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

Bodily self-consciousness Computational psychiatry Neural networks Sensory processing Social cognition Statistical inference

Journal

Biological psychiatry. Cognitive neuroscience and neuroimaging
ISSN: 2451-9030
Titre abrégé: Biol Psychiatry Cogn Neurosci Neuroimaging
Pays: United States
ID NLM: 101671285

Informations de publication

Date de publication:
08 2022
Historique:
received: 19 12 2020
revised: 08 03 2021
accepted: 29 03 2021
pubmed: 13 4 2021
medline: 11 8 2022
entrez: 12 4 2021
Statut: ppublish

Résumé

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. 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. 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. 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.

Sections du résumé

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.

Identifiants

pubmed: 33845169
pii: S2451-9022(21)00090-2
doi: 10.1016/j.bpsc.2021.03.013
pmc: PMC8521572
mid: NIHMS1692778
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

756-764

Subventions

Organisme : NIMH NIH HHS
ID : F31 MH112336
Pays : United States
Organisme : NICHD NIH HHS
ID : P50 HD103537
Pays : United States
Organisme : NIMH NIH HHS
ID : R21 MH109225
Pays : United States

Informations de copyright

Copyright © 2021 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.

Auteurs

Jean-Paul Noel (JP)

Vanderbilt Brain Institute, Vanderbilt University, Nashville, Tennessee; Center for Neural Science, New York University, New York, New York. Electronic address: Jpn5@nyu.edu.

Renato Paredes (R)

Institute for Adaptive and Neural Computation, University of Edinburgh, Edinburgh, United Kingdom.

Emily Terrebonne (E)

Undergraduate Neuroscience Program, Vanderbilt University, Nashville, Tennessee; School of Medicine and Health Sciences, George Washington University, Washington, District of Columbia.

Jacob I Feldman (JI)

Vanderbilt Brain Institute, Vanderbilt University, Nashville, Tennessee; Hearing and Speech Sciences, Vanderbilt University Medical Center, Nashville, Tennessee.

Tiffany Woynaroski (T)

Vanderbilt Brain Institute, Vanderbilt University, Nashville, Tennessee; Hearing and Speech Sciences, Vanderbilt University Medical Center, Nashville, Tennessee.

Carissa J Cascio (CJ)

Vanderbilt Brain Institute, Vanderbilt University, Nashville, Tennessee; Psychiatry and Behavioral Sciences, Vanderbilt University Medical Center, Nashville, Tennessee.

Peggy Seriès (P)

Institute for Adaptive and Neural Computation, University of Edinburgh, Edinburgh, United Kingdom.

Mark T Wallace (MT)

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.

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