Curvature-processing network in macaque visual cortex

Significance The brain processes visual stimuli along different feature dimensions, including edge orientation, visual motion, and color. To expedite visual processing, cells that process a common visual dimension are often anatomically grouped in cortical columns, patches, and/or areas. Here, we tested the hypothesis that (i) image curvature is one of these fundamental visual dimensions and, as such, (ii) curvature-selective cells are grouped together in discrete cortical areas. Using neuroimaging techniques, we confirmed this hypothesis and localized the curvature-processing sites in extrastriate visual cortex. These sites lay along a common cortical strip, spanning lower- to higher-level processing stages. Furthermore, the curvature-processing sites are adjacent to the well-known face-processing cortical areas, suggesting a possible functional link between them. Our visual environment abounds with curved features. Thus, the goal of understanding visual processing should include the processing of curved features. Using functional magnetic resonance imaging in behaving monkeys, we demonstrated a network of cortical areas selective for the processing of curved features. This network includes three distinct hierarchically organized regions within the ventral visual pathway: a posterior curvature-biased patch (PCP) located in the near-foveal representation of dorsal V4, a middle curvature-biased patch (MCP) located on the ventral lip of the posterior superior temporal sulcus (STS) in area TEO, and an anterior curvature-biased patch (ACP) located just below the STS in anterior area TE. Our results further indicate that the processing of curvature becomes increasingly complex from PCP to ACP. The proximity of the curvature-processing network to the well-known face-processing network suggests a possible functional link between them.

[1]  J. P. Guilford,et al.  Illusory Movement from a Rotating Barber Pole , 1929 .

[2]  S. A. Talbot,et al.  Physiological Studies on Neural Mechanisms of Visual Localization and Discrimination , 1941 .

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

[4]  D. Whitteridge,et al.  The representation of the visual field on the cerebral cortex in monkeys , 1961, The Journal of physiology.

[5]  D. Hubel,et al.  Stereoscopic Vision in Macaque Monkey: Cells sensitive to Binocular Depth in Area 18 of the Macaque Monkey Cortex , 1970, Nature.

[6]  L. Riggs Curvature as a Feature of Pattern Vision , 1973, Science.

[7]  D. Hubel,et al.  Anatomical demonstration of orientation columns in macaque monkey , 1978, The Journal of comparative neurology.

[8]  R. Desimone,et al.  Visual areas in the temporal cortex of the macaque , 1979, Brain Research.

[9]  E. Switkes,et al.  Deoxyglucose analysis of retinotopic organization in primate striate cortex. , 1982, Science.

[10]  Donald D. Hoffman,et al.  Parts of recognition , 1984, Cognition.

[11]  D. Hubel,et al.  Anatomy and physiology of a color system in the primate visual cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  S. Petersen,et al.  Direction-specific adaptation in area MT of the owl monkey , 1985, Brain Research.

[13]  I. Biederman Recognition-by-components: a theory of human image understanding. , 1987, Psychological review.

[14]  Terrence J. Sejnowski,et al.  Network model of shape-from-shading: neural function arises from both receptive and projective fields , 1988, Nature.

[15]  C. Gross,et al.  Visuotopic organization and extent of V3 and V4 of the macaque , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  A Treisman,et al.  Feature analysis in early vision: evidence from search asymmetries. , 1988, Psychological review.

[17]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. I. Ocular dominance, binocular interactions, and baseline conditions , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. III. Color , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  R. Tootell,et al.  Functional anatomy of the second visual area (V2) in the macaque , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  Leslie G. Ungerleider,et al.  Visual topography of area TEO in the macaque , 1991, The Journal of comparative neurology.

[21]  Keiji Tanaka,et al.  Coding visual images of objects in the inferotemporal cortex of the macaque monkey. , 1991, Journal of neurophysiology.

[22]  Minami Ito,et al.  Columns for visual features of objects in monkey inferotemporal cortex , 1992, Nature.

[23]  D. V. van Essen,et al.  Selectivity for polar, hyperbolic, and Cartesian gratings in macaque visual cortex. , 1993, Science.

[24]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[25]  S. Kosslyn,et al.  The Perception of Curvature Can Be Selectively Disrupted in Prosopagnosia , 1995, Brain and Cognition.

[26]  T. Allison,et al.  Face-sensitive regions in human extrastriate cortex studied by functional MRI. , 1995, Journal of neurophysiology.

[27]  D. C. Essen,et al.  Neural responses to polar, hyperbolic, and Cartesian gratings in area V4 of the macaque monkey. , 1996, Journal of neurophysiology.

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

[29]  K. Hikosaka Responsiveness of neurons in the posterior inferotemporal cortex to visual patterns in the macaque monkey , 1997, Behavioural Brain Research.

[30]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[31]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[32]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[33]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[34]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[35]  C. Connor,et al.  Responses to contour features in macaque area V4. , 1999, Journal of neurophysiology.

[36]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[37]  Ravi S. Menon,et al.  An fMRI study of the selective activation of human extrastriate form vision areas by radial and concentric gratings , 2000, Current Biology.

[38]  I. Gauthier,et al.  Expertise for cars and birds recruits brain areas involved in face recognition , 2000, Nature Neuroscience.

[39]  C. Connor,et al.  Shape representation in area V4: position-specific tuning for boundary conformation. , 2001, Journal of neurophysiology.

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

[41]  Norbert Krüger,et al.  Learning Object Representations Using A Priori Constraints Within ORASSYLL , 2001, Neural Computation.

[42]  R. Tootell,et al.  Where is 'dorsal V4' in human visual cortex? Retinotopic, topographic and functional evidence. , 2001, Cerebral cortex.

[43]  C. Connor,et al.  Population coding of shape in area V4 , 2002, Nature Neuroscience.

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

[45]  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.

[46]  Doris Y. Tsao,et al.  Neuroimaging Weighs In: Humans Meet Macaques in “Primate” Visual Cortex , 2003, The Journal of Neuroscience.

[47]  N. Logothetis,et al.  Anatomical and functional MR imaging in the macaque monkey using a vertical large-bore 7 Tesla setup. , 2004, Magnetic resonance imaging.

[48]  Charles E Connor,et al.  Underlying principles of visual shape selectivity in posterior inferotemporal cortex , 2004, Nature Neuroscience.

[49]  S. Thorpe,et al.  How parallel is visual processing in the ventral pathway? , 2004, Trends in Cognitive Sciences.

[50]  I. Biederman,et al.  Representation of regular and irregular shapes in macaque inferotemporal cortex. , 2005, Cerebral cortex.

[51]  I. Biederman,et al.  Tuning for shape dimensions in macaque inferior temporal cortex , 2005, The European journal of neuroscience.

[52]  Doris Y. Tsao,et al.  A Cortical Region Consisting Entirely of Face-Selective Cells , 2006, Science.

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

[54]  J. Hegdé,et al.  A comparative study of shape representation in macaque visual areas v2 and v4. , 2007, Cerebral cortex.

[55]  N. Kanwisher,et al.  A stable topography of selectivity for unfamiliar shape classes in monkey inferior temporal cortex. , 2008, Cerebral cortex.

[56]  Leslie G. Ungerleider,et al.  Perception of emotional expressions is independent of face selectivity in monkey inferior temporal cortex , 2008, Proceedings of the National Academy of Sciences.

[57]  Robert Desimone,et al.  Cortical connections of area V4 in the macaque. , 2000, Cerebral cortex.

[58]  Doris Y. Tsao,et al.  Patches with Links: A Unified System for Processing Faces in the Macaque Temporal Lobe , 2008, Science.

[59]  Leslie G. Ungerleider,et al.  Object representations in the temporal cortex of monkeys and humans as revealed by functional magnetic resonance imaging. , 2009, Journal of neurophysiology.

[60]  Roger B. H. Tootell,et al.  Does Retinotopy Influence Cortical Folding in Primate Visual Cortex? , 2009, The Journal of Neuroscience.

[61]  W. Vanduffel,et al.  Visual Field Map Clusters in Macaque Extrastriate Visual Cortex , 2009, The Journal of Neuroscience.

[62]  Doris Y. Tsao,et al.  A face feature space in the macaque temporal lobe , 2009, Nature Neuroscience.

[63]  Doris Y. Tsao,et al.  Functional Compartmentalization and Viewpoint Generalization Within the Macaque Face-Processing System , 2010, Science.

[64]  Lisa R. Betts,et al.  Decoding of Faces and Face Components in Face-Sensitive Human Visual Cortex , 2010, Front. Psychology.

[65]  Hugh R. Wilson,et al.  Heterogeneous Structure in Face-selective Human Occipito-temporal Cortex , 2010, Journal of Cognitive Neuroscience.

[66]  C. Connor,et al.  Neural representations for object perception: structure, category, and adaptive coding. , 2011, Annual review of neuroscience.

[67]  Brittany S. Cassidy,et al.  Lower-Level Stimulus Features Strongly Influence Responses in the Fusiform Face Area , 2010, Cerebral cortex.

[68]  Leslie G. Ungerleider,et al.  Relationship between Functional Magnetic Resonance Imaging-Identified Regions and Neuronal Category Selectivity , 2011, The Journal of Neuroscience.

[69]  N. Logothetis,et al.  fMRI of the Face-Processing Network in the Ventral Temporal Lobe of Awake and Anesthetized Macaques , 2011, Neuron.

[70]  Natalia Y. Bilenko,et al.  The “Parahippocampal Place Area” Responds Preferentially to High Spatial Frequencies in Humans and Monkeys , 2011, PLoS biology.

[71]  Leslie G. Ungerleider,et al.  Scene-Selective Cortical Regions in Human and Nonhuman Primates , 2011, The Journal of Neuroscience.

[72]  James J. DiCarlo,et al.  How Does the Brain Solve Visual Object Recognition? , 2012, Neuron.

[73]  Doris Y. Tsao,et al.  What Makes a Cell Face Selective? The Importance of Contrast , 2012, Neuron.

[74]  Roger B. H. Tootell,et al.  A Cardinal Orientation Bias in Scene-Selective Visual Cortex , 2012, The Journal of Neuroscience.

[75]  Cortical Shape Adaptation Transforms a Circle Into a Hexagon , 2012, Psychological science.

[76]  Elias B. Issa,et al.  Large-Scale, High-Resolution Neurophysiological Maps Underlying fMRI of Macaque Temporal Lobe , 2013, The Journal of Neuroscience.

[77]  J. Reynolds,et al.  Trade-off between curvature tuning and position invariance in visual area V4 , 2013, Proceedings of the National Academy of Sciences.

[78]  Anirvan S. Nandy,et al.  The Fine Structure of Shape Tuning in Area V4 , 2013, Neuron.

[79]  Xueqi Cheng,et al.  A Network for Scene Processing in the Macaque Temporal Lobe , 2013, Neuron.

[80]  R. Tootell,et al.  Thinking Outside the Box: Rectilinear Shapes Selectively Activate Scene-Selective Cortex , 2014, The Journal of Neuroscience.