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Processing of the S-cone signals in the early visual cortex of primates

Published online by Cambridge University Press:  13 August 2013

Youping Xiao*
Affiliation:
Department of Neuroscience, Mount Sinai School of Medicine, New York, New York
*
*Address correspondence to: Youping Xiao, Department of Neuroscience, Mount Sinai School of Medicine, New York, NY.

Abstract

The short-wavelength-sensitive (S) cones play an important role in color vision of primates, and may also contribute to the coding of other visual features, such as luminance and motion. The color signals carried by the S cones and other cone types are largely separated in the subcortical visual pathway. Studies on nonhuman primates or humans have suggested that these signals are combined in the striate cortex (V1) following a substantial amplification of the S-cone signals in the same area. In addition to reviewing these studies, this review describes the circuitry in V1 that may underlie the processing of the S-cone signals and the dynamics of this processing. It also relates the interaction between various cone signals in V1 to the results of some psychophysical and physiological studies on color perception, which leads to a discussion of a previous model, in which color perception is produced by a multistage processing of the cone signals. Finally, I discuss the processing of the S-cone signals in the extrastriate area V2.

Type
Review Articles
Copyright
Copyright © Cambridge University Press 2013 

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References

Benevento, L.A. & Yoshida, K. (1981). The afferent and efferent organization of the lateral geniculo-prestriate pathways in the macaque monkey. The Journal of Comparative Neurology 203, 455474.CrossRefGoogle ScholarPubMed
Brouwer, G.J. & Heeger, D.J. (2009). Decoding and reconstructing color from responses in human visual cortex. The Journal of Neuroscience 29, 1399214003.CrossRefGoogle ScholarPubMed
Bullier, J. & Kennedy, H. (1983). Projection of the lateral geniculate nucleus onto cortical area V2 in the macaque monkey. Experimental Brain Research 53, 168172.Google Scholar
Buzas, P., Szmajda, B.A., Hashemi-Nezhad, M., Dreher, B. & Martin, P.R. (2008). Color signals in the primary visual cortex of marmosets. Journal of Vision 8, 116.CrossRefGoogle ScholarPubMed
Casagrande, V.A. (1994). A third parallel visual pathway to primate area V1. Trends in Neurosciences 17, 305310.Google Scholar
Cecchi, G.A., Rao, A.R., Xiao, Y. & Kaplan, E. (2010). Statistics of natural scenes and cortical color processing. Journal of Vision 10, 21.Google Scholar
Chatterjee, S. & Callaway, E.M. (2002). S cone contributions to the magnocellular visual pathway in macaque monkey. Neuron 35, 11351146.Google Scholar
Chatterjee, S. & Callaway, E.M. (2003). Parallel colour-opponent pathways to primary visual cortex. Nature 426, 668671.Google Scholar
Chatterjee, S., Ohki, K. & Reid, R.C. (2008). Functional micro-architecture of color selectivity in macaque primary visual cortex. Soc. Neurosci Abstr. 34.Google Scholar
Conway, B.R. (2001). Spatial structure of cone inputs to color cells in alert macaque primary visual cortex (V-1). The Journal of Neuroscience 21, 27682783.Google Scholar
Conway, B.R., Chatterjee, S., Field, G.D., Horwitz, G.D., Johnson, E.N., Koida, K. & Mancuso, K. (2010). Advances in color science: From retina to behavior. The Journal of Neuroscience 30, 1495514963.Google Scholar
Conway, B.R. & Livingstone, M.S. (2006). Spatial and temporal properties of cone signals in alert macaque primary visual cortex. The Journal of Neuroscience 26, 1082610846.CrossRefGoogle ScholarPubMed
Conway, B.R., Moeller, S. & Tsao, D.Y. (2007). Specialized color modules in macaque extrastriate cortex. Neuron 56, 560573.Google Scholar
Cottaris, N.P. & De Valois, R.L. (1998). Temporal dynamics of chromatic tuning in macaque primary visual cortex. Nature 395, 896900.Google Scholar
D’Souza, D.V., Auer, T., Strasburger, H., Frahm, J. & Lee, B.B. (2011). Temporal frequency and chromatic processing in humans: An fMRI study of the cortical visual areas. Journal of Vision 11.Google ScholarPubMed
De Valois, R.L. (1965). Analysis and coding of color vision in the primate visual system. Cold Spring Harbor Symposia on Quantitative Biology 30, 567579.Google Scholar
De Valois, R.L., Abramov, I. & Jacobs, G.H. (1966). Analysis of response patterns of LGN cells. Journal of the Optical Society of America 56, 966977.Google Scholar
De Valois, R.L., Cottaris, N.P., Elfar, S.D., Mahon, L.E. & Wilson, J.A. (2000). Some transformations of color information from lateral geniculate nucleus to striate cortex. Proceedings of the National Academy of Sciences of the United States of America 97, 49975002.Google Scholar
De Valois, R.L. & De Valois, K.K. (1993). A multi-stage color model. Vision Research 33, 10531065.CrossRefGoogle ScholarPubMed
De Valois, R.L., De Valois, K.K., Switkes, E. & Mahon, L. (1997). Hue scaling of isoluminant and cone-specific lights. Vision Research 37, 885897.CrossRefGoogle ScholarPubMed
DeMonasterio, F.M., Schein, S.J. & McCrane, E.P. (1981). Staining of blue-sensitive cones of the macaque retina by a fluorescent dye. Science 213, 12781281.Google Scholar
Eskew, R.T. Jr. (2009). Higher order color mechanisms: A critical review. Vision Research 49, 26862704.Google Scholar
Fitzpatrick, D., Itoh, K. & Diamond, I.T. (1983). The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). The Journal of Neuroscience 3, 673702.CrossRefGoogle ScholarPubMed
Gegenfurtner, K.R. (2003). Cortical mechanisms of colour vision. Nature Reviews. Neuroscience 4, 563572.Google Scholar
Gegenfurtner, K.R. & Hawken, M.J. (1995). Temporal and chromatic properties of motion mechanisms. Vision Research 35, 15471563.Google Scholar
Gegenfurtner, K.R. & Kiper, D.C. (2003). Color vision. Annual Review of Neuroscience 26, 181206.CrossRefGoogle ScholarPubMed
Goddard, E., Mannion, D.J., McDonald, J.S., Solomon, S.G. & Clifford, C.W. (2010). Combination of subcortical color channels in human visual cortex. Journal of Vision 10, 25.CrossRefGoogle ScholarPubMed
Hashemi-Nezhad, M., Blessing, E.M., Dreher, B. & Martin, P.R. (2008). Segregation of short-wavelength sensitive (“blue”) cone signals among neurons in the lateral geniculate nucleus and striate cortex of marmosets. Vision Research 48, 26042614.Google Scholar
Hass, C.A. & Horwitz, G.D. (2013). V1 mechanisms underlying chromatic contrast detection. Journal of Neurophysiology.Google Scholar
Hendry, S.H. & Reid, R.C. (2000). The koniocellular pathway in primate vision. Annual Review of Neuroscience 23, 127153.Google Scholar
Hendry, S.H. & Yoshioka, T. (1994). A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. Science 264, 575577.Google Scholar
Horton, J.C. (1984). Cytochrome oxidase patches: A new cytoarchitectonic feature of monkey visual cortex. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 304, 199253.Google Scholar
Horwitz, G.D., Chichilnisky, E.J. & Albright, T.D. (2007). Cone inputs to simple and complex cells in V1 of awake macaque. Journal of Neurophysiology 97, 30703081.CrossRefGoogle ScholarPubMed
Hubener, M. & Bolz, J. (1992). Relationships between dendritic morphology and cytochrome oxidase compartments in monkey striate cortex. The Journal of Comparative Neurology 324, 6780.Google Scholar
Johnson, E.N., Hawken, M.J. & Shapley, R. (2004). Cone inputs in macaque primary visual cortex. Journal of Neurophysiology 91, 25012514.CrossRefGoogle ScholarPubMed
Johnson, E.N., Hawken, M.J. & Shapley, R. (2008). The orientation selectivity of color-responsive neurons in macaque V1. The Journal of Neuroscience 28, 80968106.Google Scholar
Johnson, E.N., Van Hooser, S.D. & Fitzpatrick, D. (2010). The representation of S-cone signals in primary visual cortex. The Journal of Neuroscience 30, 1033710350.Google Scholar
Kiper, D.C., Fenstemaker, S.B. & Gegenfurtner, K.R. (1997). Chromatic properties of neurons in macaque area V2. Visual Neuroscience 14, 10611072.Google Scholar
Krauskopf, J., Williams, D.R. & Heeley, D.W. (1982). Cardinal directions of color space. Vision Research 22, 11231131.Google Scholar
Lachica, E.A., Beck, P.D. & Casagrande, V.A. (1992). Parallel pathways in macaque monkey striate cortex: Anatomically defined columns in layer III. Proceedings of the National Academy of Sciences of the United States of America 89, 35663570.Google Scholar
Lennie, P., Krauskopf, J. & Sclar, G. (1990). Chromatic mechanisms in striate cortex of macaque. The Journal of Neuroscience 10, 649669.Google Scholar
Lennie, P. & Movshon, J.A. (2005). Coding of color and form in the geniculostriate visual pathway (invited review). Journal of the Optical Society of America A, Optics and Image Science 22, 20132033.Google Scholar
Lindsey, D.T. & Brown, A.M. (2006). Universality of color names. Proceedings of the National Academy of Sciences of the United States of America 103, 1660816613.CrossRefGoogle ScholarPubMed
Liu, J. & Wandell, B.A. (2005). Specializations for chromatic and temporal signals in human visual cortex. The Journal of Neuroscience 25, 34593468.Google Scholar
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. The Journal of Neuroscience 4, 309356.Google Scholar
Lu, H.D. & Roe, A.W. (2008). Functional organization of color domains in V1 and V2 of macaque monkey revealed by optical imaging. Cerebral Cortex 18, 516533.CrossRefGoogle ScholarPubMed
Lysakowski, A., Standage, G.P. & Benevento, L.A. (1988). An investigation of collateral projections of the dorsal lateral geniculate nucleus and other subcortical structures to cortical areas V1 and V4 in the macaque monkey: A double label retrograde tracer study. Experimental Brain Research 69, 651661.Google Scholar
Malach, R. (1992). Dendritic sampling across processing streams in monkey striate cortex. The Journal of Comparative Neurology 315, 303312.Google Scholar
Martin, P.R. & Grunert, U. (1999). Analysis of the short wavelength-sensitive (“blue”) cone mosaic in the primate retina: Comparison of New World and Old World monkeys. The Journal of Comparative Neurology 406, 114.Google Scholar
Mullen, K.T., Dumoulin, S.O., McMahon, K.L., de Zubicaray, G.I. & Hess, R.F. (2007). Selectivity of human retinotopic visual cortex to S-cone-opponent, L/M-cone-opponent and achromatic stimulation. The European Journal of Neuroscience 25, 491502.Google Scholar
Mullen, K.T., Thompson, B. & Hess, R.F. (2010). Responses of the human visual cortex and LGN to achromatic and chromatic temporal modulations: An fMRI study. Journal of Vision 10, 13.Google Scholar
Murphey, D.K., Yoshor, D. & Beauchamp, M.S. (2008). Perception matches selectivity in the human anterior color center. Current Biology: CB 18, 216220.Google Scholar
Nascimento, S.M., Ferreira, F.P. & Foster, D.H. (2002). Statistics of spatial cone-excitation ratios in natural scenes. Journal of the Optical Society of America A, Optics and Image Science 19, 14841490.Google Scholar
Nathans, J. (1999). The evolution and physiology of human color vision: Insights from molecular genetic studies of visual pigments. Neuron 24, 299312.Google Scholar
Parkes, L.M., Marsman, J.B., Oxley, D.C., Goulermas, J.Y. & Wuerger, S.M. (2009). Multivoxel fMRI analysis of color tuning in human primary visual cortex. Journal of Vision 9, 113.Google Scholar
Roe, A.W. & Ts’o, D.Y. (1995). Visual topography in primate V2: Multiple representation across functional stripes. The Journal of Neuroscience 15, 36893715.Google Scholar
Ruderman, D.L., Cronin, T.W. & Chiao, C.C. (1998). Statistics of cone responses to natural images: Implications for visual coding. Journal of the Optical Society of America A, Optics and Image Science 15, 20362045.Google Scholar
Sawatari, A. & Callaway, E.M. (2000). Diversity and cell type specificity of local excitatory connections to neurons in layer 3B of monkey primary visual cortex. Neuron 25, 459471.Google Scholar
Seidemann, E., Poirson, A.B., Wandell, B.A. & Newsome, W.T. (1999). Color signals in area MT of the macaque monkey. Neuron 24, 911917.Google Scholar
Shapley, R. & Hawken, M.J. (2011). Color in the cortex: Single- and double-opponent cells. Vision Research 51, 701717.Google Scholar
Shipp, S. & Zeki, S. (2002). The functional organization of area V2, I: Specialization across stripes and layers. Visual Neuroscience 19, 187210.CrossRefGoogle ScholarPubMed
Sincich, L.C. & Horton, J.C. (2002). Divided by cytochrome oxidase: A map of the projections from v1 to v2 in macaques. Science 295, 17341737.Google Scholar
Sincich, L.C., Park, K.F., Wohlgemuth, M.J. & Horton, J.C. (2004). Bypassing V1: A direct geniculate input to area MT. Nature Neuroscience 7, 11231128.Google Scholar
Smithson, H.E. & Mollon, J.D. (2004). Is the S-opponent chromatic sub-system sluggish? Vision Research 44, 29192929.Google Scholar
Solomon, S.G. & Lennie, P. (2005). Chromatic gain controls in visual cortical neurons. The Journal of Neuroscience 25, 47794792.CrossRefGoogle ScholarPubMed
Solomon, S.G., Peirce, J.W. & Lennie, P. (2004). The impact of suppressive surrounds on chromatic properties of cortical neurons. The Journal of Neuroscience 24, 148160.Google Scholar
Stockman, A., MacLeod, D.I. & DePriest, D.D. (1991). The temporal properties of the human short-wave photoreceptors and their associated pathways. Vision Research 31, 189208.Google Scholar
Stoughton, C.M., Lafer-Sousa, R., Gagin, G. & Conway, B.R. (2012). Psychophysical chromatic mechanisms in macaque monkey. The Journal of Neuroscience 32, 1521615226.Google Scholar
Sumner, P., Anderson, E.J., Sylvester, R., Haynes, J.D. & Rees, G. (2008). Combined orientation and colour information in human V1 for both L-M and S-cone chromatic axes. Neuroimage 39, 814824.CrossRefGoogle Scholar
Sun, H., Smithson, H.E., Zaidi, Q. & Lee, B.B. (2006). Do magnocellular and parvocellular ganglion cells avoid short-wavelength cone input? Visual Neuroscience 23, 441446.Google Scholar
Tailby, C., Solomon, S.G., Dhruv, N.T. & Lennie, P. (2008 a). Habituation reveals fundamental chromatic mechanisms in striate cortex of macaque. The Journal of Neuroscience 28, 11311139.Google Scholar
Tailby, C., Solomon, S.G. & Lennie, P. (2008 b). Functional asymmetries in visual pathways carrying S-cone signals in macaque. The Journal of Neuroscience 28, 40784087.Google Scholar
Tanigawa, H., Lu, H.D. & Roe, A.W. (2010). Functional organization for color and orientation in macaque V4. Nature Neuroscience 13, 15421548.Google Scholar
Tootell, R.B., Nelissen, K., Vanduffel, W. & Orban, G.A. (2004). Search for color ‘center(s)’ in macaque visual cortex. Cerebral Cortex 14, 353363.Google Scholar
Tootell, R.B., Silverman, M.S., De Valois, R.L. & Jacobs, G.H. (1983). Functional organization of the second cortical visual area in primates. Science 220, 737739.Google Scholar
Ts’o, D.Y. & Gilbert, C.D. (1988). The organization of chromatic and spatial interactions in the primate striate cortex. The Journal of Neuroscience 8, 17121727.Google Scholar
Valverde Salzmann, M.F., Bartels, A., Logothetis, N.K. & Schuz, A. (2012). Color blobs in cortical areas V1 and V2 of the new world monkey Callithrix jacchus, revealed by non-differential optical imaging. The Journal of Neuroscience 32, 78817894.Google Scholar
Wachtler, T., Sejnowski, T.J. & Albright, T.D. (2003). Representation of color stimuli in awake macaque primary visual cortex. Neuron 37, 681691.Google Scholar
Weller, R.E., Steele, G.E. & Kaas, J.H. (2002). Pulvinar and other subcortical connections of dorsolateral visual cortex in monkeys. The Journal of Comparative Neurology 450, 215240.Google Scholar
Wikler, K.C. & Rakic, P. (1990). Distribution of photoreceptor subtypes in the retina of diurnal and nocturnal primates. The Journal of Neuroscience 10, 33903401.Google Scholar
Xiao, B. & Wade, A.R. (2010). Measurements of long-range suppression in human opponent S-cone and achromatic luminance channels. Journal of Vision 10, 10.Google Scholar
Xiao, Y., Casti, A., Xiao, J. & Kaplan, E. (2007). Hue maps in primate striate cortex. Neuroimage 35, 771786.Google Scholar
Xiao, Y. & Felleman, D.J. (2004). Projections from primary visual cortex to cytochrome oxidase thin stripes and interstripes of macaque visual area 2. Proceedings of the National Academy of Sciences of the United States of America 101, 71477151.Google Scholar
Xiao, Y., Kavanau, C., Bertin, L. & Kaplan, E. (2011). The biological basis of a universal constraint on color naming: Cone contrasts and the two-way categorization of colors. PLoS One 6, e24994.Google Scholar
Xiao, Y., Wang, Y. & Felleman, D.J. (2003). A spatially organized representation of colour in macaque cortical area V2. Nature 421, 535539.Google Scholar
Yoshioka, T., Levitt, J.B. & Lund, J.S. (1994). Independence and merger of thalamocortical channels within macaque monkey primary visual cortex: Anatomy of interlaminar projections. Visual Neuroscience 11, 467489.Google Scholar
Zeki, S. (1980). The representation of colours in the cerebral cortex. Nature 284, 412418.Google Scholar