Body Patches in Inferior Temporal Cortex Encode Categories with Different Temporal Dynamics

An unresolved question in cognitive neuroscience is how representations of object categories at different levels (basic and superordinate) develop during the course of the neural response within an area. To address this, we decoded categories of different levels from the spiking responses of populations of neurons recorded in two fMRI-defined body patches in the macaque STS. Recordings of the two patches were made in the same animals with the same stimuli. Support vector machine classifiers were trained at brief response epochs and tested at the same or different epochs, thus assessing whether category representations change during the course of the response. In agreement with hierarchical processing within the body patch network, the posterior body patch mid STS body (MSB) showed an earlier onset of categorization compared with the anterior body patch anterior STS body (ASB), irrespective of the categorization level. Decoding of the superordinate body versus nonbody categories was less dynamic in MSB than in ASB, with ASB showing a biphasic temporal pattern. Decoding of the ordinate-level category human versus monkey bodies showed similar temporal patterns in both patches. The decoding onset of superordinate categorizations involving bodies was as early as for basic-level categorization, suggesting that previously reported differences between the onset of basic and superordinate categorizations may depend on the area. The qualitative difference between areas in their dynamics of category representation may hinder the interpretation of decoding dynamics based on EEG or MEG, methods that may mix signals of different areas.

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

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

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

[4]  Ha Hong,et al.  Simple Learned Weighted Sums of Inferior Temporal Neuronal Firing Rates Accurately Predict Human Core Object Recognition Performance , 2015, The Journal of Neuroscience.

[5]  S. Thorpe,et al.  Rapid categorization of natural images by rhesus monkeys , 1998, Neuroreport.

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

[7]  Rufin Vogels,et al.  Transformation of Visual Representations Across Ventral Stream Body-selective Patches , 2019, Cerebral cortex.

[8]  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.

[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]  Rufin Vogels,et al.  Encoding of Predictable and Unpredictable Stimuli by Inferior Temporal Cortical Neurons , 2017, Journal of Cognitive Neuroscience.

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

[12]  Joel Z. Leibo,et al.  The dynamics of invariant object recognition in the human visual system. , 2014, Journal of neurophysiology.

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

[14]  Michèle Fabre-Thorpe,et al.  At 120 msec You Can Spot the Animal but You Don't Yet Know It's a Dog , 2015, Journal of Cognitive Neuroscience.

[15]  Ha Hong,et al.  Performance-optimized hierarchical models predict neural responses in higher visual cortex , 2014, Proceedings of the National Academy of Sciences.

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

[17]  Majid Nili Ahmadabadi,et al.  Temporal dynamics of visual category representation in the macaque inferior temporal cortex. , 2016, Journal of neurophysiology.

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

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

[20]  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.

[21]  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.

[22]  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.

[23]  David A. Tovar,et al.  Representational dynamics of object vision: the first 1000 ms. , 2013, Journal of vision.

[24]  Thomas Serre,et al.  Object decoding with attention in inferior temporal cortex , 2011, Proceedings of the National Academy of Sciences.

[25]  Byron M. Yu,et al.  Cortical Areas Interact through a Communication Subspace , 2019, Neuron.

[26]  Radoslaw Martin Cichy,et al.  Resolving human object recognition in space and time , 2014, Nature Neuroscience.

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

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

[29]  David J. Freedman,et al.  Dynamic population coding of category information in inferior temporal and prefrontal cortex. , 2008, Journal of neurophysiology.

[30]  Susan G. Wardle,et al.  Decoding the time-course of object recognition in the human brain: From visual features to categorical decisions , 2017, Neuropsychologia.

[31]  Mehrdad Jazayeri,et al.  Navigating the Neural Space in Search of the Neural Code , 2017, Neuron.

[32]  Carlo Baldassi,et al.  Shape Similarity, Better than Semantic Membership, Accounts for the Structure of Visual Object Representations in a Population of Monkey Inferotemporal Neurons , 2013, PLoS Comput. Biol..

[33]  Scott L. Brincat,et al.  Dynamic Shape Synthesis in Posterior Inferotemporal Cortex , 2006, Neuron.

[34]  Susan G. Wardle,et al.  Decoding Dynamic Brain Patterns from Evoked Responses: A Tutorial on Multivariate Pattern Analysis Applied to Time Series Neuroimaging Data , 2016, Journal of Cognitive Neuroscience.