The Visual Representation of 3D Object Orientation in Parietal Cortex

An accurate representation of three-dimensional (3D) object orientation is essential for interacting with the environment. Where and how the brain visually encodes 3D object orientation remains unknown, but prior studies suggest the caudal intraparietal area (CIP) may be involved. Here, we develop rigorous analytical methods for quantifying 3D orientation tuning curves, and use these tools to the study the neural coding of surface orientation. Specifically, we show that single neurons in area CIP of the rhesus macaque jointly encode the slant and tilt of a planar surface, and that across the population, the distribution of preferred slant-tilts is not statistically different from uniform. This suggests that all slant-tilt combinations are equally represented in area CIP. Furthermore, some CIP neurons are found to also represent the third rotational degree of freedom that determines the orientation of the image pattern on the planar surface. Together, the present results suggest that CIP is a critical neural locus for the encoding of all three rotational degrees of freedom specifying an object's 3D spatial orientation.

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

[2]  Daniel E. Koditschek,et al.  Visual servoing via navigation functions , 2002, IEEE Trans. Robotics Autom..

[3]  Mattia Marangon,et al.  Evidence for context sensitivity of grasp representations in human parietal and premotor cortices. , 2011, Journal of neurophysiology.

[4]  Kent A. Stevens,et al.  Slant-tilt: The visual encoding of surface orientation , 1983, Biological Cybernetics.

[5]  Yong Gu,et al.  Decoding of MSTd Population Activity Accounts for Variations in the Precision of Heading Perception , 2010, Neuron.

[6]  P. O. Bishop,et al.  Discrimination of orientation and position disparities by binocularly activated neurons in cat straite cortex. , 1977, Journal of neurophysiology.

[7]  Douglas B. Tweed,et al.  Non-commutativity in the brain , 1999, Nature.

[8]  John J. Craig,et al.  Introduction to Robotics Mechanics and Control , 1986 .

[9]  Ari Rosenberg,et al.  Responses to direction and transparent motion stimuli in area FST of the macaque , 2008, Visual Neuroscience.

[10]  R. Andersen,et al.  Response of MSTd neurons to simulated 3D orientation of rotating planes. , 2002, Journal of neurophysiology.

[11]  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.

[12]  John P. Snyder,et al.  Map Projections: A Working Manual , 2012 .

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

[14]  N. Issa,et al.  Subcortical Representation of Non-Fourier Image Features , 2010, The Journal of Neuroscience.

[15]  D. Gubbins,et al.  Encyclopedia of geomagnetism and paleomagnetism , 2007 .

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

[17]  B G Cumming,et al.  Responses of Macaque V1 Neurons to Binocular Orientation Differences , 2001, The Journal of Neuroscience.

[18]  R. Fox,et al.  The computation of retinal disparity , 1985, Perception & psychophysics.

[19]  John J. Craig Zhu,et al.  Introduction to robotics mechanics and control , 1991 .

[20]  R. Weale Vision. A Computational Investigation Into the Human Representation and Processing of Visual Information. David Marr , 1983 .

[21]  Steven M. LaValle,et al.  Deterministic sampling methods for spheres and SO(3) , 2004, IEEE International Conference on Robotics and Automation, 2004. Proceedings. ICRA '04. 2004.

[22]  Dora E Angelaki,et al.  Macaque Parieto-Insular Vestibular Cortex: Responses to Self-Motion and Optic Flow , 2010, Journal of Neuroscience.

[23]  Takahisa M. Sanada,et al.  Representation of 3-D surface orientation by velocity and disparity gradient cues in area MT. , 2012, Journal of Neurophysiology.

[24]  T. Haslwanter Mathematics of three-dimensional eye rotations , 1995, Vision Research.

[25]  Muge M. Bakircioglu,et al.  Mapping visual cortex in monkeys and humans using surface-based atlases , 2001, Vision Research.

[26]  Takahisa M. Sanada,et al.  Encoding of three-dimensional surface slant in cat visual areas 17 and 18. , 2006, Journal of neurophysiology.

[27]  Ivan Toni,et al.  Perceptuo-Motor Interactions during Prehension Movements , 2008, The Journal of Neuroscience.

[28]  R. Freeman,et al.  Oblique effect: a neural basis in the visual cortex. , 2003, Journal of neurophysiology.

[29]  Christopher Bingham An Antipodally Symmetric Distribution on the Sphere , 1974 .

[30]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[31]  H. Sakata,et al.  Functional and histological properties of caudal intraparietal area of macaque monkey , 2010, Neuroscience.

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

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

[34]  David M. Smith,et al.  Learning-Related Development of Context-Specific Neuronal Responses to Places and Events: The Hippocampal Role in Context Processing , 2006, The Journal of Neuroscience.

[35]  David R. Anderson,et al.  Model selection and multimodel inference : a practical information-theoretic approach , 2003 .

[36]  Dora E Angelaki,et al.  Control of eye orientation: where does the brain's role end and the muscle's begin? , 2004, The European journal of neuroscience.

[37]  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.

[38]  A. B. Bonds,et al.  Are primate lateral geniculate nucleus (LGN) cells really sensitive to orientation or direction? , 2002, Visual Neuroscience.

[39]  C. Blakemore,et al.  A second neural mechanism of binocular depth discrimination , 1972, The Journal of physiology.

[40]  Ari Rosenberg,et al.  The Y Cell Visual Pathway Implements a Demodulating Nonlinearity , 2011, Neuron.

[41]  J. Crawford,et al.  Neural control of three-dimensional eye and head movements , 2003, Current Opinion in Neurobiology.

[42]  I. Ohzawa,et al.  Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. , 1993, Journal of neurophysiology.

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

[44]  D. Bradley,et al.  Neural population code for fine perceptual decisions in area MT , 2005, Nature Neuroscience.