Selectivity for three-dimensional contours and surfaces in the anterior intraparietal area.

The macaque anterior intraparietal area (AIP) is crucial for visually guided grasping. AIP neurons respond during the visual presentation of real-world objects and encode the depth profile of disparity-defined curved surfaces. We investigated the neural representation of curved surfaces in AIP using a stimulus-reduction approach. The stimuli consisted of three-dimensional (3-D) shapes curved along the horizontal axis, the vertical axis, or both the horizontal and the vertical axes of the shape. The depth profile was defined solely by binocular disparity that varied along either the boundary or the surface of the shape or along both the boundary and the surface of the shape. The majority of AIP neurons were selective for curved boundaries along the horizontal or the vertical axis, and neural selectivity emerged at short latencies. Stimuli in which disparity varied only along the surface of the shape (with zero disparity on the boundaries) evoked selectivity in a smaller proportion of AIP neurons and at considerably longer latencies. AIP neurons were not selective for 3-D surfaces composed of anticorrelated disparities. Thus the neural selectivity for object depth profile in AIP is present when only the boundary is curved in depth, but not for disparity in anticorrelated stereograms.

[1]  D. Pandya,et al.  Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey , 1978, Brain Research.

[2]  M. Goodale,et al.  FMRI Reveals a Dissociation between Grasping and Perceiving the Size of Real 3D Objects , 2007, PloS one.

[3]  G. Orban,et al.  Macaque Inferior Temporal Neurons Are Selective for Three-Dimensional Boundaries and Surfaces , 2001, The Journal of Neuroscience.

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

[5]  R. Andersen,et al.  Intentional maps in posterior parietal cortex. , 2002, Annual review of neuroscience.

[6]  G. Orban,et al.  Selectivity for 3D shape that reveals distinct areas within macaque inferior temporal cortex. , 2000, Science.

[7]  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.

[8]  K Tsutsui,et al.  Neural coding of 3D features of objects for hand action in the parietal cortex of the monkey. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

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

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

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

[13]  F. Qiu,et al.  Figure and Ground in the Visual Cortex: V2 Combines Stereoscopic Cues with Gestalt Rules , 2005, Neuron.

[14]  A. Simeone,et al.  The TINS Lecture Understanding the roles of Otx1 and Otx2 in the control of brain morphogenesis , 1999, Trends in Neurosciences.

[15]  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.

[16]  C. Tyler,et al.  Stereoprocessing of cyclopean depth images: horizontally elongated summation fields , 2001, Vision Research.

[17]  H. Sakata,et al.  Neural mechanisms of visual guidance of hand action in the parietal cortex of the monkey. , 1995, Cerebral cortex.

[18]  Paul B Hibbard,et al.  Binocular cues and the control of prehension. , 2004, Spatial vision.

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

[20]  B. Rogers,et al.  Disparity curvature and the perception of three-dimensional surfaces , 1989, Nature.

[21]  A. Cobo-Lewis,et al.  Monocular dot-density cues in random-dot stereograms , 1996, Vision Research.

[22]  L E Mays,et al.  Neurons in monkey parietal area LIP are tuned for eye-movement parameters in three-dimensional space. , 1995, Journal of neurophysiology.

[23]  H. Sakata,et al.  Deficit of hand preshaping after muscimol injection in monkey parietal cortex , 1994, Neuroreport.

[24]  Hansjörg Scherberger,et al.  Context-Specific Grasp Movement Representation in the Macaque Anterior Intraparietal Area , 2009, The Journal of Neuroscience.

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

[26]  H. Sakata,et al.  The TINS Lecture The parietal association cortex in depth perception and visual control of hand action , 1997, Trends in Neurosciences.

[27]  H. Sakata,et al.  Selectivity of the parietal visual neurones in 3D orientation of surface of stereoscopic stimuli. , 1996, Neuroreport.

[28]  John H. R. Maunsell,et al.  Visual response latencies in striate cortex of the macaque monkey. , 1992, Journal of neurophysiology.

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

[30]  Umberto Castiello,et al.  The Cortical Control of Visually Guided Grasping , 2008, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

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

[32]  Takahiro Doi,et al.  Matching and correlation computations in stereoscopic depth perception. , 2011, Journal of vision.

[33]  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.

[34]  Peter Janssen,et al.  Synchronization between the end stages of the dorsal and the ventral visual stream. , 2011, Journal of neurophysiology.

[35]  Ichiro Fujita,et al.  Disparity-energy signals in perceived stereoscopic depth. , 2008, Journal of vision.

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

[37]  Eric T. Carlson,et al.  A neural code for three-dimensional object shape in macaque inferotemporal cortex , 2008, Nature Neuroscience.

[38]  J. Culham,et al.  The role of parietal cortex in visuomotor control: What have we learned from neuroimaging? , 2006, Neuropsychologia.

[39]  H. Sakata,et al.  Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. , 2000, Journal of neurophysiology.

[40]  H. Komatsu,et al.  Disparity sensitivity of neurons in monkey extrastriate area MST , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[42]  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.

[43]  G. Orban,et al.  Coding of Shape and Position in Macaque Lateral Intraparietal Area , 2008, The Journal of Neuroscience.

[44]  Jan J. Koenderink,et al.  Solid shape , 1990 .

[45]  John H. R. Maunsell,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. II. Binocular interactions and sensitivity to binocular disparity. , 1983, Journal of neurophysiology.

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

[47]  R. Vogels,et al.  Contribution of Inferior Temporal and Posterior Parietal Activity to Three-Dimensional Shape Perception , 2010, Current Biology.

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

[49]  Aldo Genovesio,et al.  Integration of retinal disparity and fixation-distance related signals toward an egocentric coding of distance in the posterior parietal cortex of primates. , 2004, Journal of neurophysiology.

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

[51]  S. McKee,et al.  Contour completion through depth interferes with stereoacuity , 2002, Vision Research.

[52]  Ravi S. Menon,et al.  Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas , 2003, Experimental Brain Research.

[53]  Peter Janssen,et al.  A Distinct Representation of Three-Dimensional Shape in Macaque Anterior Intraparietal Area: Fast, Metric, and Coarse , 2009, The Journal of Neuroscience.

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

[55]  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.

[56]  Hong Zhou,et al.  Representation of stereoscopic edges in monkey visual cortex , 2000, Vision Research.