Beyond Shape: How You Learn about Objects Affects How They Are Represented in Visual Cortex

Background Experience can alter how objects are represented in the visual cortex. But experience can take different forms. It is unknown whether the kind of visual experience systematically alters the nature of visual cortical object representations. Methodology/Principal Findings We take advantage of different training regimens found to produce qualitatively different types of perceptual expertise behaviorally in order to contrast the neural changes that follow different kinds of visual experience with the same objects. Two groups of participants went through training regimens that required either subordinate-level individuation or basic-level categorization of a set of novel, artificial objects, called “Ziggerins”. fMRI activity of a region in the right fusiform gyrus increased after individuation training and was correlated with the magnitude of configural processing of the Ziggerins observed behaviorally. In contrast, categorization training caused distributed changes, with increased activity in the medial portion of the ventral occipito-temporal cortex relative to more lateral areas. Conclusions/Significance Our results demonstrate that the kind of experience with a category of objects can systematically influence how those objects are represented in visual cortex. The demands of prior learning experience therefore appear to be one factor determining the organization of activity patterns in visual cortex.

[1]  M. Tarr,et al.  Levels of categorization in visual recognition studied using functional magnetic resonance imaging , 1997, Current Biology.

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

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

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

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

[6]  T A Polk,et al.  The neural development and organization of letter recognition: evidence from functional neuroimaging, computational modeling, and behavioral studies. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[7]  J. Haxby,et al.  Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects , 1999, Nature Neuroscience.

[8]  Russell A. Epstein,et al.  The Parahippocampal Place Area Recognition, Navigation, or Encoding? , 1999, Neuron.

[9]  M. Tarr,et al.  Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects , 1999, Nature Neuroscience.

[10]  Isabel Gauthier,et al.  What constrains the organization of the ventral temporal cortex? , 2000, Trends in Cognitive Sciences.

[11]  J. Wagemans,et al.  The Representation of Shape in the Context of Visual Object Categorization Tasks , 2000, NeuroImage.

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

[13]  J. Tanaka The entry point of face recognition: evidence for face expertise. , 2001, Journal of experimental psychology. General.

[14]  N. Kanwisher,et al.  The Human Body , 2001 .

[15]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[16]  R. Malach,et al.  The topography of high-order human object areas , 2002, Trends in Cognitive Sciences.

[17]  M. Tarr,et al.  Unraveling mechanisms for expert object recognition: bridging brain activity and behavior. , 2002, Journal of experimental psychology. Human perception and performance.

[18]  Jean-Luc Velay,et al.  Visual presentation of single letters activates a premotor area involved in writing , 2003, NeuroImage.

[19]  M. Riesenhuber,et al.  Face processing in humans is compatible with a simple shape–based model of vision , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[20]  J. Rodd,et al.  Processing Objects at Different Levels of Specificity , 2004, Journal of Cognitive Neuroscience.

[21]  Isabel Gauthier,et al.  Letter processing in the visual system: Different activation patterns for single letters and strings , 2005, Cognitive, affective & behavioral neuroscience.

[22]  David L. Sheinberg,et al.  The Training and Transfer of Real-World Perceptual Expertise , 2005, Psychological science.

[23]  Yaoda Xu Revisiting the role of the fusiform face area in visual expertise. , 2005, Cerebral cortex.

[24]  Michael X. Cohen,et al.  Neural Mechanisms of Expert Skills in Visual Working Memory , 2006, The Journal of Neuroscience.

[25]  I. Biederman,et al.  What makes faces special? , 2006, Vision Research.

[26]  E. Miller,et al.  Experience-dependent sharpening of visual shape selectivity in inferior temporal cortex. , 2005, Cerebral cortex.

[27]  N. Kanwisher,et al.  Discrimination Training Alters Object Representations in Human Extrastriate Cortex , 2006, The Journal of Neuroscience.

[28]  James W. Tanaka,et al.  A Reevaluation of the Electrophysiological Correlates of Expert Object Processing , 2006, Journal of Cognitive Neuroscience.

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

[30]  Cindy M. Bukach,et al.  Beyond faces and modularity: the power of an expertise framework , 2006, Trends in Cognitive Sciences.

[31]  I. Gauthier,et al.  An analysis of letter expertise in a levels-of-categorization framework , 2007 .

[32]  Bradford Z. Mahon,et al.  Action-Related Properties Shape Object Representations in the Ventral Stream , 2007, Neuron.

[33]  Russell A. Poldrack,et al.  The Neural Substrates of Visual Perceptual Learning of Words: Implications for the Visual Word Form Area Hypothesis , 2007, Journal of Cognitive Neuroscience.

[34]  M. Riesenhuber,et al.  Categorization Training Results in Shape- and Category-Selective Human Neural Plasticity , 2007, Neuron.

[35]  Eric T. Carlson,et al.  A neural code for three-dimensional object shape in macaque inferotemporal cortex , 2008, Nature Neuroscience.

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

[37]  Johan Wagemans,et al.  Perceived Shape Similarity among Unfamiliar Objects and the Organization of the Human Object Vision Pathway , 2008, The Journal of Neuroscience.

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

[39]  David L. Sheinberg,et al.  The role of category learning in the acquisition and retention of perceptual expertise: A behavioral and neurophysiological study , 2008, Brain Research.

[40]  I. Gauthier,et al.  Conditions for Facelike Expertise with Objects Becoming a Ziggerin Expert—but Which Type? , 2022 .

[41]  Isabel Gauthier,et al.  Expertise with characters in alphabetic and nonalphabetic writing systems engage overlapping occipito-temporal areas , 2009, Cognitive neuropsychology.

[42]  Erin M. Harley,et al.  Activity in the fusiform face area supports expert perception in radiologists and does not depend upon holistic processing of images , 2009, Medical Imaging.

[43]  Johan Wagemans,et al.  Subordinate Categorization Enhances the Neural Selectivity in Human Object-selective Cortex for Fine Shape Differences , 2009, Journal of Cognitive Neuroscience.

[44]  K. James,et al.  The role of sensorimotor learning in the perception of letter-like forms: Tracking the causes of neural specialization for letters , 2009, Cognitive neuropsychology.

[45]  Yetta Kwailing Wong,et al.  A Multimodal Neural Network Recruited by Expertise with Musical Notation , 2010, Journal of Cognitive Neuroscience.