Neural modulation by binocular disparity greatest in human dorsal visual stream.

Although cortical activation to binocular disparity can be demonstrated throughout occipital and parietal cortices, the relative contributions to depth perception made by different human cortical areas have not been established. To investigate whether different regions are optimized for specific disparity ranges, we have measured the responses of occipital and parietal areas to different magnitudes of binocular disparity. Using stimuli consisting of sinusoidal depth modulations, we measured cortical activation when the stimuli were located at pedestal disparities of 0, 0.1, 0.35, and 0.7 degrees from fixation. Across all areas, occipital and parietal, there was an increase in BOLD signal with increasing pedestal disparity, compared with a plane at zero disparity. However, the greatest modulation of response by the different pedestals was found in the dorsal visual areas and the parietal areas. These differences contrast with the response to the zero disparity plane, compared with fixation, which is greatest in the early visual areas, smaller in the ventral and dorsal visual areas, and absent in parietal areas. Using the simultaneously acquired psychophysical data we also measured a greater response to correct than to incorrect trials, an effect that increased with rising pedestal disparity and was greatest in dorsal visual and parietal areas. These results illustrate that the dorsal stream, along both its occipital and parietal branches, can reliably discriminate a large range of disparities.

[1]  Patrick Dupont,et al.  The Quantitative Nature of a Visual Task Differentiates between Ventral and Dorsal Stream , 2002, Journal of Cognitive Neuroscience.

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

[3]  Gregory C DeAngelis,et al.  Binocular Vision: An Orientation to Disparity Coding , 2002, Current Biology.

[4]  Guy A. Orban,et al.  Mapping the parietal cortex of human and non-human primates , 2006, Neuropsychologia.

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

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

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

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

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

[10]  Bruce G Cumming,et al.  A simple model accounts for the response of disparity-tuned V1 neurons to anticorrelated images , 2002, Visual Neuroscience.

[11]  A. Parker.  Binocular depth perception and the cerebral cortex , 2007, Nature Reviews Neuroscience.

[12]  A J Parker,et al.  Binocular disparity processing with opposite-contrast stimuli. , 1995 .

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

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

[15]  Scott T. Grafton,et al.  Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustments of grasp , 2005, Nature Neuroscience.

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

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

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

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

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

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

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

[23]  Christopher W. Tyler,et al.  A stereoscopic view of visual processing streams , 1990, Vision Research.

[24]  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.

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

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

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

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

[29]  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.

[30]  A. Parker,et al.  Perceptually Bistable Three-Dimensional Figures Evoke High Choice Probabilities in Cortical Area MT , 2001, The Journal of Neuroscience.

[31]  D. Heeger,et al.  Topographic organization for delayed saccades in human posterior parietal cortex. , 2005, Journal of neurophysiology.

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

[33]  Keiji Tanaka,et al.  Connections between Anterior Inferotemporal Cortex and Superior Temporal Sulcus Regions in the Macaque Monkey , 2000, The Journal of Neuroscience.

[34]  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.

[35]  B. Cumming,et al.  Testing quantitative models of binocular disparity selectivity in primary visual cortex. , 2003, Journal of neurophysiology.

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

[37]  R. Andersen,et al.  Encoding of three-dimensional structure-from-motion by primate area MT neurons , 1998, Nature.

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

[39]  Holly Bridge,et al.  Topographical representation of binocular depth in the human visual cortex using fMRI. , 2007, Journal of vision.

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

[41]  Izumi Ohzawa,et al.  Mechanisms of stereoscopic vision: the disparity energy model , 1998, Current Opinion in Neurobiology.

[42]  Ione Fine,et al.  Face adaptation does not improve perceptual salience , 2010 .

[43]  A. Parker,et al.  Range and mechanism of encoding of horizontal disparity in macaque V1. , 2002, Journal of neurophysiology.

[44]  J Mazziotta,et al.  A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). , 2001, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

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

[47]  G. DeAngelis,et al.  Cortical area MT and the perception of stereoscopic depth , 1998, Nature.

[48]  Arthur W. Toga,et al.  A Probabilistic Atlas of the Human Brain: Theory and Rationale for Its Development The International Consortium for Brain Mapping (ICBM) , 1995, NeuroImage.

[49]  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.

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

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

[52]  Andrew J. Parker,et al.  Local Disparity Not Perceived Depth Is Signaled by Binocular Neurons in Cortical Area V1 of the Macaque , 2000, The Journal of Neuroscience.

[53]  G C DeAngelis,et al.  The physiology of stereopsis. , 2001, Annual review of neuroscience.

[54]  M. Sereno,et al.  Mapping of Contralateral Space in Retinotopic Coordinates by a Parietal Cortical Area in Humans , 2001, Science.

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

[56]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[57]  K. Grill-Spector,et al.  The human visual cortex. , 2004, Annual review of neuroscience.

[58]  Doris Y. Tsao,et al.  Stereopsis Activates V3A and Caudal Intraparietal Areas in Macaques and Humans , 2003, Neuron.

[59]  Jonas Larsson,et al.  Imaging vision : Functional mapping of intermediate visual processes in man , 2001 .

[60]  B G Cumming,et al.  Disparity Detection in Anticorrelated Stereograms , 1998, Perception.

[61]  K. Grill-Spector,et al.  fMR-adaptation: a tool for studying the functional properties of human cortical neurons. , 2001, Acta psychologica.

[62]  Jerry D. Nguyenkim,et al.  Disparity-Based Coding of Three-Dimensional Surface Orientation by Macaque Middle Temporal Neurons , 2003, The Journal of Neuroscience.

[63]  Ichiro Fujita,et al.  Representation of stereoscopic depth based on relative disparity in macaque area V4. , 2007, Journal of neurophysiology.

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

[65]  D. Heeger,et al.  Sustained Activity in Topographic Areas of Human Posterior Parietal Cortex during Memory-Guided Saccades , 2006, The Journal of Neuroscience.

[66]  David J. Fleet,et al.  Human cortical activity correlates with stereoscopic depth perception. , 2001, Journal of neurophysiology.

[67]  Bruce G. Cumming,et al.  Understanding the Cortical Specialization for Horizontal Disparity , 2004, Neural Computation.

[68]  Leslie G. Ungerleider,et al.  Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[71]  A. Parker,et al.  The Precision of Single Neuron Responses in Cortical Area V1 during Stereoscopic Depth Judgments , 2000, The Journal of Neuroscience.

[72]  J. Pettigrew.  Comparative Physiology of Binocular Vision , 1980 .

[73]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

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

[75]  Peter Neri,et al.  A stereoscopic look at visual cortex. , 2005, Journal of neurophysiology.

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

[77]  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.

[78]  B. G. Cumming,et al.  An unexpected specialization for horizontal disparity in primate primary visual cortex , 2002, Nature.

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

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

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

[82]  B. G. Cumming,et al.  Responses of primary visual cortical neurons to binocular disparity without depth perception , 1997, Nature.

[83]  D. Heeger,et al.  Topographic maps of visual spatial attention in human parietal cortex. , 2005, Journal of neurophysiology.

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

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

[86]  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.

[87]  P. O. Bishop,et al.  Analysis of retinal correspondence by studying receptive fields of rinocular single units in cat striate cortex , 2004, Experimental Brain Research.

[88]  Svetlana S. Georgieva,et al.  The Processing of Three-Dimensional Shape from Disparity in the Human Brain , 2009, The Journal of Neuroscience.

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

[90]  Z. Kourtzi,et al.  Multivoxel Pattern Selectivity for Perceptually Relevant Binocular Disparities in the Human Brain , 2008, The Journal of Neuroscience.

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

[92]  B. Julesz,et al.  Binocular disparity modulation sensitivity to disparities offset from the plane of fixation , 1984, Vision Research.

[93]  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.

[94]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[95]  Zoe Kourtzi,et al.  Neural correlates of disparity-defined shape discrimination in the human brain. , 2007, Journal of neurophysiology.

[96]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

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

[98]  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.

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

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

[101]  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.