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Chromatic properties of neurons in macaque area V2

Published online by Cambridge University Press:  02 June 2009

Daniel C. Kiper ,
Suzanne B. Fenstemaker  and
Karl R. Gegenfurtner
Daniel C. Kiper
Affiliation:
Howard Hughes Medical Institute and Center for Neural Science, New York University, New York
Suzanne B. Fenstemaker
Affiliation:
Howard Hughes Medical Institute and Center for Neural Science, New York University, New York
Karl R. Gegenfurtner
Affiliation:
Howard Hughes Medical Institute and Center for Neural Science, New York University, New York
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Abstract

We recorded from single cells in area V2 of cynomolgus monkeys using standard acute recording techniques. After measuring each cell's spatial and temporal properties, we performed several tests of its chromatic properties using sine-wave gratings modulated around a mean gray background. Most cells behaved like neurons in area V1 and their responses were adequately described by a model that assumes a linear combination of cone signals. Unlike in V1, we found a subpopulation of cells whose activity was increased or inhibited by stimuli within a narrow range of color combinations. No particular color directions were preferentially represented. V2 cells showing color specificity, including cells showing narrow chromatic tuning, were present in any of the stripe compartments, as defined by cytochrome-oxidase (CO) staining. An addition of chromatic contrast facilitated the responses of most neurons to gratings with various luminance contrasts. Neurons in all three CO compartments gave significant responses to isoluminant gratings. Receptive-field properties of cells were generally similar for luminance and chromatically defined stimuli. We found only a small number of cells with a clearly identifiable double-opponent receptive-field organization.

Keywords

Visual cortexColorV2IsoluminanceMacaque
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 6 , November 1997 , pp. 1061 - 1072
Copyright
Copyright © Cambridge University Press 1997

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References

Baizer, J.S., Robinson, D.L. & Dow, B.M. (1977). Visual responses of area 18, neurons in awake behaving monkey. Journal of Neurophysiology 40, 1024–1037.CrossRefGoogle ScholarPubMed
Barlow, H.B., Blakemore, C. & Pettigrew, J.D. (1967). The neural mechanism of binocular depth discrimination. Journal of Physiology 93, 327–342.CrossRefGoogle Scholar
Blasdel, G.G., Lund, J.S. & Fitzpatrick, D. (1985). Intrinsic connections of macaque striate cortex: Axonal projections of cells outside lamina 4C. Journal of Neuroscience 5, 3350–3369.CrossRefGoogle ScholarPubMed
Burkhalter, A. & Van Essen, D.C. (1986). Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in the macaque monkey. Journal of Neuroscience 6, 2327–2351.CrossRefGoogle ScholarPubMed
Chandler, J.P. (1969). STEPIT: Finds local minima of a smooth function of several parameters. Behavioral Science 14, 81–82.Google Scholar
Daw, N.W. (1968). Color-coded ganglion cells in the goldfish retina: Extension of their receptive field by means of new stimuli. Journal of Physiology 197, 567–592.CrossRefGoogle Scholar
de Monasterio, F.M. & Schein, S.J. (1982). Spectral bandwidths of color-opponent cells of geniculostriate pathway of macaque monkeys. Journal of Neurophysiology 47, 214–224.CrossRefGoogle Scholar
Derrington, A.M., Krauskopf, J. & Lennie, P. (1984). Chromatic mechanisms in the lateral geniculate nucleus of macaque. Journal of Physiology 357, 241–265.CrossRefGoogle ScholarPubMed
DeValois, R.L. (1965). Analysis and coding of color vision in the primate visual system. Cold Spring Harbor Symposium on Quantitative Biology 30, 567–579.CrossRefGoogle Scholar
DeYoe, E.A. & Van Essen, D.C. (1985). Segregation of efferent connections and receptive field properties in visual area V2 of the macaque. Nature 317, 58–61.CrossRefGoogle ScholarPubMed
DeYoe, E.A., Hockfield, S., Garren, H. & Van Essen, D.C. (1990). Antibody labeling of functional subdivisions in visual cortex: Cat-301 immunoreactivity in striate and extrastriate cortex of the macaque monkey. Visual Neuroscience 5, 67–81.CrossRefGoogle ScholarPubMed
Dobkins, K.R. & Albright, T.D. (1995). Behavioral and neural effects of chromatic isoluminance in the primate visual motion system. Visual Neuroscience 12, 321–332.Google ScholarPubMed
Dow, B.M. (1974). Functional classes of cells and their laminar distribution in monkey visual cortex. Journal of Neurophysiology 37, 927–946.CrossRefGoogle ScholarPubMed
Dow, B.M. & Gouras, P. (1973). Color and spatial specificity of single units in rhesus monkey foveal striate cortex. Journal of Neurophysiology 36, 79–100.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Lund, J.S. & Blasdel, G.G. (1985). Intrinsic connections of macaque striate cortex: Afferent and efferent connections of lamina 4C. Journal of Neuroscience 5, 3329–3349.CrossRefGoogle ScholarPubMed
Gegenfurtner, K.R. & Kiper, D.C. (1992). Contrast detection in luminance and chromatic noise. Journal of the Optical Society of America A 9, 1880–1888.CrossRefGoogle ScholarPubMed
Gegenfurtner, K.R., Kiper, D.C., Beusmans, J., Carandini, M., Zaidi, Q. & Movshon, J.A. (1994). Chromatic properties of neurons in macaque MT. Visual Neuroscience 11, 455–466.CrossRefGoogle ScholarPubMed
Gegenfurtner, K.R. & Hawken, M.H. (1996). Interaction of motion and color in the visual pathways. Trends in Neurosciences 19, 394–401.CrossRefGoogle ScholarPubMed
Gegenfurtner, K.R., Kiper, D.C. & Fenstemaker, S.B. (1996). Processing of color, form, and motion in macaque area V2. Visual Neuroscience 13, 161–172.CrossRefGoogle ScholarPubMed
Gershon, R., Jepson, A.D. & Tsotsos, J.K. (1986). Ambient illumination and the determination of material changes. Journal of the Optical Society of America A 3, 1700–1707.CrossRefGoogle ScholarPubMed
Gouras, P. (1974). Opponent-colour cells in different layers of foveal striate cortex. Journal of Physiology 238, 583–602.CrossRefGoogle ScholarPubMed
Healey, G. (1989). Using color for geometry-insensitive segmentation. Journal of the Optical Society of America A 6, 920–937.CrossRefGoogle Scholar
Hering, E. (1878). Zur Lehre vom Lichtsinne. Wien: Carl Gerald's Sohn.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology 195, 215–243.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Livingstone, M.S. (1987). Segregation of form, color, and stereopsis in primate area 18. Journal of Neuroscience 4, 309–356.Google Scholar
Hurvich, L.M. & Jameson, D. (1955). Some quantitative aspects of an opponent colors theory: II. Brightness, saturation, and hue in normal and dichromatic vision. Journal of the Optical Society of America 45, 602–616.CrossRefGoogle ScholarPubMed
Krauskopf, J., Williams, D.R. & Heeley, D.W. (1982). Cardinal directions of color space. Vision Research 22, 1123–1131.CrossRefGoogle ScholarPubMed
Krauskopf, J. & Gegenfurtner, K.R. (1992). Color discrimination and adaptation. Vision Research 32, 2165–2175.CrossRefGoogle ScholarPubMed
Krauskopf, J., Wu, H.J. & Farell, B. (1996). Coherence, cardinal directions and higher-order mechanisms. Vision Research 36, 1235–1245.Google ScholarPubMed
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 U.S.A. 89, 3566–3570.CrossRefGoogle ScholarPubMed
Lee, B.B., Martin, P.R. & Valberg, A. (1988). The physiological basis of heterochromatic flicker photometry demonstrated in the ganglion cells of the macaque monkey. Journal of Physiology 404, 323–347.CrossRefGoogle Scholar
Lennie, P., Krauskopf, J. & Sclar, G. (1990). Chromatic mechanisms in striate cortex of macaque. Journal of Neuroscience 10, 649–669.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Thompson, K.G., Liu, D., Zhou, Y. & Ault, S.J. (1995). Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex. Journal of Neuroscience 15, 1808–1818.CrossRefGoogle Scholar
Levitt, J.B., Kiper, D.C. & Movshon, J.A. (1994 a). Receptive fields and functional architecture of macaque V2. Journal of Neurophysiology 71, 2517–2542.CrossRefGoogle ScholarPubMed
Levitt, J.B., Yoshioka, T. & Lund, J.S. (1994 b). Intrinsic cortical connections in macaque area V2: Evidence for interaction between different functional streams. Journal of Comparative Neurology 342, 551–570.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–356.CrossRefGoogle ScholarPubMed
Lund, J.S. & Boothe, R.G. (1975). Interlaminar connections and pyramidal neuron organization in the visual cortex, area 17, of the macaque monkey. Journal of Comparative Neurology 159, 305–334.CrossRefGoogle Scholar
Merigan, W.H., Nealey, T.A. & Maunsell, J.H.R. (1993). Visual effects of lesions of cortical area V2 in macaques. Journal of Neuroscience 13, 3180–3191.CrossRefGoogle ScholarPubMed
Merrill, E.G. & Ainsworth, A. (1972). Glass-coated platinum-plated tungsten microelectrode. Medical Biology and Engineering 10, 495–504.CrossRefGoogle Scholar
Michael, C.R. (1978 a). Color vision mechanisms in monkey striate cortex: Dual-opponent cells with concentric receptive fields. Journal of Neurophysiology 41, 572–588.CrossRefGoogle ScholarPubMed
Michael, C.R. (1978 b). Color vision mechanisms in monkey striate cortex: Simple cells with dual opponent-color concentric receptive fields. Journal of Neurophysiology 41, 1233–1249.CrossRefGoogle Scholar
Michael, C.R. (1978 c). Color-sensitive complex cells in monkey striate cortex. Journal of Neurophysiology 41, 1250–1266.CrossRefGoogle ScholarPubMed
Michael, C.R. (1979). Color-sensitive hypercomplex cells in monkey striate cortex. Journal of Neurophysiology 42, 726–744.CrossRefGoogle ScholarPubMed
Nathans, J., Thomas, D. & Hogness, D.S. (1986). Molecular genetics of human color vision: The genes encoding blue, green and red pigments. Science 232, 193–202.CrossRefGoogle ScholarPubMed
Nealey, T.A. & Maunsell, J.H.R. (1994). Magnocellular and parvocellular contributions to the responses of neurons in macaque striate cortex. Journal of Neuroscience 14, 2069–2079.CrossRefGoogle Scholar
Rockland, K.S. (1985). A reticular pattern of intrinsic connections in primate area V2 (area 18). Journal of Comparative Neurology 235, 467–478.CrossRefGoogle ScholarPubMed
Roe, A. & Ts'o, D.Y. (1995). Visual topography in primate V2: Multiple representations across functional stripes. Journal of Neuroscience 15, 3689–3715.CrossRefGoogle ScholarPubMed
Rubin, J.M. & Richards, W.A. (1982). Color vision and image intensities: When are changes material? Biological Cybernetics 45, 215–226.CrossRefGoogle ScholarPubMed
Sandell, J.H. (1986). NADPH diaphorase histochemistry in the macaque striate cortex. Journal of Comparative Neurology 251, 388–397.CrossRefGoogle ScholarPubMed
Schein, S.J. & Desimone, R. (1990). Spectral properties of V4 neurons in the macaque. Journal of Neuroscience 10, 3369–3389.CrossRefGoogle ScholarPubMed
Schein, S.J., Marrocco, R.T. & de Monasterio, F.M. (1982). Is there a high concentration of color-selective cells in area V4 of monkey visual cortex? Journal of Neurophysiology 47, 193–213.CrossRefGoogle Scholar
Schiller, P.H. & Colby, C.L. (1983). The responses of single cells in the lateral geniculate nucleus of the rhesus monkey to color and luminance contrast. Vision Research 23, 1631–1641.CrossRefGoogle ScholarPubMed
Schnapf, J.L, Kraft, T.W. & Baylor, D.A. (1987). Spectral sensitivity of human cone photoreceptors. Nature 325, 439–441.CrossRefGoogle ScholarPubMed
Shapley, R. (1990). Visual sensitivity and parallel retinocortical channels. Annual Reviews of Psychology 41, 635–658.CrossRefGoogle ScholarPubMed
Shipp, S. & Zeki, S.M. (1985). Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex. Nature 315, 322–325.CrossRefGoogle ScholarPubMed
Smith, V.C. & Pokorny, J. (1975). Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm. Vision Research 15, 161–171.CrossRefGoogle Scholar
Thorell, L.G., DeValois, R.L. & Albrecht, D.G. (1984). Spatial mapping of monkey VI cells with pure color and luminance stimuli. Vision Research 24, 751–769.CrossRefGoogle Scholar
Tootell, R.B.H., Silverman, M.S., DeValois, R.L. & Jacobs, G.H. (1983). Functional organization of the second cortical visual area in primates. Science 220, 737–739.CrossRefGoogle ScholarPubMed
Ts'o, D.Y. & Gilbert, C.D. (1988). The organization of chromatic and spatial interactions in the primate striate cortex. Journal of Neuroscience 8, 1712–1727.CrossRefGoogle ScholarPubMed
Valberg, A. & Seim, T. (1983). Chromatic induction: Responses of neurophysiological double opponent units? Biological Cybernetics 46, 149–158.CrossRefGoogle ScholarPubMed
Vautin, R.G. & Dow, B.M. (1985). Color cell groups in foveal striate cortex of the behaving macaque. Journal of Neurophysiology 54, 273–292.CrossRefGoogle ScholarPubMed
Webster, M.A. & Mollon, J.D. (1991). Changes in colour appearance following post-receptoral adaptation. Nature 349, 235–238.CrossRefGoogle ScholarPubMed
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured and enucleated cat demonstrated with cytochrome oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle Scholar
Yates, J.T. (1974). Chromatic information processing in the foveal projection (area striata) of unanesthetized primate. Vision Research 14, 163–173.CrossRefGoogle ScholarPubMed
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, 467–489.CrossRefGoogle ScholarPubMed
Zaidi, Q. & Halevy, D. (1993). Visual mechanisms that signal the direction of color change. Vision Research 33, 1037–1051.CrossRefGoogle Scholar
Zeki, S.M. (1978). Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex. Journal of Physiology 277, 273–290.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1980). The representation of colours in the cerebral cortex. Nature 284, 412–418.CrossRefGoogle ScholarPubMed