Orientation Decoding Depends on Maps, Not Columns

The representation of orientation in primary visual cortex (V1) has been examined at a fine spatial scale corresponding to the columnar architecture. We present functional magnetic resonance imaging (fMRI) measurements providing evidence for a topographic map of orientation preference in human V1 at a much coarser scale, in register with the angular-position component of the retinotopic map of V1. This coarse-scale orientation map provides a parsimonious explanation for why multivariate pattern analysis methods succeed in decoding stimulus orientation from fMRI measurements, challenging the widely held assumption that decoding results reflect sampling of spatial irregularities in the fine-scale columnar architecture. Decoding stimulus attributes and cognitive states from fMRI measurements has proven useful for a number of applications, but our results demonstrate that the interpretation cannot assume decoding reflects or exploits columnar organization.

[1]  Eero P. Simoncelli,et al.  Implicit encoding of prior probabilities in optimal neural populations , 2010, NIPS.

[2]  Damien J. Mannion,et al.  Orientation anisotropies in human visual cortex. , 2010, Journal of neurophysiology.

[3]  Hans P. Op de Beeck,et al.  Against hyperacuity in brain reading: Spatial smoothing does not hurt multivariate fMRI analyses? , 2010, NeuroImage.

[4]  Yasuhito Sawahata,et al.  Spatial smoothing hurts localization but not information: Pitfalls for brain mappers , 2010, NeuroImage.

[5]  A. Shmuel,et al.  Mechanisms underlying decoding at 7 T: Ocular dominance columns, broad structures, and macroscopic blood vessels in V1 convey information on the stimulated eye , 2010, NeuroImage.

[6]  Nikolaus Kriegeskorte,et al.  How does an fMRI voxel sample the neuronal activity pattern: Compact-kernel or complex spatiotemporal filter? , 2010, NeuroImage.

[7]  Justin L. Gardner,et al.  Is cortical vasculature functionally organized? , 2010, NeuroImage.

[8]  Jascha D. Swisher,et al.  Multiscale Pattern Analysis of Orientation-Selective Activity in the Primary Visual Cortex , 2010, The Journal of Neuroscience.

[9]  D. Heeger,et al.  Decoding and Reconstructing Color from Responses in Human Visual Cortex , 2009, The Journal of Neuroscience.

[10]  B. Spehar,et al.  The Foveal Confluence in Human Visual Cortex , 2009, The Journal of Neuroscience.

[11]  Jochen Triesch,et al.  Learning independent causes in natural images explains the spacevariant oblique effect , 2009, 2009 IEEE 8th International Conference on Development and Learning.

[12]  Colin W. G. Clifford,et al.  Discrimination of the local orientation structure of spiral Glass patterns early in human visual cortex , 2009, NeuroImage.

[13]  W. K. Simmons,et al.  Circular analysis in systems neuroscience: the dangers of double dipping , 2009, Nature Neuroscience.

[14]  H. Pashler,et al.  Puzzlingly High Correlations in fMRI Studies of Emotion, Personality, and Social Cognition 1 , 2009, Perspectives on psychological science : a journal of the Association for Psychological Science.

[15]  Kendrick N Kay,et al.  I can see what you see , 2009, Nature Neuroscience.

[16]  F. Tong,et al.  Decoding reveals the contents of visual working memory in early visual areas , 2009, Nature.

[17]  Miranda Scolari,et al.  Estimating the influence of attention on population codes in human visual cortex using voxel-based tuning functions , 2009, NeuroImage.

[18]  Justin L. Gardner,et al.  Executed and Observed Movements Have Different Distributed Representations in Human aIPS , 2008, The Journal of Neuroscience.

[19]  J. Movshon,et al.  Maps of Visual Space in Human Occipital Cortex Are Retinotopic, Not Spatiotopic , 2008, The Journal of Neuroscience.

[20]  J. Gallant,et al.  Identifying natural images from human brain activity , 2008, Nature.

[21]  N. Kanwisher,et al.  Interpreting fMRI data: maps, modules and dimensions , 2008, Nature Reviews Neuroscience.

[22]  Brian A. Wandell,et al.  Population receptive field estimates in human visual cortex , 2008, NeuroImage.

[23]  B. Wandell,et al.  Visual Field Maps in Human Cortex , 2007, Neuron.

[24]  Lawrence C. Sincich,et al.  Complete Pattern of Ocular Dominance Columns in Human Primary Visual Cortex , 2007, The Journal of Neuroscience.

[25]  D. Ringach.  On the Origin of the Functional Architecture of the Cortex , 2007, PloS one.

[26]  D. Heeger,et al.  Two Retinotopic Visual Areas in Human Lateral Occipital Cortex , 2006, The Journal of Neuroscience.

[27]  Wim Vanduffel,et al.  The Radial Bias: A Different Slant on Visual Orientation Sensitivity in Human and Nonhuman Primates , 2006, Neuron.

[28]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[29]  Sooyoung Chung,et al.  Highly ordered arrangement of single neurons in orientation pinwheels , 2006, Nature.

[30]  G. Rees,et al.  Neuroimaging: Decoding mental states from brain activity in humans , 2006, Nature Reviews Neuroscience.

[31]  F. Tong,et al.  Decoding Seen and Attended Motion Directions from Activity in the Human Visual Cortex , 2006, Current Biology.

[32]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[33]  G. Rees,et al.  Predicting the orientation of invisible stimuli from activity in human primary visual cortex , 2005, Nature Neuroscience.

[34]  Geoffrey M Boynton,et al.  Imaging orientation selectivity: decoding conscious perception in V1 , 2005, Nature Neuroscience.

[35]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

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

[37]  Michael P. Stryker,et al.  New Paradigm for Optical Imaging Temporally Encoded Maps of Intrinsic Signal , 2003, Neuron.

[38]  Gerald Westheimer,et al.  The distribution of preferred orientations in the peripheral visual field , 2003, Vision Research.

[39]  S. R. Jammalamadaka,et al.  Topics in Circular Statistics , 2001 .

[40]  C. Furmanski,et al.  An oblique effect in human primary visual cortex , 2000, Nature Neuroscience.

[41]  D J Heeger,et al.  Robust multiresolution alignment of MRI brain volumes , 2000, Magnetic resonance in medicine.

[42]  J. Duyn,et al.  Investigation of Low Frequency Drift in fMRI Signal , 1999, NeuroImage.

[43]  T Bonhoeffer,et al.  Orientation selectivity in pinwheel centers in cat striate cortex. , 1997, Science.

[44]  C. Gilbert,et al.  Distortions of visuotopic map match orientation singularities in primary visual cortex , 1997, Nature.

[45]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[46]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[47]  E. DeYoe,et al.  Mapping striate and extrastriate visual areas in human cerebral cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[48]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[49]  Adrian T. Lee,et al.  fMRI of human visual cortex , 1994, Nature.

[50]  Dave M. Stampe,et al.  Heuristic filtering and reliable calibration methods for video-based pupil-tracking systems , 1993 .

[51]  Y. Chino,et al.  Orientation bias of neurons in the lateral geniculate nucleus of macaque monkeys , 1990, Visual Neuroscience.

[52]  D. Tank,et al.  Brain magnetic resonance imaging with contrast dependent on blood oxygenation. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[53]  T. Wiesel,et al.  Functional architecture of cortex revealed by optical imaging of intrinsic signals , 1986, Nature.

[54]  G. Blasdel,et al.  Voltage-sensitive dyes reveal a modular organization in monkey striate cortex , 1986, Nature.

[55]  J D Schall,et al.  Retinal constraints on orientation specificity in cat visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  R. W. Rodieck,et al.  Parasol and midget ganglion cells of the human retina , 1985, The Journal of comparative neurology.

[57]  A. Leventhal,et al.  Relationship between preferred orientation and receptive field position of neurons in cat striate cortex , 1983, The Journal of comparative neurology.

[58]  R. L. Valois,et al.  The orientation and direction selectivity of cells in macaque visual cortex , 1982, Vision Research.

[59]  J Rovamo,et al.  Resolution of gratings oriented along and across meridians in peripheral vision. , 1982, Investigative ophthalmology & visual science.

[60]  W. Levick,et al.  Analysis of orientation bias in cat retina , 1982, The Journal of physiology.

[61]  W. Levick,et al.  Orientation bias of cat retinal ganglion cells , 1980, Nature.

[62]  S. Sherman,et al.  Receptive-field characteristics of neurons in cat striate cortex: Changes with visual field eccentricity. , 1976, Journal of neurophysiology.

[63]  D. W. Watkins,et al.  Grating visibility as a function of orientation and retinal eccentricity , 1975, Vision Research.

[64]  R. Mansfield,et al.  Neural Basis of Orientation Perception in Primate Vision , 1974, Science.

[65]  D. Hubel,et al.  Shape and arrangement of columns in cat's striate cortex , 1963, The Journal of physiology.

[66]  Y. Zhou,et al.  The orientation bias of LGN neurons shows topographic relation to area centralis in the cat retina , 2004, Experimental Brain Research.

[67]  S. Ogawa.  Brain magnetic resonance imaging with contrast-dependent oxygenation , 1990 .