Transformation of Visual Representations Across Ventral Stream Body-selective Patches

Although the neural processing of visual images of bodies is critical for survival, it is much less well understood than face processing. Functional imaging studies demonstrated body selective regions in primate inferior temporal cortex. To advance our understanding of how the visual brain represents bodies, we compared the representation of animate and inanimate objects in two such body patches with fMRI-guided single unit recordings in rhesus monkeys. We found that the middle Superior Temporal Sulcus body patch (MSB) distinguishes to a greater extent bodies from non-bodies than the anterior Superior Temporal Sulcus body patch (ASB). Importantly, ASB carried more viewpoint-tolerant information about body posture and body identity than MSB, while MSB showed greater orientation selectivity. Combined with previous work on faces, this suggests that an increase in view-tolerant representations, coupled with a refined individuation, along the visual hierarchy is a general property of information processing within the inferior temporal cortex.

[1]  S. Altmann,et al.  A FIELD STUDY OF THE SOCIOBIOLOGY OF RHESUS MONKEYS, MACACA MULATTA * , 1962, Annals of the New York Academy of Sciences.

[2]  Galit Yovel,et al.  A Revised Neural Framework for Face Processing. , 2015, Annual review of vision science.

[3]  Jeffrey N. Rouder,et al.  Bayes factor approaches for testing interval null hypotheses. , 2011, Psychological methods.

[4]  C. Darwin.  The Expression of the Emotions in Man and Animals , .

[5]  D. Sade.  An ethogram for Rhesus monkeys. I. Antithetical contrasts in posture and movement. , 1973, American journal of physical anthropology.

[6]  L. Tyler,et al.  Understanding What We See: How We Derive Meaning From Vision , 2015, Trends in Cognitive Sciences.

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

[8]  Doris Y. Tsao,et al.  Faces and objects in macaque cerebral cortex , 2003, Nature Neuroscience.

[9]  Dwight J. Kravitz,et al.  The ventral visual pathway: an expanded neural framework for the processing of object quality , 2013, Trends in Cognitive Sciences.

[10]  Paul Wright,et al.  Objects and Categories: Feature Statistics and Object Processing in the Ventral Stream , 2013, Journal of Cognitive Neuroscience.

[11]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[12]  Rufin Vogels,et al.  Shape Selectivity of Middle Superior Temporal Sulcus Body Patch Neurons , 2017, eNeuro.

[13]  Peter Janssen,et al.  Effective Connectivity Reveals Largely Independent Parallel Networks of Face and Body Patches , 2016, Current Biology.

[14]  Rufin Vogels,et al.  Tolerance of Macaque Middle STS Body Patch Neurons to Shape-preserving Stimulus Transformations , 2015, Journal of Cognitive Neuroscience.

[15]  Bruno Rossion,et al.  Constraining the cortical face network by neuroimaging studies of acquired prosopagnosia , 2008, NeuroImage.

[16]  Kendrick Kay,et al.  The Functional Neuroanatomy of Human Face Perception. , 2017, Annual review of vision science.

[17]  C. Gross,et al.  Representations of faces and body parts in macaque temporal cortex: a functional MRI study. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Wim Vanduffel,et al.  Stimulus representations in body-selective regions of the macaque cortex assessed with event-related fMRI , 2012, NeuroImage.

[19]  J. Sliwa,et al.  A dedicated network for social interaction processing in the primate brain , 2017, Science.

[20]  Ha Hong,et al.  Explicit information for category-orthogonal object properties increases along the ventral stream , 2016, Nature Neuroscience.

[21]  R. A. Hinde,et al.  COMMUNICATION BY POSTURES AND FACIAL EXPRESSIONS IN THE RHESUS MONKEY (MACACA MULATTA) , 2009 .

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

[23]  C. Gross,et al.  Neural representations of faces and body parts in macaque and human cortex: a comparative FMRI study. , 2009, Journal of neurophysiology.

[24]  N. Kanwisher,et al.  A Cortical Area Selective for Visual Processing of the Human Body , 2001, Science.

[25]  Guy A. Orban,et al.  Fine-grained stimulus representations in body selective areas of human occipito-temporal cortex , 2014, NeuroImage.

[26]  Malika Charrad,et al.  NbClust: An R Package for Determining the Relevant Number of Clusters in a Data Set , 2014 .

[27]  Bruno Rossion,et al.  The Face-Processing Network Is Resilient to Focal Resection of Human Visual Cortex , 2016, The Journal of Neuroscience.

[28]  Doris Y. Tsao,et al.  Single-Unit Recordings in the Macaque Face Patch System Reveal Limitations of fMRI MVPA , 2015, The Journal of Neuroscience.

[29]  P. Roelfsema,et al.  Bottom-Up Dependent Gating of Frontal Signals in Early Visual Cortex , 2008, Science.

[30]  Ethan Meyers,et al.  The neural decoding toolbox , 2013, Front. Neuroinform..

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

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

[33]  Jeffrey N. Rouder,et al.  Bayesian t tests for accepting and rejecting the null hypothesis , 2009, Psychonomic bulletin & review.

[34]  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.

[35]  Fionn Murtagh,et al.  Ward’s Hierarchical Agglomerative Clustering Method: Which Algorithms Implement Ward’s Criterion? , 2011, Journal of Classification.

[36]  Bevil R. Conway,et al.  Parallel, multi-stage processing of colors, faces and shapes in macaque inferior temporal cortex , 2013, Nature Neuroscience.

[37]  F. Baker.  Stability of Two Hierarchical Grouping Techniques Case I: Sensitivity to Data Errors , 1974 .

[38]  L. M. M.-T..  Theory of Probability , 1929, Nature.

[39]  D I Perrett,et al.  Organization and functions of cells responsive to faces in the temporal cortex. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[40]  Rufin Vogels,et al.  Stimulus features coded by single neurons of a macaque body category selective patch , 2016, Proceedings of the National Academy of Sciences.

[41]  Wilbert Zarco,et al.  A causal relationship between face-patch activity and face-detection behavior , 2017, eLife.

[42]  Doris Y. Tsao,et al.  Intelligent Information Loss: The Coding of Facial Identity, Head Pose, and Non-Face Information in the Macaque Face Patch System , 2015, The Journal of Neuroscience.

[43]  D. Maestripieri.  Gestural Communication in Macaques: Usage and Meaning of Nonvocal Signals , 1997 .

[44]  R. Kirk.  Experimental Design: Procedures for the Behavioral Sciences , 1970 .