Neural correlates of disparity-defined shape discrimination in the human brain.

Binocular disparity, the slight differences between the images registered by our two eyes, provides an important cue when estimating the three-dimensional (3D) structure of the complex environment we inhabit. Sensitivity to binocular disparity is evident at multiple levels of the visual hierarchy in the primate brain, from early visual cortex to parietal and temporal areas. However, the relationship between activity in these areas and key perceptual functions that exploit disparity information for 3D shape perception remains an important open question. Here we investigate the link between human cortical activity and the perception of disparity-defined shape, measuring fMRI responses concurrently with psychophysical shape judgments. We parametrically degraded the coherence of shapes by shuffling the spatial position of dots whose disparity defined the 3D structure and investigated the effect of this stimulus manipulation on both cortical activity and shape discrimination. We report significant relationships between shape coherence and fMRI response in both dorsal (V3, hMT+/V5) and ventral (LOC) visual areas that correspond to the observers' discrimination performance. In contrast to previous suggestions of a dichotomy of disparity-related processes in the ventral and dorsal streams, these findings are consistent with proposed interactions between these pathways that may mediate a continuum of processes important in perceiving 3D shape from coarse contour segmentation to fine curvature estimation.

[1]  S. Zeki,et al.  The processing of kinetic contours in the brain. , 2003, Cerebral cortex.

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

[3]  Alex R. Wade,et al.  The specificity of cortical region KO to depth structure , 2006, NeuroImage.

[4]  D. Heeger,et al.  Retinotopy and Functional Subdivision of Human Areas MT and MST , 2002, The Journal of Neuroscience.

[5]  G. DeAngelis,et al.  Organization of Disparity-Selective Neurons in Macaque Area MT , 1999, The Journal of Neuroscience.

[6]  R. van Ee,et al.  Activation in Visual Cortex Correlates with the Awareness of Stereoscopic Depth , 2005 .

[7]  R. Andersen,et al.  Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[9]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[11]  E. Callaway.  Local circuits in primary visual cortex of the macaque monkey. , 1998, Annual review of neuroscience.

[12]  Scott O. Murray,et al.  Processing Shape, Motion and Three-dimensional Shape-from-motion in the Human Cortex , 2003 .

[13]  Karl J. Friston,et al.  A direct quantitative relationship between the functional properties of human and macaque V5 , 2000, Nature Neuroscience.

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

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

[16]  長沼 朋佳.  Information processing of geometrical features of a surface based on binocular disparity cues : an fMRI study , 2005 .

[17]  Shimon Ullman,et al.  Shape‐selective stereo processing in human object‐related visual areas , 2002, Human brain mapping.

[18]  Makoto Kato,et al.  Processing of shape defined by disparity in monkey inferior temporal cortex. , 2001 .

[19]  Ravi S. Menon,et al.  Differential Effects of Viewpoint on Object-Driven Activation in Dorsal and Ventral Streams , 2002, Neuron.

[20]  G. Orban,et al.  The kinetic occipital (KO) region in man: an fMRI study. , 1997, Cerebral cortex.

[21]  Guy Marchal,et al.  Human Cortical Regions Involved in Extracting Depth from Motion , 1999, Neuron.

[22]  G. Orban,et al.  Attention to 3-D Shape, 3-D Motion, and Texture in 3-D Structure from Motion Displays , 2004, Journal of Cognitive Neuroscience.

[23]  Johan Wagemans,et al.  Characteristics and models of human symmetry detection , 1997, Trends in Cognitive Sciences.

[24]  John H. R. Maunsell,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.

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

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

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

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

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

[30]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

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

[32]  B. Gulyás,et al.  Binocular disparity discrimination in human cerebral cortex: functional anatomy by positron emission tomography. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[33]  H. Sakata,et al.  From Three-Dimensional Space Vision to Prehensile Hand Movements: The Lateral Intraparietal Area Links the Area V3A and the Anterior Intraparietal Area in Macaques , 2001, The Journal of Neuroscience.

[34]  W. Newsome,et al.  Local Field Potential in Cortical Area MT: Stimulus Tuning and Behavioral Correlations , 2006, The Journal of Neuroscience.

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

[36]  Charles E Connor,et al.  Quantitative characterization of disparity tuning in ventral pathway area V4. , 2005, Journal of neurophysiology.

[37]  M. Young,et al.  Neuronal population activity and functional imaging , 1999, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[38]  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.

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

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

[41]  A. Dale,et al.  The Representation of Illusory and Real Contours in Human Cortical Visual Areas Revealed by Functional Magnetic Resonance Imaging , 1999, The Journal of Neuroscience.

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

[43]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  F. A. Miles,et al.  Population Coding in Cortical Area MST , 2002, Annals of the New York Academy of Sciences.

[45]  Wim Vanduffel,et al.  Symmetry activates extrastriate visual cortex in human and nonhuman primates. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[46]  H. C. Longuet-Higgins.  The Role of the Vertical Dimension in Stereoscopic Vision , 1982, Perception.

[47]  C. Büchel,et al.  Surface orientation discrimination activates caudal and anterior intraparietal sulcus in humans: an event-related fMRI study. , 2001, Journal of neurophysiology.

[48]  Tomoka Naganuma,et al.  Neural Correlates for Perception of 3D Surface Orientation from Texture Gradient , 2002, Science.

[49]  Nikos K. Logothetis,et al.  Three-Dimensional Shape Representation in Monkey Cortex , 2002, Neuron.

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

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

[52]  A. Parker,et al.  Efficiency of stereopsis in random-dot stereograms. , 1992, Journal of the Optical Society of America. A, Optics and image science.

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

[54]  S. McKee,et al.  Steroscopic acuity for moving retinal images. , 1978, Journal of the Optical Society of America.

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

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

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

[58]  M. Taira,et al.  Cortical Areas Related to Attention to 3D Surface Structures Based on Shading: An fMRI Study , 2001, NeuroImage.

[59]  H. Bülthoff,et al.  3D shape perception from combined depth cues in human visual cortex , 2005, Nature Neuroscience.

[60]  Michael Erb,et al.  Object-selective responses in the human motion area MT/MST , 2002, Nature Neuroscience.

[61]  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.

[62]  Gregory C DeAngelis,et al.  Macaque Middle Temporal Neurons Signal Depth in the Absence of Motion , 2003, The Journal of Neuroscience.

[63]  D. Heeger,et al.  Activity in primary visual cortex predicts performance in a visual detection task , 2000, Nature Neuroscience.

[64]  Peter Janssen,et al.  Extracting 3D structure from disparity , 2006, Trends in Neurosciences.

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

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

[67]  Rufin Vogels,et al.  Convergence of Depth from Texture and Depth from Disparity in Macaque Inferior Temporal Cortex , 2004, The Journal of Neuroscience.

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

[69]  H. Sakata,et al.  Toward an understanding of the neural processing for 3D shape perception , 2005, Neuropsychologia.

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

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

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

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

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

[75]  D. L. Adams,et al.  Functional organization of macaque V3 for stereoscopic depth. , 2001, Journal of neurophysiology.

[76]  Ione Fine,et al.  The Relationship between Task Performance and Functional Magnetic Resonance Imaging Response , 2005, The Journal of Neuroscience.

[77]  G. Orban,et al.  Extracting 3D from Motion: Differences in Human and Monkey Intraparietal Cortex , 2002, Science.

[78]  H. Bülthoff,et al.  Representation of the perceived 3-D object shape in the human lateral occipital complex. , 2003, Cerebral cortex.

[79]  David J Heeger,et al.  Response Suppression in V1 Agrees with Psychophysics of Surround Masking , 2003, The Journal of Neuroscience.

[80]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

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

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

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

[84]  Frank Bremmer,et al.  Neural correlates of implied motion , 2003, Nature.

[85]  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.

[86]  Ian P. Howard,et al.  Seeing in Depth , 2008 .

[87]  A Grinvald,et al.  Optical imaging reveals the functional architecture of neurons processing shape and motion in owl monkey area MT , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

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

[89]  Mark W Greenlee,et al.  BOLD response in dorsal areas varies with relative disparity level , 2004, Neuroreport.

[90]  G. Orban,et al.  A Higher Order Motion Region in Human Inferior Parietal Lobule Evidence from fMRI , 2003, Neuron.