell, B. A. Specializations for chromatic and temporal signals in human visual cortex. J. Neurosci. 25, 3459–3468 (2005).
Smallwood, P. M., Wang, Y. & Nathans, J. Role of a locus control region in the mutually exclusive expression of human red and green cone pigment genes. Proc. Natl Acad. Sci. USA 99, 1008–1011 (2002).
Smallwood, P. M. et al. Genetically engineered mice with an additional class of cone photoreceptors: implications for the evolution of color vision. Proc. Natl Acad. Sci. USA 100, 11706–11711 (2003).
Newsome, W. T., Britten, K. H. & Movshon, J. A. Neuronal correlates of a perceptual decision. Nature 341, 52–54 (1989).
Salzman, C. D., Britten, K. H. & Newsome, W. T. Cortical microstimulation influences perceptual judgements of motion direction. Nature 346, 174–177 (1990).
Sincich, L. C., Park, K. F., Wohlgemuth, M. J. & Horton, J. C. Bypassing V1: a direct geniculate input to area MT. Nature Neurosci. 7, 1123–1128 (2004).
MacLeod, D. I. & Boynton, R. M. Chromaticity diagram showing cone excitation by stimuli of equal luminance. J. Opt. Soc. Am. 69, 1183–1186 (1979). Describes a simple colour space, which has become standard, where hue is defined in a plane formed by two axes — one of S-cone activation and another of differential L- and M-cone activation.
Webb, B. S., Dhruv, N. T., Solomon, S. G., Tailby, C. & Lennie, P. Early and late mechanisms of surround suppression in striate cortex of macaque. J. Neurosci. 25, 11666–11675 (2005).
We thank N. Dhruv, J. Forte, J. Krauskopf, J. Peirce and C. Tailby for help in experiments and analysis, and for many discussions, over several years, at the Center for Neural Science, New York University, USA. We are grateful to H. Hofer and D. Williams for providing the mosaics of Figure 1; N. Gilroy, E. Weston and A. White also commented on the figures. Supporting grants were made to S.G.S. from the National Institutes of Health, and the Australian National Health and Medical Research Council.
The authors declare no competing financial interests.
A G protein membrane-bound receptor usually found in rod and cone photoreceptors that initiates phototransduction. Its spectral sensitivity depends on the sequence of amino acids.
A molecule, or part of one, that changes conformation upon absorbing light, inducing a conformational change in the opsin bound to it and thereby triggering phototransduction.
- Crossing over
During meiosis, two like-chromosomes can both break; each can reconnect with the fragment from the other, exchanging genes or parts of genes in the process.
Small deviations of colour vision from the normal observer (often only revealed in tasks requiring fine discriminations) brought about by mutations that shift the spectral sensitivity of the M-cone opsin.
Small deviations of colour vision from the normal observer (often only revealed in tasks requiring fine discriminations) brought about by mutations that shift the spectral sensitivity of the L-cone opsin.
Formless fields of light, and ineffective stimuli for ganglion cells driven by photoreceptors.
- Receptive fields
The region of visual space (or, equivalently, an area on the retinal surface) where presentation of an appropriate pattern of light causes changes in the activity of a neuron.
- Contrast adaptation
The change in sensitivity (of human perception, or of individual neurons) to stimulus contrast that results from prolonged exposure to modulation of a visual stimulus.
The capacity to determine the distance to a surface through the comparison of the disparate images formed in the two eyes.
About this article
Cite this article
Solomon, S., Lennie, P. The machinery of colour vision. Nat Rev Neurosci 8, 276–286 (2007). https://doi.org/10.1038/nrn2094
This article is cited by
Brightness perception under photopic conditions: experiments and modeling with contributions of S-cone and ipRGC
Scientific Reports (2023)
A diagnostic model based on color vision examination for dysthyroid optic neuropathy using Hardy-Rand-Rittler color plates
Graefe's Archive for Clinical and Experimental Ophthalmology (2023)
The Contribution of Adaptive Optics to Our Understanding of the Mechanisms of Color Vision in Humans
Neuroscience and Behavioral Physiology (2023)
Zeitschrift für Arbeitswissenschaft (2023)
B cell-dependent EAE induces visual deficits in the mouse with similarities to human autoimmune demyelinating diseases
Journal of Neuroinflammation (2022)