Representation of stereoscopic depth based on relative disparity in macaque area V4.

Stereoscopic vision is characterized by greater visual acuity when a background feature serves as a reference. When a reference is present, the perceived depth of an object is predominantly dependent on this reference. Neural representations of stereoscopic depth are expected to have a relative frame of reference. The conversion of absolute disparity encoded in area V1 to relative disparity begins in area V2, although the information encoded in this area appears to be insufficient for stereopsis. This study examines whether relative disparity is encoded in a higher cortical area. We recorded the responses of V4 neurons from macaque monkeys to various combinations of the absolute disparities of two features: the center patch and surrounding annulus of a dynamic random-dot stereogram. We analyzed the effects of the disparity of the surrounding annulus on the tuning for the disparity of the center patch; the tuning curves of relative-disparity-selective neurons for disparities of the center patch should shift with changes in the disparity of the surrounding annulus. Most V4 tuning curves exhibited significant shifts. The magnitudes of the shifts were larger than those reported for V2 neurons and smaller than that expected for an ideal relative-disparity-selective cell. No correlation was found between the shift magnitude and the degree of size suppression, suggesting that the two phenomena are not the result of a common mechanism. Our results suggest that the coding of relative disparity advances as information flows along the cortical pathway that includes areas V2 and V4.

[1]  C. Connor,et al.  Three-dimensional orientation tuning in macaque area V4 , 2002, Nature Neuroscience.

[2]  C. Connor,et al.  Responses to contour features in macaque area V4. , 1999, Journal of neurophysiology.

[3]  R. Desimone,et al.  Visual properties of neurons in area V4 of the macaque: sensitivity to stimulus form. , 1987, Journal of neurophysiology.

[4]  D. Regan,et al.  Necessary conditions for the perception of motion in depth. , 1986, Investigative ophthalmology & visual science.

[5]  R. Wurtz,et al.  Response to motion in extrastriate area MSTl: disparity sensitivity. , 1999, Journal of neurophysiology.

[6]  D. V. van Essen,et al.  Selectivity for polar, hyperbolic, and Cartesian gratings in macaque visual cortex. , 1993, Science.

[7]  N. Draper,et al.  Applied Regression Analysis: Draper/Applied Regression Analysis , 1998 .

[8]  G. DeAngelis,et al.  Contribution of Middle Temporal Area to Coarse Depth Discrimination: Comparison of Neuronal and Psychophysical Sensitivity , 2003, The Journal of Neuroscience.

[9]  G. DeAngelis,et al.  Linking Neural Representation to Function in Stereoscopic Depth Perception: Roles of the Middle Temporal Area in Coarse versus Fine Disparity Discrimination , 2006, The Journal of Neuroscience.

[10]  Gregory C DeAngelis,et al.  Coding of horizontal disparity and velocity by MT neurons in the alert macaque. , 2003, Journal of neurophysiology.

[11]  I. Fujita,et al.  Disparity selectivity of neurons in monkey inferior temporal cortex. , 2000, Journal of neurophysiology.

[12]  M. Carandini Receptive fields and suppressive fields in the early visual system , 2004 .

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

[14]  A. Parker,et al.  Comparing perceptual signals of single V5/MT neurons in two binocular depth tasks. , 2004, Journal of neurophysiology.

[15]  F. A. Miles,et al.  Single-unit activity in cortical area MST associated with disparity-vergence eye movements: evidence for population coding. , 2001, Journal of neurophysiology.

[16]  Ichiro Fujita,et al.  Neural Correlates of Fine Depth Discrimination in Monkey Inferior Temporal Cortex , 2005, The Journal of Neuroscience.

[17]  J. Allman,et al.  Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. , 1985, Annual review of neuroscience.

[18]  David J Heeger,et al.  Stereoscopic processing of absolute and relative disparity in human visual cortex. , 2004, Journal of neurophysiology.

[19]  C E Connor,et al.  Disparity tuning in macaque area V4 , 2001, Neuroreport.

[20]  S. Zeki,et al.  Colour coding in rhesus monkey prestriate cortex. , 1973, Brain research.

[21]  Jay Hegdé,et al.  Stimulus dependence of disparity coding in primate visual area V4. , 2005, Journal of neurophysiology.

[22]  G. Orban,et al.  Three-Dimensional Shape Coding in Inferior Temporal Cortex , 2000, Neuron.

[23]  C. Gross,et al.  Visuotopic organization and extent of V3 and V4 of the macaque , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  Ichiro Fujita,et al.  Disparity-selective neurons in area V4 of macaque monkeys. , 2002 .

[25]  L. Chalupa,et al.  The visual neurosciences , 2004 .

[26]  Takahiro Doi,et al.  Disparity-tuning characteristics of neuronal responses to dynamic random-dot stereograms in macaque visual area V4. , 2005, Journal of neurophysiology.

[27]  H. Sakata,et al.  Parietal neurons represent surface orientation from the gradient of binocular disparity. , 2000, Journal of neurophysiology.

[28]  R. Desimone,et al.  Shape recognition and inferior temporal neurons. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[29]  G. Westheimer,et al.  Cooperative neural processes involved in stereoscopic acuity , 1979, Experimental Brain Research.

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

[31]  Leslie G. Ungerleider,et al.  Contour, color and shape analysis beyond the striate cortex , 1985, Vision Research.

[32]  G. DeAngelis,et al.  Contribution of Area MT to Stereoscopic Depth Perception Choice-Related Response Modulations Reflect Task Strategy , 2004, Neuron.

[33]  D. Marr,et al.  Representation and recognition of the spatial organization of three-dimensional shapes , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[34]  I. Fujita,et al.  Rejection of False Matches for Binocular Correspondence in Macaque Visual Cortical Area V4 , 2004, The Journal of Neuroscience.

[35]  Y. Frégnac,et al.  The “silent” surround of V1 receptive fields: theory and experiments , 2003, Journal of Physiology-Paris.

[36]  G. Orban,et al.  At Least at the Level of Inferior Temporal Cortex, the Stereo Correspondence Problem Is Solved , 2003, Neuron.

[37]  C R Olson,et al.  Object-centered direction selectivity in the macaque supplementary eye field , 1995, Science.

[38]  A. Parker,et al.  A specialization for relative disparity in V2 , 2002, Nature Neuroscience.

[39]  D. B. Bender,et al.  Visual properties of neurons in inferotemporal cortex of the Macaque. , 1972, Journal of neurophysiology.

[40]  H. Collewijn,et al.  Motion perception during dichoptic viewing of moving random-dot stereograms , 1985, Vision Research.

[41]  Minami Ito,et al.  Size and position invariance of neuronal responses in monkey inferotemporal cortex. , 1995, Journal of neurophysiology.

[42]  Jay Hegdé,et al.  Role of primate visual area V4 in the processing of 3-D shape characteristics defined by disparity. , 2005, Journal of neurophysiology.

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

[44]  A. Parker,et al.  Binocular Neurons in V1 of Awake Monkeys Are Selective for Absolute, Not Relative, Disparity , 1999, The Journal of Neuroscience.

[45]  Peter Janssen,et al.  Selectivity for three-dimensional shape in macaque posterior parietal cortex , 2006 .

[46]  Carl R Olson,et al.  Brain representation of object-centered space in monkeys and humans. , 2003, Annual review of neuroscience.

[47]  N. Draper,et al.  Applied Regression Analysis , 1966 .

[48]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[49]  R Vogels,et al.  Macaque inferior temporal neurons are selective for disparity-defined three-dimensional shapes. , 1999, Proceedings of the National Academy of Sciences of the United States of America.