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Processing of color, form, and motion in macaque area V2

Published online by Cambridge University Press:  02 June 2009

Karl R. Gegenfurtner
Affiliation:
Howard Hughes Medical Institute and Center for Neural Science, New York University, New York
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

Abstract

We investigated the representation of color in cortical area V2 of macaque monkeys, and the association of color with other stimulus attributes. We measured the selectivity of individual V2 neurons for color, motion, and form. Most neurons in V2 were orientation selective, about half of them were selective for color, and a minority of cells (about 20%) were selective for size or direction. We correlated these physiological measurements with the anatomical location of the cells with respect to the cytochrome oxidase (CO) compartments of area V2. There was a tendency for color-selective cells to be found more frequently in the thin stripes, but color-selective cells also occurred frequently in thick stripes and inter-stripes. We found no difference in the degree of color selectivity between the different CO compartments. Furthermore, there was no negative correlation between color selectivity and selectivity for other stimulus attributes. We found many cells capable of encoding information along more than one stimulus dimension, regardless of their location with respect to the CO compartments. We suggest that area V2 plays an important role in integrating information about color, motion, and form. By this integration of stimulus attributes a cue-invariant representation of the visual world might be achieved.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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References

REFERENCES

Albright, T.D. (1992). Form-cue invariant motion processing in primate visual cortex. Science 255, 11411143.CrossRefGoogle ScholarPubMed
Baizer, J.S., Robinson, D.L. & Dow, B.M. (1977). Visual responses of area 18 neurons in awake, behaving monkey. Journal of Neurophysiology 40, 10241037.CrossRefGoogle ScholarPubMed
Barlow, H.B., Blakemore, C. & Pettigrew, J.D. (1967). The neural mechanism of binocular depth discrimination. Journal of Physiology 193, 327342.CrossRefGoogle ScholarPubMed
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, 33503369.CrossRefGoogle ScholarPubMed
Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. (1992). The analysis of visual motion: A comparison of neuronal and psychophysical performance. Journal of Neuroscience 12, 47454765.CrossRefGoogle Scholar
Buchsbaum, G. & Gottschalk, A. (1983). Trichromacy, opponent colours coding and optimum colour information transmission in the retina. Proceedings of the Royal Society B (London) 220, 80113.Google 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, 23272351.CrossRefGoogle ScholarPubMed
Chaparro, A., Stromeyer, C.F. III., Huang, E.P., Kronauer, R.E. & Eskew, R.T. (1993). Colour is what the eye sees best. Nature 361, 348350.CrossRefGoogle ScholarPubMed
Cheng, K., Hasegawa, T., Saleem, K.S. & Tanaka, K. (1994). Comparison of neuronal selectivity for stimulus speed, length, and contrast in the prestriate cortical areas V4 and MT of the macaque monkey. Journal of Neurophysiology 71, 22692280.CrossRefGoogle ScholarPubMed
Derrington, A.M. & Henning, G.B. (1993). Detecting and discriminating the direction of motion of luminance and colour gratings. Vision Research 33, 799811.CrossRefGoogle ScholarPubMed
Derrington, A.M., Krauskopf, J. & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. Journal of Physiology 357, 241265.CrossRefGoogle ScholarPubMed
Desimone, R. & Schein, S.J. (1987). Visual properties of neurons in area V4 of the macaque: Sensitivity to stimulus form. Journal of Neurophysiology 57, 835868.CrossRefGoogle ScholarPubMed
De Valois, K.K. & Switkes, E. (1983). Simultaneous masking interactions between chromatic and luminance gratings. Journal of the Optical Society of America 73, 1118.CrossRefGoogle ScholarPubMed
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, 5861.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, 6781.CrossRefGoogle ScholarPubMed
Felleman, D.J. & Van Essen, D.C. (1987). Receptive field properties of neurons in area V3 of macaque monkey extrastriate cortex. Journal of Neurophysiology 57, 889920.CrossRefGoogle ScholarPubMed
Felleman, D.J. & Van Essen, D.C. (1991). Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex 1, 147.CrossRefGoogle ScholarPubMed
Ferrera, V.P., Nealey, T.A. & Maunsell, J.H.R. (1994). Responses in macaque visual area V4 following inactivation of the parvocellular and magnocellular LGN pathways. Journal of Neuroscience 14, 20802088.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, 33293349.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, 18801888.CrossRefGoogle ScholarPubMed
Gegenfurtner, K.R., Kiper, D.C., Beusmans, J., Carandini, M., Zaidi, Q. & Movshon, J.A. (1994 a). Chromatic properties of neurons in macaque MT. Visual Neuroscience 11, 455466.CrossRefGoogle ScholarPubMed
Gegenfurtner, K.R., Kiper, D.C. & Levitt, J.B. (1994 b). Analysis of color and motion in macaque area V3. Society for Neuroscience Abstracts 20, 1741.Google Scholar
Gegenfurtner, K.R. & Hawken, M.H. (1995). Temporal and chromatic properties of motion mechanisms. Vision Research 35, 15471563.CrossRefGoogle ScholarPubMed
Hawken, M.J., Gegenfurtner, K.R. & Tang, C. (1994). Contrast dependence of colour and luminance motion mechanisms in human vision. Nature 367, 268270.CrossRefGoogle ScholarPubMed
Hays, W.L. (1981). Statistics (third edition). New York: CBS College Publishing.Google Scholar
Hubel, D.H. & Livingstone, M.S. (1987). Segregation of form, color, and stereopsis in primate area 18. Journal of Neuroscience 7, 33783415.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1972). Laminar and columnar distribution of geniculo-cortical fibers in the macaque monkey. Journal of Comparative Neurology 158, 421450.CrossRefGoogle Scholar
Kaplan, E. & Shapley, R.M. (1986). The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proceedings of the National Academy of Sciences of the U.S.A. 83, 27552757.CrossRefGoogle ScholarPubMed
Komatsu, H. & Ideura, Y. (1993). Relationships between color, shape, and pattern selectivities of neurons in the inferior temporal cortex of the macaque. Journal of Neurophysiology 70, 677694.CrossRefGoogle Scholar
Krauskopf, J. & Farell, B. (1991). Vernier acuity: Effects of chromatic content, blur and contrast. Vision Research 31, 735749.CrossRefGoogle ScholarPubMed
Lachica, E.A., Beck, P.D. & Casagrande, V.A. (1992). Parallel path ways in macaque monkey striate cortex: Anatomically defined columns in layer III. Proceedings of the National Academy of Sciences of the U.S.A. 89, 35663570.CrossRefGoogle Scholar
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1981). Retinal ganglion cell classes in the old-world monkey: Morphology and central projections. Science 213, 11391142.CrossRefGoogle ScholarPubMed
Levitt, J.B., Kiper, D.C. & Movshon, J.A. (1994 a). Receptive fields and functional architecture of macaque V2. Journal of Neurophysiology 71, 25172542.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, 551570.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, 309356.CrossRefGoogle ScholarPubMed
Livingstone, M.S. & Hubel, D.H. (1987). Psychophysical evidence for separate channels for the perception of form, color, movement, and depth. Journal of Neuroscience 7, 34163468.CrossRefGoogle ScholarPubMed
Lund, J.S. (1973). Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta). Journal of Comparative Neurology 147, 455475.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, 305334.CrossRefGoogle Scholar
MacLeod, D.I.A. & Boynton, R.M. (1979). Chromaticity diagram showing cone excitation by stimuli of equal luminance. Journal of the Optical Society of America 69, 11831186.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R., Nealey, T.A. & DePriest, D.D. (1990). Magno cellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey. Journal of Neuroscience 10, 33233334.CrossRefGoogle Scholar
Metha, A.B., Vingrys, A.J. & Badcock, D.R. (1994). Detection and discrimination of moving stimuli: The effects of color, luminance, and eccentricity. Journal of the Optical Society of America A 11, 16971709.CrossRefGoogle ScholarPubMed
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, 31803191.CrossRefGoogle ScholarPubMed
Merrill, E.G. & Ainsworth, A. (1972). Glass-coated platinum-plated tungsten microelectrode. Medical and Biological Engineering 10, 495504.CrossRefGoogle Scholar
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, 20692079.CrossRefGoogle Scholar
Newsome, W.T., Wurtz, R.H., Dürsteler, M.R. & Mikami, A. (1985). Deficits in visual motion processing following ibotenic acid lesions of the middle temporal visual area of the macaque monkey. Journal of Neuroscience 5, 825840.CrossRefGoogle ScholarPubMed
Perry, V.H., Oehler, R. & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 11011123.CrossRefGoogle Scholar
Peterhans, E. & von der Heydt, R. (1989). Mechanisms of contour perception in monkey visual cortex. II. Contours bridging gaps. Journal of Neuroscience 9, 17491763.CrossRefGoogle ScholarPubMed
Peterhans, E. & von der Heydt, R. (1993). Functional organization of area V2 in the alert macaque. European Journal of Neuroscience 5, 509524.CrossRefGoogle ScholarPubMed
Poggio, G.F. & Fischer, B. (1977). Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey. Journal of Neurophysiology 40, 13921405.CrossRefGoogle ScholarPubMed
Rockland, K.S. (1985). A reticular pattern of intrinsic connections in primate area V2 (area 18). Journal of Comparative Neurology 235, 467478.CrossRefGoogle ScholarPubMed
Roe, A.W. & Ts'o, D.Y. (1993). Visual field representation within primate V2 and its relationship to the functionally distinct stripes. Investigative Ophthalmology and Visual Science (Suppl.) 34, 812.Google Scholar
Sandell, J.H. (1986). NADPH diaphorase histochemistry in the macaque striate cortex. Journal of Comparative Neurology 251, 388397.CrossRefGoogle ScholarPubMed
Sary, G., Vogels, R. & Orban, G.A. (1993). Cue-invariant shape selectivity of macaque inferior temporal neurons. Science 260, 995997.CrossRefGoogle ScholarPubMed
Schein, S.J. & Desimone, R. (1990). Spectral properties of V4 neurons in the macaque. Journal of Neuroscience 10, 33693389.CrossRefGoogle ScholarPubMed
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, 16311641.CrossRefGoogle ScholarPubMed
Schiller, P.H., Logothetis, N.K. & Charles, E.R. (1991). Parallel pathways in the visual system: Their role in perception at isoluminance. Neuropsychologia 29, 433441.CrossRefGoogle ScholarPubMed
Shapley, R. (1990). Visual sensitivity and parallel retinocortical channels. Annual Review of Psychology 41, 635658.CrossRefGoogle ScholarPubMed
Stromeyer, C.F. III., Kronauer, R.E., Ryu, A., Chaparro, A. & Eskew, R.T. (1995). Contributions of human long-wave and middle-wave cones to motion detection. Journal of Physiology 485.1, 221243.CrossRefGoogle ScholarPubMed
Switkes, E., Bradley, A. & De Valois, K.K. (1988). Contrast dependence and mechanisms of masking interactions among chromatic & luminance gratings. Journal of the Optical Society of America A 7, 11491162.CrossRefGoogle Scholar
von der Heydt, R. & Peterhans, E. (1989). Mechanisms of contour perception in monkey visual cortex. I. Lines of pattern discontinuity. Journal of Neuroscience 9, 17311748.CrossRefGoogle ScholarPubMed
Webster, M.A., De Valois, K.K. & Switkes, E. (1990). Orientation and spatial-frequency discrimination for luminance and chromatic gratings. Journal of the Optical Society of America A 7, 10341049.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, 1128.CrossRefGoogle Scholar
Würger, S.M. & Landy, M.S. (1993). Role of chromatic and luminance contrast in inferring structure from motion. Journal of the Optical Society of America A 10, 13631372.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1978). Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex. Journal of Physiology 277, 273290.CrossRefGoogle ScholarPubMed