Interaction envelope: Local spatial representations of objects at all scales in scene-selective regions

While several cortical regions have been highlighted for their category selectivity (e.g., scene-selective regions like the parahippocampal place area, object selective regions like the lateral occipital complex), a growing trend in cognitive neuroscience has been to investigate what particular perceptual properties these regions calculate. Classical scene-selective regions have been particularly targeted in recent work as being sensitive to object size or other related properties. Here we test to which extent these regions are sensitive to spatial information of stimuli at any size. We introduce the spatial object property of “interaction envelope,” defined as the space through which a user trans-verses to interact with an object. In two functional magnetic resonance imaging experiments, we examined activity in a comprehensive set of perceptual regions of interest for when human participants viewed object images varying along the dimensions of interaction envelope and physical size. Importantly, we controlled for confounding perceptual and semantic object properties. We find that scene-selective regions are in fact sensitive to object interaction envelope for small, manipulable objects regardless of real-world size and task. Meanwhile, small-scale entity regions maintain selectivity to stimulus physical size. These results indicate that regions traditionally associated with scene processing may not be solely sensitive to larger object and scene information, but instead are calculating local spatial information of objects and scenes of all sizes.

[1]  Aude Oliva,et al.  Parametric Coding of the Size and Clutter of Natural Scenes in the Human Brain. , 2014, Cerebral cortex.

[2]  Gabriele Janzen,et al.  Selective neural representation of objects relevant for navigation , 2004, Nature Neuroscience.

[3]  A. Oliva,et al.  A Real-World Size Organization of Object Responses in Occipitotemporal Cortex , 2012, Neuron.

[4]  Yaacov Trope,et al.  Activation of ventral visual cortex supports distance representation , 2012 .

[5]  Jennifer K. E. Steeves,et al.  Transcranial Magnetic Stimulation to the Transverse Occipital Sulcus Affects Scene but Not Object Processing , 2012, Journal of Cognitive Neuroscience.

[6]  G. Aschersleben,et al.  The Theory of Event Coding (TEC): a framework for perception and action planning. , 2001, The Behavioral and brain sciences.

[7]  Melvyn A. Goodale,et al.  The role of apparent size in building- and object-specific regions of ventral visual cortex , 2011, Brain Research.

[8]  C. Cavina-Pratesi,et al.  Dissociable neural responses to hands and non-hand body parts in human left extrastriate visual cortex. , 2010, Journal of neurophysiology.

[9]  Rainer Goebel,et al.  Fundamentals of data analysis methods in fMRI , 2006 .

[10]  Soojin Park,et al.  Different roles of the parahippocampal place area (PPA) and retrosplenial cortex (RSC) in panoramic scene perception , 2009, NeuroImage.

[11]  M. Peelen,et al.  Body and Object Effectors: The Organization of Object Representations in High-Level Visual Cortex Reflects Body–Object Interactions , 2013, The Journal of Neuroscience.

[12]  Z Kourtzi,et al.  Representation of Perceived Object Shape by the Human Lateral Occipital Complex , 2001, Science.

[13]  Leslie G. Ungerleider,et al.  Dissociation of object and spatial visual processing pathways in human extrastriate cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Yaacov Trope,et al.  Do object-category selective regions in the ventral visual stream represent perceived distance information? , 2012, Brain and Cognition.

[15]  Soojin Park,et al.  Disentangling Scene Content from Spatial Boundary: Complementary Roles for the Parahippocampal Place Area and Lateral Occipital Complex in Representing Real-World Scenes , 2011, The Journal of Neuroscience.

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

[17]  Russell A. Epstein,et al.  Multiple object properties drive scene-selective regions. , 2014, Cerebral cortex.

[18]  R. Passingham,et al.  Objects automatically potentiate action: an fMRI study of implicit processing , 2003, The European journal of neuroscience.

[19]  Antonio Torralba,et al.  Statistics of natural image categories , 2003, Network.

[20]  Russell A. Epstein The cortical basis of visual scene processing , 2005 .

[21]  A. Wohlschläger,et al.  Visual motion priming by invisible actions , 2000, Vision Research.

[22]  Irving Biederman,et al.  Adaptation to objects in the lateral occipital complex (LOC): Shape or semantics? , 2009, Vision Research.

[23]  Eleanor A. Maguire,et al.  Retrosplenial Cortex Codes for Permanent Landmarks , 2012, PloS one.

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

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

[26]  Daniel D. Dilks,et al.  The Occipital Place Area Is Causally and Selectively Involved in Scene Perception , 2013, The Journal of Neuroscience.

[27]  S. Edelman,et al.  Differential Processing of Objects under Various Viewing Conditions in the Human Lateral Occipital Complex , 1999, Neuron.

[28]  M. Goodale,et al.  Two visual systems re-viewed , 2008, Neuropsychologia.

[29]  M. Bar,et al.  Cortical Analysis of Visual Context , 2003, Neuron.

[30]  Jennifer K. E. Steeves,et al.  TMS to the Lateral Occipital Cortex Disrupts Object Processing but Facilitates Scene Processing , 2011, Journal of Cognitive Neuroscience.

[31]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[32]  Dwight J. Kravitz,et al.  Real-World Scene Representations in High-Level Visual Cortex: It's the Spaces More Than the Places , 2011, The Journal of Neuroscience.

[33]  Eleanor A Maguire,et al.  A New Role for the Parahippocampal Cortex in Representing Space , 2011, The Journal of Neuroscience.

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

[35]  Dwight J. Kravitz,et al.  Task context impacts visual object processing differentially across the cortex , 2014, Proceedings of the National Academy of Sciences.

[36]  Michelle R. Greene,et al.  Disentangling scene content from its spatial boundary: Complementary roles for the PPA and LOC in representing real-world scenes , 2011 .

[37]  W. Macklin,et al.  Expression of Proteolipid Protein Gene in Spinal Cord Stem Cells and Early Oligodendrocyte Progenitor Cells Is Dispensable for Normal Cell Migration and Myelination , 2014, The Journal of Neuroscience.

[38]  Paul E. Downing,et al.  Viewpoint-Specific Scene Representations in Human Parahippocampal Cortex , 2003, Neuron.

[39]  Marvin M. Chun,et al.  Different roles of the parahippocampal place area (PPA) and retrosplenial cortex (RSC) in scene perception , 2010 .

[40]  Michelle R. Greene,et al.  Visual search in scenes involves selective and nonselective pathways , 2011, Trends in Cognitive Sciences.