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Inflexible Updating of the Self-Other Divide During a Social Context in Autism: Psychophysical, Electrophysiological, and Neural Network Modeling Evidence

  • Author Footnotes
    1 J-PN and RP contributed equally to this work as joint first authors.
    Jean-Paul Noel
    Correspondence
    Address correspondence to Jean-Paul Noel, Ph.D.
    Footnotes
    1 J-PN and RP contributed equally to this work as joint first authors.
    Affiliations
    Vanderbilt Brain Institute, Vanderbilt University, Nashville, Tennessee

    Center for Neural Science, New York University, New York, New York
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  • Author Footnotes
    1 J-PN and RP contributed equally to this work as joint first authors.
    Renato Paredes
    Footnotes
    1 J-PN and RP contributed equally to this work as joint first authors.
    Affiliations
    Institute for Adaptive and Neural Computation, University of Edinburgh, Edinburgh, United Kingdom
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  • Emily Terrebonne
    Affiliations
    Undergraduate Neuroscience Program, Vanderbilt University, Nashville, Tennessee

    School of Medicine and Health Sciences, George Washington University, Washington, District of Columbia
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  • Jacob I. Feldman
    Affiliations
    Vanderbilt Brain Institute, Vanderbilt University, Nashville, Tennessee

    Hearing and Speech Sciences, Vanderbilt University Medical Center, Nashville, Tennessee
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  • Tiffany Woynaroski
    Affiliations
    Vanderbilt Brain Institute, Vanderbilt University, Nashville, Tennessee

    Hearing and Speech Sciences, Vanderbilt University Medical Center, Nashville, Tennessee
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  • Carissa J. Cascio
    Affiliations
    Vanderbilt Brain Institute, Vanderbilt University, Nashville, Tennessee

    Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center, Nashville, Tennessee
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  • Author Footnotes
    2 PS and MTW contributed equally to this work as joint senior authors.
    Peggy Seriès
    Footnotes
    2 PS and MTW contributed equally to this work as joint senior authors.
    Affiliations
    Institute for Adaptive and Neural Computation, University of Edinburgh, Edinburgh, United Kingdom
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  • Author Footnotes
    2 PS and MTW contributed equally to this work as joint senior authors.
    Mark T. Wallace
    Footnotes
    2 PS and MTW contributed equally to this work as joint senior authors.
    Affiliations
    Vanderbilt Brain Institute, Vanderbilt University, Nashville, Tennessee

    Hearing and Speech Sciences, Vanderbilt University Medical Center, Nashville, Tennessee

    Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center, Nashville, Tennessee
    Search for articles by this author
  • Author Footnotes
    1 J-PN and RP contributed equally to this work as joint first authors.
    2 PS and MTW contributed equally to this work as joint senior authors.
Published:April 09, 2021DOI:https://doi.org/10.1016/j.bpsc.2021.03.013

      Abstract

      Background

      Autism spectrum disorder (ASD) affects many aspects of life, from social interactions to (multi)sensory processing. Similarly, the condition expresses at a variety of levels of description, from genetics to neural circuits and interpersonal behavior. We attempt to bridge between domains and levels of description by detailing the behavioral, electrophysiological, and putative neural network basis of peripersonal space (PPS) updating in ASD during a social context, given that the encoding of this space relies on appropriate multisensory integration, is malleable by social context, and is thought to delineate the boundary between the self and others.

      Methods

      Fifty (20 male/30 female) young adults, either diagnosed with ASD or age- and sex-matched individuals, took part in a visuotactile reaction time task indexing PPS, while high-density electroencephalography was continuously recorded. Neural network modeling was performed in silico.

      Results

      Multisensory psychophysics demonstrates that while PPS in neurotypical individuals shrinks in the presence of others—as to “give space”—this does not occur in ASD. Likewise, electroencephalography recordings suggest that multisensory integration is altered by social context in neurotypical individuals but not in individuals with ASD. Finally, a biologically plausible neural network model shows, as a proof of principle, that PPS updating may be inflexible in ASD owing to the altered excitatory/inhibitory balance that characterizes neural circuits in animal models of ASD.

      Conclusions

      Findings are conceptually in line with recent statistical inference accounts, suggesting diminished flexibility in ASD, and further these observations by suggesting within an example relevant for social cognition that such inflexibility may be due to excitatory/inhibitory imbalances.

      Keywords

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