Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-23T07:11:25.309Z Has data issue: false hasContentIssue false
  • English
  • Français

Role of the color-opponent and broad-band channels in vision

Published online by Cambridge University Press:  02 June 2009

Peter H. Schiller ,
Nikos K. Logothetis  and
Eliot R. Charles
Peter H. Schiller
Affiliation:
Massachusetts Institute of Technology, Cambridge
Nikos K. Logothetis
Affiliation:
Massachusetts Institute of Technology, Cambridge
Eliot R. Charles
Affiliation:
Massachusetts Institute of Technology, Cambridge
Get access Rights & Permissions [Opens in a new window]

Abstract

The functions of the primate color-opponent and broad-band channels were assessed by examining the visual capacities of rhesus monkeys following selective lesions of parvocellular and magnocellular lateral geniculate nucleus, which respectively relay these two channels to the cortex. Parvocellular lesions impaired color vision, high spatial-frequency form vision, and fine stereopsis. Magnocellular lesions impaired high temporal- frequency flicker and motion perception but produced no deficits in stereopsis. Low spatial-frequency form vision, stereopsis, and brightness perception were unaffected by either lesion. Much as the rods and cones of the retina can be thought of as extending the range of vision in the intensity domain, we propose that the color-opponent channel extends visual capacities in the wavelength and spatial-frequency domains whereas the broad-band channel extends them in the temporal domain.

Keywords

Parallel pathwaysVisual capacityColor-opponent cellsBroad-band cells
Type
Research Article
Information
Visual Neuroscience , Volume 5 , Issue 4 , October 1990 , pp. 321 - 346
Copyright
Copyright © Cambridge University Press 1990

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bishop, P.O. (1984). Processing of visual information within the retinostriate system. Handbook of Physiology 3, 341–424.Google Scholar
Connolly, M. & Van Essen, D.C. (1984). The representation of the visual field in parvocellular and magnocellular layers of the lateral geniculate nucleus in the macaque monkey. Journal of Comparative Neurology 226, 544–564.CrossRefGoogle Scholar
De Monasterio, F.M. & Gouras, P. (1975). Functional properties of ganglion cells of the rhesus monkey retina. Journal of Physiology (London) 251, 167–195.CrossRefGoogle ScholarPubMed
De Monasterio, F.M. (1978a). Properties of concentrically organized X and Y ganglion cells of macaques. Journal of Neurophysiology 41, 1394–1417.Google Scholar
De Monasterio, F.M. (1978 b). Center and surround mechanisms of opponent-color X and Y ganglion cells of retina of macaques. Journal of Neurophysiology 41, 1418–1434.Google Scholar
Derrington, A.M., Krauskopf, J. & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. Journal of Physiology (London) 357, 241–265.CrossRefGoogle ScholarPubMed
Desimone, R., Schein, S.J., Moran, J. & Ungerleider, L.G. (1985). Contour, color, and shape analysis beyond the striate cortex. Vision Research 25, 441–;452.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, 966–977.Google Scholar
De Valois, R.L. & Jacobs, G.H. (1968). Primate color vision. Science 162, 533–540.Google Scholar
De Valois, R.L. & De Valois, K.K. (1975). Neural coding of color. Handbook of Perception, Vol. 5 ed. Carterette, E. C. & Friedman, M.P.New York: Academic Press, pp. 117–166.Google Scholar
De Yoe, E.A. & Van Essen, D.C. (1985). Segregation of efferent connections and receptive-field properties in visual areas V2 of the macaque. Nature 317, 58–61.Google Scholar
De Yoe, E.A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neurosciences 11, 219–226.CrossRefGoogle ScholarPubMed
Dreher, B., Fukada, Y. & Rodieck, R.W. (1976). Identification, classification, and anatomical segregation of cells with X-like and Y-like properties in the LGN of Old World primates. Journal of Physiology (London) 258, 433–452.CrossRefGoogle Scholar
Enroth-Cugell, C. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology (London) 187, 517–552.Google Scholar
Fries, W. (1981). The projection from the lateral geniculate nucleus to the prestriate cortex of the macaque monkey. Processing of the Royal Society B (London) 213, 73–80.Google Scholar
Gouras, P. (1969). Antidromic responses of orthodromically identified ganglion cells in monkey retina. Journal of Physiology (London) 204, 407–419.Google Scholar
Hartline, H.K. (1938). The responses of single optic fibers of the vertebrate eye to illumination of the retina. American Journal of Physiology 121, 400–415.Google Scholar
Ingling, C.R. & Grigsby, S.S. (1990). Perceptual correlates of magnocellular and parvocellular channels. Vision Research 30, 823–828.Google Scholar
Kuffler, S.W. (1953). Discharge patterns and functional organization of the mammalian retina. Journal of Neurophysiology 16, 37–68.Google Scholar
Lennie, P. (1980). Parallel visual pathways: a review. Vision Research 20, 561–564.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1981). Retinal ganglion cell classes in Old World monkey: morphology and central projections. Science 213, 1139–1142.Google Scholar
Levengstone, M.S. & Hubel, D.H. (1984). Anatomy and physiology of a color system in the primate visual system. Journal of Neuroscience 4, 309–356.CrossRefGoogle Scholar
Livingstone, M.S. & Hubel, D.H. (1987). Psychophysical evidence for separate channels for the perception of form, color, movement, and stereopsis. Journal of Neuroscience 7, 3416–3468.CrossRefGoogle Scholar
Livingstone, M.S. & Hubel, D.H. (1988). Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240, 740–749.CrossRefGoogle ScholarPubMed
Logothetis, N.K., Schiller, P.H., Charles, E.R. & Hublbert, A.C. (1990). Perceptual deficits and the activity of the color-opponent and broad-band pathways at isoluminance. Science 247, 214–217.Google Scholar
Logothetis, N.K. (1990). Use of a color monitor in vision research: calibration and color programming (submitted for publication).Google Scholar
Malpeli, J.G. & Baker, F. H. (1975). The representation of the visual field in the lateral geniculate nucleus of the Macaca mulatta. Journal of Comparative Neurology 161, 569–594.CrossRefGoogle ScholarPubMed
Martin, K.A.C. (1988). From enzymes to visual perception: a bridge too far? Trends in Neurosciences 11, 380–387.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. (1985). Physiological evidence for two visual subsystems. Matters of Intelligence (ed., Vaina, L.), 1–25.Google Scholar
Merigan, W.H. (1989). Chromatic and achromatic vision of macaques: role of the P pathway. Journal of Neuroscience 9, 776–783.Google Scholar
Mohler, C.W. & Wurtz, R.H. (1977). Role of striate cortex and superior colliculus in visual guidance of saccadic eye movements in monkeys. Journal of Neurophysiology 40, 74–94.Google Scholar
Newsome, W.T., Wurtz, R.H., Duersteller, M.R. & Mikami, A. (1985). Punctate chemical lesions of striate cortex in the macaque monkey: effects of visually guided saccades. Experimental Brain Research 58, 392–399.CrossRefGoogle ScholarPubMed
Newsome, W.T., Wurtz, R.H. (1988). Probing visual cortical function with discrete chemical lesions. Trends in Neurosciences 11, 394–400.Google Scholar
Perry, V.H. & Cowey, A. (1985). The ganglion cell and cone distributions in the monkey's retina: implications for central magnification factors. Vision Research 25, 1795–1810.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, 1101–1123.CrossRefGoogle Scholar
Purpura, K.Kaplan, E. & Shapley, R. (1988). Background light and the contrast gain of primate P and M retinal ganglion cells. Proceedings of the National Academy of Sciences of the U.S.A. 85, 4534.Google Scholar
Robinson, D.A. (1963). A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Transactions in Biomedical Electronics, 10, 137–145.Google ScholarPubMed
Schiller, P.H. (1986). The central visual system. Vision Research 26, 1351–1386.Google Scholar
Schiller, P.H. & Colby, C. (1983). The responses of single cells in the lateral geniculate nucleus of the rhesus monkey to color and luminance contrast. Visual Research 23, 1631–1641.Google ScholarPubMed
Schiller, P.H., Logothetis, N.K. & Charles, E.R. (1990 a). Functions of the color-opponent and broad-band channels of the visual system. Nature 343, 68–70.CrossRefGoogle Scholar
Schiller, P.H., Logothetis, N.K. & Charles, E.R. (1990b). Parallel pathways in the visual system: their role in perception at isoluminance. Journal of Neurophychologia (in press).Google Scholar
Schiller, P.H. & Logothetis, N.K. (1990). The color-opponent and broad-band channels of the primate visual system. Trends in Neurosciences. (in press).Google Scholar
Schiller, P.R. & Malpeli, J.G. (1977). Properties and tectal projections of the monkey retinal ganglion cells. Journal of Neurophysiology 40, 428–445.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Malpeli, J.G. (1978). Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. Journal of Neurophysiology 41, 788–797.CrossRefGoogle ScholarPubMed
Schiller, P.H., Malpeli, J.G. & Schein, (1979). Composition of geniculostriate input to superior colliculus of the rhesus monkey. Journal of Neurophysiology 42, 1124–1133.CrossRefGoogle ScholarPubMed
Schiller, P.H., Maunsel, J.H.R. & Malpeli, J.G. (1985). The effect of lateral geniculate lesions on the detection of visual stimuli. Investigative Ophthalmology and Visual Science (Suppl.) 26, 195.Google Scholar
Shapley, R.M., Kaplan, E. & Soodak, R. (1981). Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque. Nature 292, 543–545.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Perry, V.H. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in Neurosciences 9, 229–235.CrossRefGoogle Scholar
Sherman, S.M. (1985). Functional organization of the W-, X-, and Ycell pathways in the cat: a review and hypothesis. Progress in Psychobiology and Physiological Psychology 11, 233–314.Google Scholar
Stone, J. (1983). Parallel Processing in the Visual System. New York: Plenum Press.Google Scholar
Ungerleider, L.G. & Miskin, M. (1982). Two cortical visual systems. In Analysis of Visual Behavior, ed. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.W., Cambridge: MIT Press, pp. 549–586.Google Scholar
Van Essen, D.C. (1985) Functional organization of primate visual cortex. In Cerebral Cortex, ed. Peters, A. & Jones, E.G., New York: Plenum Publishing Company.Google Scholar
Watson, A.B., Nielsen, K.R.K., Poirson, A., Futzhugh, A., Bilson, A., Nuyen, K. & Aumada, A. (1986). Behavioral Research Methods Instruments and Computers 18, 587–594.Google Scholar
Waessle, H., Boycott, B.B. & Roehrenbeck, J. (1989). Horizontal cells in monkey retina: cone connections and dendritic network. European Journal of Neuroscience 1, 421–435.CrossRefGoogle Scholar
Wiesel, T.N. & Hubel, D.H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. Journal of Neurophysiology 29, 1115–1156.Google Scholar
Zeki, S. & Shipp, S. (1988). The functional logic of cortical connections. Nature 335, 311–317.Google Scholar