Responses of primary visual cortical neurons to binocular disparity without depth perception

The identification of brain regions that are associated with the conscious perception of visual stimuli is a major goal in neuroscience. Here we present a test of whether the signals on neurons in cortical area V1 correspond directly to our conscious perception of binocular stereoscopic depth. Depth perception requires that image features on one retina are first matched with appropriate features on the other retina. The mechanisms that perform this matching can be examined by using random-dot stereograms, in which the left and right eyes view randomly positioned but binocularly correlated dots. We exploit the fact that anticorrelated random-dot stereograms (in which dots in one eye are matched geometrically to dots of the opposite contrast in the other eye) do not give rise to the perception of depth because the matching process does not find a consistent solution. Anticorrelated random-dot stereograms contain binocular features that could excite neurons that have not solved the correspondence problem. We demonstrate that disparity-selective neurons in V1 signal the disparity of anticorrelated random-dot stereograms, indicating that they do not unambiguously signal stereoscopic depth. Hence single V1 neurons cannot account for the conscious perception of stereopsis, although combining the outputs of many V1 neurons could solve the matching problem. The accompanying paper suggests an additional function for disparity signals from V1: they may be important for the rapid involuntary control of vergence eye movements (eye movements that bring the images on the two foveae into register).

[1]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[2]  T. Poggio,et al.  A computational theory of human stereo vision , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

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

[4]  Ning Qian,et al.  Computing Stereo Disparity and Motion with Known Binocular Cell Properties , 1994, Neural Computation.

[5]  A. B. Bonds,et al.  Classifying simple and complex cells on the basis of response modulation , 1991, Vision Research.

[6]  C. Koch,et al.  Are we aware of neural activity in primary visual cortex? , 1995, Nature.

[7]  G. Poggio,et al.  Stereoscopic mechanisms in monkey visual cortex: binocular correlation and disparity selectivity , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  Alexander I. Cogan,et al.  Depth in anticorrelated stereograms: Effects of spatial density and interocular delay , 1993, Vision Research.

[9]  F. A. Miles,et al.  Vergence eye movements in response to binocular disparity without depth perception , 1997, Nature.

[10]  B. Julesz Foundations of Cyclopean Perception , 1971 .

[11]  Gian F. Poggio Mechanisms of Stereopsis in Monkey Visual Cortex , 1995 .

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

[13]  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.

[14]  T. Poggio,et al.  The analysis of stereopsis. , 1984, Annual review of neuroscience.

[15]  I. Ohzawa,et al.  Stereoscopic depth discrimination in the visual cortex: neurons ideally suited as disparity detectors. , 1990, Science.

[16]  W E Grimson,et al.  A computer implementation of a theory of human stereo vision. , 1981, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.