Stereoscopic mechanisms in monkey visual cortex: binocular correlation and disparity selectivity

The neural signals in visual cortex associated with positional disparity and contrast texture correlation of binocular images are the subject of this study. We have analyzed the effects of stereoscopically presented luminous bars and of dynamic random-dot patterns on the activity of single neurons in cortical visual areas V1, V2, and V3-V3A of the alert, visually trained rhesus macaque. The interpretation of the results and considerations of possible neural mechanisms led us to recognize 2 functional sets of stereoscopic neurons. (1) A set of neurons, tuned excitatory (T0) or tuned inhibitory (TI), which respond sharply to images of zero or near-zero disparity. Objects at or about the horopter drive the T0 neurons and suppress the TI, while objects nearer and farther have the opposite effects on each type, inhibition of the T0 and excitation of the TI. The activity of these neurons may provide, in a reciprocal way, the definition of the plane of fixation, and the basic reference for binocular single vision and depth discrimination. (2) A second set of neurons includes tuned excitatory at larger crossed or uncrossed disparities (TN/TF) and neurons with reciprocal excitatory and inhibitory disparity sensitivity with cross- over at the horopter (NE/FA). Binocularly uncorrelated image contrast drives these neurons to a maintained level of activity, which shifts, in response to correlated images, toward facilitation or suppression as a function of positional disparity. These neurons may operate in the neural processing leading to stereopsis, both coarse and fine, and also provide signals for the system controlling binocular vergence. These results indicate that cortical visual neurons are binocularly linked to respond to the relative position and contrast of the images over their receptive fields, and also that both these aspects of binocular stimulation may be utilized by the brain as a source of stereoscopic information.

[1]  C. Wheatstone.  XVIII. Contributions to the physiology of vision. —Part the first. On some remarkable, and hitherto unobserved, phenomena of binocular vision , 1962, Philosophical Transactions of the Royal Society of London.

[2]  M L Wolbarsht,et al.  Glass Insulated Platinum Microelectrode , 1960, Science.

[3]  B. Julesz.  Binocular depth perception of computer-generated patterns , 1960 .

[4]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[5]  Wilfrid Rall,et al.  Theoretical significance of dendritic trees for neuronal input-output relations , 1964 .

[6]  C. Blakemore,et al.  The neural mechanism of binocular depth discrimination , 1967, The Journal of physiology.

[7]  W Rall,et al.  Dendritic location of synapses and possible mechanisms for the monosynaptic EPSP in motoneurons. , 1967, Journal of neurophysiology.

[8]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[9]  S. Zeki.  Representation of central visual fields in prestriate cortex of monkey. , 1969, Brain research.

[10]  B. Cragg.  The topography of the afferent projections in the circumstriate visual cortex of the monkey studied by the Nauta method. , 1969, Vision research.

[11]  D. Hubel,et al.  Stereoscopic Vision in Macaque Monkey: Cells sensitive to Binocular Depth in Area 18 of the Macaque Monkey Cortex , 1970, Nature.

[12]  P. O. Bishop,et al.  Binocular interaction fields of single units in the cat striate cortex , 1971, The Journal of physiology.

[13]  P. O. Bishop,et al.  Spatial vision. , 1971, Annual review of psychology.

[14]  P. Schiller,et al.  Quantitative studies of single-cell properties in monkey striate cortex. I. Spatiotemporal organization of receptive fields. , 1976, Journal of neurophysiology.

[15]  P. Schiller,et al.  Quantitative studies of single-cell properties in monkey striate cortex. II. Orientation specificity and ocular dominance. , 1976, Journal of neurophysiology.

[16]  S. Zeki,et al.  Combined anatomical and electrophysiological studies on the boundary between the second and third visual areas of rhesus monkey cortex , 1976, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[17]  R. Doty,et al.  Foveal striate cortex of behaving monkey: single-neuron responses to square-wave gratings during fixation of gaze. , 1977, Journal of neurophysiology.

[18]  G. Poggio,et al.  Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey. , 1977, Journal of neurophysiology.

[19]  J. Baizer,et al.  Visual responses of area 18 neurons in awake, behaving monkey. , 1977, Journal of neurophysiology.

[20]  D. C. Essen,et al.  The topographic organization of rhesus monkey prestriate cortex. , 1978, The Journal of physiology.

[21]  S. Zeki,et al.  The third visual complex of rhesus monkey prestriate cortex. , 1978, The Journal of physiology.

[22]  S. Zeki.  Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex. , 1978, The Journal of physiology.

[23]  J. Movshon,et al.  Receptive field organization of complex cells in the cat's striate cortex. , 1978, The Journal of physiology.

[24]  Christopher W. Tyler,et al.  Binocular cross-correlation in time and space , 1978, Vision Research.

[25]  J. Lund,et al.  Anatomical organization of primate visual cortex area VII , 1981, The Journal of comparative neurology.

[26]  C. Gross,et al.  Visual topography of V2 in the macaque , 1981, The Journal of comparative neurology.

[27]  D. Ferster.  A comparison of binocular depth mechanisms in areas 17 and 18 of the cat visual cortex , 1981, The Journal of physiology.

[28]  J. Baizer.  Receptive field properties of V3 neurons in monkey. , 1982, Investigative ophthalmology & visual science.

[29]  D. V. van Essen,et al.  The pattern of interhemispheric connections and its relationship to extrastriate visual areas in the macaque monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  D C Van Essen,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. , 1983, Journal of neurophysiology.

[31]  T. Poggio,et al.  Nonlinear interactions in a dendritic tree: localization, timing, and role in information processing. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[32]  M. Silverman,et al.  Functional organization of the second cortical visual area in primates. , 1983, Science.

[33]  G. Blasdel,et al.  Physiological organization of layer 4 in macaque striate cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  John H. R. Maunsell,et al.  The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability , 1984, Vision Research.

[35]  J. P. Jones,et al.  Periodic simple cells in cat area 17. , 1984, Journal of neurophysiology.

[36]  D. Hubel,et al.  Anatomy and physiology of a color system in the primate visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[37]  T. Poggio,et al.  Biophysics of Computation: Neurons, Synapses and Membranes , 1984 .

[38]  J. P. Jones,et al.  Receptive-field properties and laminar distribution of X-like and Y-like simple cells in cat area 17. , 1984, Journal of neurophysiology.

[39]  P. O. Bishop,et al.  Binocular simple cells for local stereopsis: Comparison of receptive field organizations for the two eyes , 1984, Vision Research.

[40]  S Yamane,et al.  Simple and B-cells in cat striate cortex. Complementarity of responses to moving light and dark bars. , 1985, Journal of neurophysiology.

[41]  E. DeYoe,et al.  Segregation of efferent connections and receptive field properties in visual area V2 of the macaque , 1985, Nature.

[42]  B. C. Motter,et al.  Responses of neurons in visual cortex (V1 and V2) of the alert macaque to dynamic random-dot stereograms , 1985, Vision Research.

[43]  S. Zeki,et al.  Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex , 1985, Nature.

[44]  B M Dow,et al.  The mapping of visual space onto foveal striate cortex in the macaque monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  W. Newsome,et al.  The projections from striate cortex (V1) to areas V2 and V3 in the macaque monkey: Asymmetries, areal boundaries, and patchy connections , 1986, The Journal of comparative neurology.

[46]  P. O. Bishop,et al.  End-stopped cells and binocular depth discrimination in the striate cortex of cats , 1986, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[47]  S Yamane,et al.  Stereoscopic mechanisms: binocular responses of the striate cells of cats to moving light and dark bars , 1986, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[48]  D. V. van Essen,et al.  Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[49]  D C Van Essen,et al.  Shifter circuits: a computational strategy for dynamic aspects of visual processing. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[50]  D. J. Felleman,et al.  Receptive field properties of neurons in area V3 of macaque monkey extrastriate cortex. , 1987, Journal of neurophysiology.

[51]  R. Blake,et al.  Depth without disparity in random-dot stereograms , 1987, Perception & psychophysics.

[52]  Klein,et al.  Nonlinear directionally selective subunits in complex cells of cat striate cortex. , 1987, Journal of neurophysiology.

[53]  DH Hubel,et al.  Segregation of form, color, and stereopsis in primate area 18 , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[54]  DH Hubel,et al.  Psychophysical evidence for separate channels for the perception of form, color, movement, and depth , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.