Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-18T18:16:41.809Z Has data issue: false hasContentIssue false

Ocular dominance and disparity coding in cat visual cortex

Published online by Cambridge University Press:  02 June 2009

Simon LeVay
Affiliation:
Robert Bosch Vision Research Center, The Salk Institute for Biological Studies, San Diego
Thomas Voigt
Affiliation:
Robert Bosch Vision Research Center, The Salk Institute for Biological Studies, San Diego

Abstract

The orientation selectivity, ocular dominance, and binocular disparity tuning of 272 cells in areas 17 and 18 of barbiturate-anesthetized, paralyzed cats were studied with automated, quantitative techniques. Disparity was varied along the axis orthogonal to each cell's best orientation. Binocular correspondence was established by means of a reference electrode positioned at the boundary of lamina A and Al in the area centralis representation of the lateral geniculate nucleus. Measures were derived that expressed each cell's disparity sensitivity and best disparity and the shape and slope of its tuning curve. Cells were found that corresponded to categories described by previous authors (“disparity-insensitive,” “tuned excitatory,” “near,” and “far” cells), but many others had intermediate response patterns, or patterns that were difficult to categorize. Quantitative analysis suggested that the various types belong to a continuum.

No relationship could be established between a cell's best orientation and its ocular dominance or any aspect of its disparity tuning. There was no relationship between a cell's ocular dominance and its sensitivity to disparity. Ocular dominance and best disparity were related. As reported by others, cells with best disparities close to zero (the fixation plane) tended to have balanced ocularity, while cells with best disparities in the near or far range had a broad distribution of ocular dominance. Among cells with receptive fields near the vertical meridian, those preferring far disparities tended to be dominated by the contralateral eye, and those preferring near disparities by the ipsilateral eye. It is suggested that this relationship follows from the geometry of near and far images and the pattern of decussation in the visual pathway. There was a significant grouping of cells with similar best disparities along tangential electrode tracks. We believe that this grouping is due to the columnar organization for ocular dominance and the relationship between ocular dominance and best disparity. No evidence was found for a columnar segregation of disparity-sensitive and disparity-insensitive cells.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1988

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

Albus, K. (1975). Predominance of monocularly driven cells in the projection area of the central visual field in cat's striate cortex. Brain Research 89, 341347.Google Scholar
Barlow, H.B., Blakemore, C. & Pettigrew, J.D. (1967). The neural mechanism of binocular depth discrimination. Journal of Physiology (London) 193, 327342.Google Scholar
Bishop, P.O., Henry, G.H. & Smith, C.J. (1971). Binocular interaction fields of single units in the cat striate cortex. Journal of Physiology (London) 216, 3968.CrossRefGoogle ScholarPubMed
Blakemore, C. (1969). Binocular depth discrimination and the naso-temporal division. Journal of Physiology 205, 471497.Google Scholar
Blakemore, C. (1970). The representation of three-dimensional visual space in the cat's striate cortex. Journal of Physiology 209, 155178.CrossRefGoogle ScholarPubMed
Blakemore, C. & Pettigrew, J.D. (1970). Retinal disparity and retinal dominance of binocular cortical neurones. Journal of Physiology 210, 157P159P.Google Scholar
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
Clarke, P.G.H., Donaldson, I.M.L. & Whitteridge, D. (1976). Binocular visual mechanisms in cortical areas I and II of the sheep. Journal of Physiology 256, 509526.Google Scholar
Ferster, D. (1981). A comparison of binocular depth mechanisms in areas 17 and 18 of cat visual cortex. Journal of Physiology 311, 623655.Google Scholar
Fischer, B. & Kruger, J. (1979). Disparity tuning and binocularity of single neurons in the cat visual cortex. Experimental Brain Research 35, 18.Google Scholar
Gardner, J.C. & Rajten, E.J. (1986). Ocular dominance and disparity sensitivity: why there are cells in the visual cortex driven unequally by the two eyes. Experimental Brain Research 64, 505514.Google Scholar
Gilbert, C.D. (1977). Laminar differences in receptive field properties of cells in cat primary visual cortex. Journal of Physiology (London) 268, 391421.Google Scholar
Gilbert, C.D. & Kelly, J.P. (1975). The projections of cells in different layers of the cat's visual cortex. Journal of Comparative Neurology 163, 81106.CrossRefGoogle ScholarPubMed
Hammond, P. (1981). Nonstationarity of ocular dominance in cat striate cortex. Experimental Brain Research 42, 189195.Google Scholar
Hammond, P., Andrews, D.P. & James, D.R. (1975). Invariance of orientational and directional tuning in visual cortical cells of the adult cat. Brain Research 96, 5659.Google Scholar
Hubel, D.H. (1957). Tungsten microelectrode for recording from single units. Science 125, 549550.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. (1962). Receptive Fields, binocular interaction, and functional architecture in the cat's visual cortex. Journal of Physiology (London) 160, 106154.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1965). Binocular interaction in striate cortex of kittens reared with artificial squint. Journal of Neurophysiology 28, 10411059.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1967). Cortical and callosal connections concerned with the vertical meridian of visual fields in the cat. Journal of Neurophysiology 30, 15611573.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology (London) 195, 214243.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1970). Cells sensitive to binocular depth in area 18 of the macaque monkey cortex. Nature 225, 4142.Google Scholar
Kato, H., Bishop, P.O. & Orban, G.A. (1978). Hypercomplex and simple/complex cell classifications in cat striate cortex. Journal of Neurophysiology 41, 10711095.Google Scholar
Kato, H., Bishop, P.O. & Orban, G.A. (1981). Binocular interaction on monocularly discharged lateral geniculate and striate neurons in the cat. Journal of Neurophysiology 46, 932951.CrossRefGoogle ScholarPubMed
Kaye, M., Mitchell, D.E. & Cynader, M. (1981). Selective loss of binocular depth perception after ablation of cat visual cortex. Science 283, 6062.Google Scholar
Lehky, S.R., Jester, J.M. & Sejnowski, T.J. (1987). Line element model of disparity discrimination. Investigative Ophthalmology and Visual Science 28, 293.Google Scholar
Leicester, J. (1968). Projection of the visual vertical meridian to cerebral cortex of the cat. Journal of Neurophysiology 31, 371382.Google Scholar
Levay, S. & Voigt, T. (1987). Ocular dominance and binocular disparity tuning in cat visual cortex. Neuroscience Abstracts 13, 1449.Google Scholar
Macy, A., Ohzawa, I. & Freeman, R.D. (1982). A quantitative study of the classification and stability of ocular dominance in the cat's visual cortex. Experimental Brain Research 48, 401408.Google Scholar
Marr, D. & Poggio, T. (1976). Cooperative computation of stereo disparity. Science 194, 283287.Google Scholar
Marr, D. & Poggio, T. (1979). A computational theory of human stereo vision. Proceedings of the Royal Society of London B 204, 301328.Google Scholar
Maske, R., Yamane, S. & Bishop, P.O. (1986 a). Stereoscopic mechanisms: binocular responses of the striate cells of cats to moving light and dark bars. Proceedings of the Royal Society of London B 229, 227256.Google ScholarPubMed
Maske, R., Yamane, S. & Bishop, P.O. (1986 b). End-stopped cells and binocular depth discrimination in the striate cortex of cats. Proceedings of the Royal Society of London B 229, 257276.Google Scholar
Mayhew, J.E.W. & Longuet-Higgins, C. (1982). A computational model of binocular depth perception. Nature 297, 376378.Google Scholar
Mitchell, D.E. & Blakemore, C. (1970). Binocular depth perception and the corpus callosum. Vision Research 10, 4954.CrossRefGoogle ScholarPubMed
Nelson, J.I., Kato, H. & Bishop, P.O. (1977). The discrimination of orientation and position disparities by binocularly activated neurons in cat striate cortex. Journal of Neurophysiology 40, 260283.CrossRefGoogle Scholar
Ogle, K.N. (1962). The optical space sense. In The Eye, 4, Part 2. pp. 211247. New York: Academic Press.Google Scholar
Ohzawa, I. & Freeman, R.D. (1986 a). The binocular organization of simple cells in the cat's visual cortex. Journal of Neurophysiology 56, 221242.Google Scholar
Ohzawa, I. & Freeman, R.D. (1986 b). The binocular organization of complex cells in the cat's visual cortex. Journal of Neurophysiology 56, 243259.CrossRefGoogle ScholarPubMed
Packwood, J. & Gordon, B. (1975). Stereopsis in normal domestic cat, Siamese cat, and cat raised with alternating monocular occlusion. Journal of Neurophysiology 38, 14851499.Google Scholar
Palmer, L.A. & Rosenquist, A.C. (1974). Visual receptive Fields of single striate cortical units projecting to the superior colliculus in the cat. Brain Research 67, 2742.Google Scholar
Pettigrew, J.D., Cooper, M.L. & Blasdel, G.G. (1979). Improved use of tapetal reflection for eye-position monitoring. Investigative Ophthalmology and Visual Science 18, 490495.Google Scholar
Pettigrew, J.D., Ramachandran, V.S. & Bravo, H. (1984). Some neural connections subserving binocular vision in ungulates. Brain, Behavior, and Evolution 24, 6593.CrossRefGoogle ScholarPubMed
Poggio, G.F. & Fischer, B. (1977). Binocular interaction and depth sensitivity of striate and prestriate cortical neurons of the behaving rhesus monkey. Journal of Neurophysiology 40, 13921405.Google Scholar
Poggio, G.F. & Talbot, W.H. (1981). Mechanisms of static and dynamic stereopsis in foveal cortex of the rhesus monkey. Journal of Physiology 315, 469492.Google Scholar
Richards, W. (1971). Anomalous stereoscopic depth perception. Journal of the Optical Society of America 61, 410414.CrossRefGoogle ScholarPubMed
Robinson, D.A. (1968). Eye movement control in primates. Science 161, 12191224.Google Scholar
Sanderson, K.J. & Sherman, S.M. (1971). Nasotemporal overlap in visual field projected to lateral geniculate nucleus in the cat. Journal of Neurophysiology 34, 453466.Google Scholar
Sherk, H. & Levay, S. (1981). The visual claustrum of the cat. 3. Receptive field properties. Journal of Neuroscience 1, 9931002.Google Scholar
Skottun, B.C. & Freeman, R.D. (1984). Stimulus specificity of binocular cells in the cat's visual cortex: ocular dominance and the matching of left and right eyes. Experimental Brain Research 56, 206216.Google Scholar
Stone, J. (1966). The nasotemporal division of the cat's retina. Journal of Comparative Neurology 126, 585599.Google Scholar
Swindale, N.V., Matsubara, J.A. & Cynader, M.S. (1987). Surface organization of orientation and direction selectivity in cat area 18. Journal of Neuroscience 7, 14141427.CrossRefGoogle ScholarPubMed
Terao, N., Inatomi, A. & Maeda, T. (1982). Anatomical evidence for the overlapped distribution of ipsilaterally and contralaterally projecting ganglion cells to the lateral geniculate nucleus in the cat retina: a morphologic study with fluorescent tracers. Investigative Ophthalmology and Visual Science 23, 796798.Google Scholar
Timney, B. (1983). The effects of early and late monocular deprivation on binocular depth perception in cats. Developmental Brain Research 7, 235243.Google Scholar