Cortical Transformation of Stimulus Space in Order to Linearize a Linearly Inseparable Task

The human brain is able to learn difficult categorization tasks, even ones that have linearly inseparable boundaries; however, it is currently unknown how it achieves this computational feat. We investigated this by training participants on an animal categorization task with a linearly inseparable prototype structure in a morph shape space. Participants underwent fMRI scans before and after 4 days of behavioral training. Widespread representational changes were found throughout the brain, including an untangling of the categories' neural patterns that made them more linearly separable after behavioral training. These neural changes were task dependent, as they were only observed while participants were performing the categorization task, not during passive viewing. Moreover, they were found to occur in frontal and parietal areas, rather than ventral temporal cortices, suggesting that they reflected attentional and decisional reweighting, rather than changes in object recognition templates. These results illustrate how the brain can flexibly transform neural representational space to solve computationally challenging tasks.

[1]  S. Edelman,et al.  Representation of object similarity in human vision: psychophysics and a computational model , 1998, Vision Research.

[2]  Carol A. Seger,et al.  Generalization in Category Learning: The Roles of Representational and Decisional Uncertainty , 2015, The Journal of Neuroscience.

[3]  Kingson Man,et al.  Multivariate cross-classification: applying machine learning techniques to characterize abstraction in neural representations , 2015, Front. Hum. Neurosci..

[4]  Michael L. Mack,et al.  Dynamic updating of hippocampal object representations reflects new conceptual knowledge , 2016, Proceedings of the National Academy of Sciences.

[5]  M. Posner,et al.  On the genesis of abstract ideas. , 1968, Journal of experimental psychology.

[6]  Li Su,et al.  A Toolbox for Representational Similarity Analysis , 2014, PLoS Comput. Biol..

[7]  Su Keun Jeong,et al.  Behaviorally Relevant Abstract Object Identity Representation in the Human Parietal Cortex , 2016, The Journal of Neuroscience.

[8]  Nikolaus Kriegeskorte,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[9]  John-Dylan Haynes,et al.  The Relationship between Perceptual Decision Variables and Confidence in the Human Brain. , 2016, Cerebral cortex.

[10]  David D. Cox,et al.  Untangling invariant object recognition , 2007, Trends in Cognitive Sciences.

[11]  H. P. Op de Beeck,et al.  Task Context Overrules Object- and Category-Related Representational Content in the Human Parietal Cortex , 2017, Cerebral cortex.

[12]  Alexander Borst,et al.  How does Nature Program Neuron Types? , 2008, Front. Neurosci..

[13]  Stephen D. Mayhew,et al.  Article Learning Shapes the Representation of Behavioral Choice in the Human Brain , 2022 .

[14]  Yaoda Xu,et al.  Goal-Directed Visual Processing Differentially Impacts Human Ventral and Dorsal Visual Representations , 2017, The Journal of Neuroscience.

[15]  S Edelman,et al.  Effects of parametric manipulation of inter-stimulus similarity on 3D object categorization. , 1999, Spatial vision.

[16]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[17]  Carol A. Seger,et al.  Occipitotemporal Category Representations Are Sensitive to Abstract Category Boundaries Defined by Generalization Demands , 2017, The Journal of Neuroscience.

[18]  Richard B. Ivry,et al.  Hemispheric Asymmetries , 2000, Encyclopedia of Personality and Individual Differences.

[19]  Martin N. Hebart,et al.  Human visual and parietal cortex encode visual choices independent of motor plans , 2012, NeuroImage.

[20]  David J. Freedman,et al.  Experience-dependent representation of visual categories in parietal cortex , 2006, Nature.

[21]  M. Giese,et al.  Flexible Coding for Categorical Decisions in the Human Brain , 2007, The Journal of Neuroscience.

[22]  Michael L. Mack,et al.  Decoding the Brain’s Algorithm for Categorization from Its Neural Implementation , 2013, Current Biology.

[23]  P J Reber,et al.  Cortical areas supporting category learning identified using functional MRI. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[24]  S. Edelman,et al.  Toward direct visualization of the internal shape representation space by fMRI , 1998, Psychobiology.

[25]  Anthony Widjaja,et al.  Learning with Kernels: Support Vector Machines, Regularization, Optimization, and Beyond , 2003, IEEE Transactions on Neural Networks.

[26]  Jonathan R. Folstein,et al.  Category Learning Stretches Neural Representations in Visual Cortex , 2015, Current directions in psychological science.

[27]  Jonathan R. Folstein,et al.  How category learning affects object representations: not all morphspaces stretch alike. , 2012, Journal of experimental psychology. Learning, memory, and cognition.

[28]  Jonathan R. Folstein,et al.  Category learning increases discriminability of relevant object dimensions in visual cortex. , 2013, Cerebral cortex.

[29]  Michael C. Hout,et al.  Multidimensional Scaling , 2003, Encyclopedic Dictionary of Archaeology.

[30]  Margaret Henderson,et al.  Human frontoparietal cortex represents behaviorally relevant target status based on abstract object features. , 2019, Journal of neurophysiology.

[31]  D J Field,et al.  Relations between the statistics of natural images and the response properties of cortical cells. , 1987, Journal of the Optical Society of America. A, Optics and image science.

[32]  Robert L. Goldstone Influences of categorization on perceptual discrimination. , 1994, Journal of experimental psychology. General.

[33]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[34]  Hervé Abdi,et al.  How to compute reliability estimates and display confidence and tolerance intervals for pattern classifiers using the Bootstrap and 3-way multidimensional scaling (DISTATIS) , 2009, NeuroImage.

[35]  Lotfi B Merabet,et al.  Visual Topography of Human Intraparietal Sulcus , 2007, The Journal of Neuroscience.

[36]  Russell A Poldrack,et al.  Hemispheric asymmetries and individual differences in visual concept learning as measured by functional MRI , 2000, Neuropsychologia.

[37]  W. Torgerson Multidimensional scaling: I. Theory and method , 1952 .

[38]  R. Nosofsky Attention, similarity, and the identification-categorization relationship. , 1986, Journal of experimental psychology. General.

[39]  L. Squire,et al.  The learning of categories: parallel brain systems for item memory and category knowledge. , 1993, Science.

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

[41]  S. Kastner,et al.  Two hierarchically organized neural systems for object information in human visual cortex , 2008, Nature Neuroscience.