Anterior Regions of Monkey Parietal Cortex Process Visual 3D Shape

The intraparietal cortex is involved in the control of visually guided actions, like reach-to-grasp movements, which require extracting the 3D shape and position of objects from 2D retinal images. Using fMRI in behaving monkeys, we investigated the role of the intraparietal cortex in processing stereoscopic information for recovering the depth structure and the position in depth of objects. We found that while several areas (CIP, LIP, and AIP on the lateral bank; PIP and MIP on the medial bank) are activated by stereoscopic stimuli, AIP and an adjoining portion of LIP are sensitive only to depth structure. Furthermore, only these two regions are sensitive to both the depth structure and the 2D shape of small objects. These results indicate that extracting 3D spatial information from stereo involves several intraparietal areas, among which AIP and anterior LIP are more specifically engaged in extracting the 3D shape of objects.

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

[2]  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.

[3]  Olivier D. Faugeras,et al.  Flows of diffeomorphisms for multimodal image registration , 2002, Proceedings IEEE International Symposium on Biomedical Imaging.

[4]  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.

[5]  J. Tresilian.  Attention in action or obstruction of movement? A kinematic analysis of avoidance behavior in prehension , 1998, Experimental Brain Research.

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

[7]  Olivier D. Faugeras,et al.  Variational Methods for Multimodal Image Matching , 2002, International Journal of Computer Vision.

[8]  Olivier P. Faugeras,et al.  The Retinotopic Organization of Primate Dorsal V4 and Surrounding Areas: A Functional Magnetic Resonance Imaging Study in Awake Monkeys , 2003, The Journal of Neuroscience.

[9]  J. Tenenbaum,et al.  A global geometric framework for nonlinear dimensionality reduction. , 2000, Science.

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

[11]  H. Sakata,et al.  Integration of perspective and disparity cues in surface-orientation-selective neurons of area CIP. , 2001, Journal of neurophysiology.

[12]  Anders M. Dale,et al.  Repeated fMRI Using Iron Oxide Contrast Agent in Awake, Behaving Macaques at 3 Tesla , 2002, NeuroImage.

[13]  Simon Grant,et al.  Advantages of binocular vision for the control of reaching and grasping , 2006, Experimental Brain Research.

[14]  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.

[15]  Maurizio Corbetta,et al.  Distribution of activity across the monkey cerebral cortical surface, thalamus and midbrain during rapid, visually guided saccades. , 2006, Cerebral cortex.

[16]  Leslie G. Ungerleider,et al.  Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. , 1994, Cerebral cortex.

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

[18]  C. Galletti,et al.  Occipital (V6) and parietal (V6A) areas in the anterior wall of the parieto‐occipital sulcus of the macaque: a cytoarchitectonic study , 2005, The European journal of neuroscience.

[19]  R. Mansfield,et al.  Analysis of visual behavior , 1982 .

[20]  Svetlana S. Georgieva,et al.  Using Functional Magnetic Resonance Imaging to Assess Adaptation and Size Invariance of Shape Processing by Humans and Monkeys , 2005, The Journal of Neuroscience.

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

[22]  Roger Selley,et al.  The authors are indebted , 1978 .

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

[24]  M. Arbib,et al.  Grasping objects: the cortical mechanisms of visuomotor transformation , 1995, Trends in Neurosciences.

[25]  L H Snyder,et al.  Saccade-related activity in the parietal reach region. , 2000, Journal of neurophysiology.

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

[27]  N. Kanwisher,et al.  Cortical Regions Involved in Perceiving Object Shape , 2000, The Journal of Neuroscience.

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

[29]  B. Anderson.  Depth perception , 2008 .

[30]  Michael A. Arbib,et al.  Modeling parietal-premotor interactions in primate control of grasping , 1998, Neural Networks.

[31]  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.

[32]  Leslie G. Ungerleider.  Two cortical visual systems , 1982 .

[33]  H. Sakata,et al.  Neural representation of three-dimensional features of manipulation objects with stereopsis , 1999, Experimental Brain Research.

[34]  M. Jeannerod.  Intersegmental coordination during reaching at natural visual objects , 1981 .

[35]  R. Andersen,et al.  Memory related motor planning activity in posterior parietal cortex of macaque , 1988, Experimental Brain Research.

[36]  A. Georgopoulos,et al.  Parietal cortex neurons of the monkey related to the visual guidance of hand movement , 1990, Experimental Brain Research.

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

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

[39]  Charles Wheatstone.  On some remarkable and hitherto unobserved phenomena of binocular vision. , 1962 .

[40]  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.

[41]  J. Gottlieb.  From Thought to Action: The Parietal Cortex as a Bridge between Perception, Action, and Cognition , 2007, Neuron.

[42]  S. R. Lehky,et al.  Comparison of shape encoding in primate dorsal and ventral visual pathways. , 2007, Journal of neurophysiology.

[43]  G. Orban,et al.  Charting the Lower Superior Temporal Region, a New Motion-Sensitive Region in Monkey Superior Temporal Sulcus , 2006, The Journal of Neuroscience.

[44]  Hideo Sakata,et al.  Neural mechanisms of three-dimensional vision , 2005, Neuroscience Research.

[45]  J. Mandeville,et al.  Vascular filters of functional MRI: Spatial localization using BOLD and CBV contrast , 1999, Magnetic resonance in medicine.

[46]  R. Andersen,et al.  The posterior parietal cortex: Sensorimotor interface for the planning and online control of visually guided movements , 2006, Neuropsychologia.

[47]  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.

[48]  M. Goldberg,et al.  The representation of visual salience in monkey parietal cortex , 1998, Nature.

[49]  G. Orban,et al.  Observing Others: Multiple Action Representation in the Frontal Lobe , 2005, Science.

[50]  Simon J Watt,et al.  The visual control of reaching and grasping: binocular disparity and motion parallax. , 2003, Journal of experimental psychology. Human perception and performance.

[51]  Olivier J. Blanchard.  The Basic Mechanisms , 1998 .

[52]  M. Goldberg,et al.  Saccades, salience and attention: the role of the lateral intraparietal area in visual behavior. , 2006, Progress in brain research.

[53]  D. V. van Essen,et al.  Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto‐occipital cortex , 2000, The Journal of comparative neurology.

[54]  D. V. van Essen,et al.  The Processing of Visual Shape in the Cerebral Cortex of Human and Nonhuman Primates: A Functional Magnetic Resonance Imaging Study , 2004, The Journal of Neuroscience.

[55]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[56]  John H. R. Maunsell,et al.  Shape selectivity in primate lateral intraparietal cortex , 1998, Nature.

[57]  R. Andersen,et al.  Visual receptive field organization and cortico‐cortical connections of the lateral intraparietal area (area LIP) in the macaque , 1990, The Journal of comparative neurology.

[58]  U. Castiello.  The neuroscience of grasping , 2005, Nature Reviews Neuroscience.

[59]  M. Jeannerod.  The formation of finger grip during prehension. A cortically mediated visuomotor pattern , 1986, Behavioural Brain Research.

[60]  Y. Miyashita,et al.  Functional Magnetic Resonance Imaging of Macaque Monkeys Performing Visually Guided Saccade Tasks Comparison of Cortical Eye Fields with Humans , 2004, Neuron.

[61]  G. Luppino,et al.  Cortical connections of the inferior parietal cortical convexity of the macaque monkey. , 2006, Cerebral cortex.

[62]  Keiji Tanaka,et al.  Inferotemporal cortex and object vision. , 1996, Annual review of neuroscience.

[63]  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.

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

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

[66]  R. Harwerth,et al.  Fusional vergence ranges of the monkey: A behavioral study , 1979, Experimental Brain Research.

[67]  D. V. van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. , 2005, NeuroImage.

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

[69]  G. Orban,et al.  Visual Motion Processing Investigated Using Contrast Agent-Enhanced fMRI in Awake Behaving Monkeys , 2001, Neuron.

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

[71]  E. Brenner,et al.  A new view on grasping. , 1999, Motor control.

[72]  S. Ben Hamed,et al.  Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis , 2001, Experimental Brain Research.

[73]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

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

[75]  A. Murata,et al.  Largely segregated parietofrontal connections linking rostral intraparietal cortex (areas AIP and VIP) and the ventral premotor cortex (areas F5 and F4) , 1999, Experimental Brain Research.

[76]  Melvyn A. Goodale,et al.  The role of binocular vision in prehension: a kinematic analysis , 1992, Vision Research.

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

[78]  J. Aloimonos,et al.  On the kinetic depth effect , 1989, Biological Cybernetics.

[79]  Ping Wang,et al.  Cortical layer-dependent BOLD and CBV responses measured by spin-echo and gradient-echo fMRI: Insights into hemodynamic regulation , 2006, NeuroImage.