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Attentional influences on neural processing of biological motion in typically developing children and those on the autism spectrum

BACKGROUND: Biological motion imparts rich information related to the movement, actions, intentions and affective state of others, which can provide foundational support for various aspects of social cognition and behavior. Given that atypical social communication and cognition are hallmark symptoms...

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Autores principales: Knight, Emily J., Krakowski, Aaron I., Freedman, Edward G., Butler, John S., Molholm, Sophie, Foxe, John J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9290301/
https://www.ncbi.nlm.nih.gov/pubmed/35850696
http://dx.doi.org/10.1186/s13229-022-00512-7
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author Knight, Emily J.
Krakowski, Aaron I.
Freedman, Edward G.
Butler, John S.
Molholm, Sophie
Foxe, John J.
author_facet Knight, Emily J.
Krakowski, Aaron I.
Freedman, Edward G.
Butler, John S.
Molholm, Sophie
Foxe, John J.
author_sort Knight, Emily J.
collection PubMed
description BACKGROUND: Biological motion imparts rich information related to the movement, actions, intentions and affective state of others, which can provide foundational support for various aspects of social cognition and behavior. Given that atypical social communication and cognition are hallmark symptoms of autism spectrum disorder (ASD), many have theorized that a potential source of this deficit may lie in dysfunctional neural mechanisms of biological motion processing. Synthesis of existing literature provides some support for biological motion processing deficits in autism spectrum disorder, although high study heterogeneity and inconsistent findings complicate interpretation. Here, we attempted to reconcile some of this residual controversy by investigating a possible modulating role for attention in biological motion processing in ASD. METHODS: We employed high-density electroencephalographic recordings while participants observed point-light displays of upright, inverted and scrambled biological motion under two task conditions to explore spatiotemporal dynamics of intentional and unintentional biological motion processing in children and adolescents with ASD (n = 27), comparing them to a control cohort of neurotypical (NT) participants (n = 35). RESULTS: Behaviorally, ASD participants were able to discriminate biological motion with similar accuracy to NT controls. However, electrophysiologic investigation revealed reduced automatic selective processing of upright biologic versus scrambled motion stimuli in ASD relative to NT individuals, which was ameliorated when task demands required explicit attention to biological motion. Additionally, we observed distinctive patterns of covariance between visual potentials evoked by biological motion and functional social ability, such that Vineland Adaptive Behavior Scale-Socialization domain scores were differentially associated with biological motion processing in the N1 period in the ASD but not the NT group. LIMITATIONS: The cross-sectional design of this study does not allow us to definitively answer the question of whether developmental differences in attention to biological motion cause disruption in social communication, and the sample was limited to children with average or above cognitive ability. CONCLUSIONS: Together, these data suggest that individuals with ASD are able to discriminate, with explicit attention, biological from non-biological motion but demonstrate diminished automatic neural specificity for biological motion processing, which may have cascading implications for the development of higher-order social cognition. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13229-022-00512-7.
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spelling pubmed-92903012022-07-19 Attentional influences on neural processing of biological motion in typically developing children and those on the autism spectrum Knight, Emily J. Krakowski, Aaron I. Freedman, Edward G. Butler, John S. Molholm, Sophie Foxe, John J. Mol Autism Research BACKGROUND: Biological motion imparts rich information related to the movement, actions, intentions and affective state of others, which can provide foundational support for various aspects of social cognition and behavior. Given that atypical social communication and cognition are hallmark symptoms of autism spectrum disorder (ASD), many have theorized that a potential source of this deficit may lie in dysfunctional neural mechanisms of biological motion processing. Synthesis of existing literature provides some support for biological motion processing deficits in autism spectrum disorder, although high study heterogeneity and inconsistent findings complicate interpretation. Here, we attempted to reconcile some of this residual controversy by investigating a possible modulating role for attention in biological motion processing in ASD. METHODS: We employed high-density electroencephalographic recordings while participants observed point-light displays of upright, inverted and scrambled biological motion under two task conditions to explore spatiotemporal dynamics of intentional and unintentional biological motion processing in children and adolescents with ASD (n = 27), comparing them to a control cohort of neurotypical (NT) participants (n = 35). RESULTS: Behaviorally, ASD participants were able to discriminate biological motion with similar accuracy to NT controls. However, electrophysiologic investigation revealed reduced automatic selective processing of upright biologic versus scrambled motion stimuli in ASD relative to NT individuals, which was ameliorated when task demands required explicit attention to biological motion. Additionally, we observed distinctive patterns of covariance between visual potentials evoked by biological motion and functional social ability, such that Vineland Adaptive Behavior Scale-Socialization domain scores were differentially associated with biological motion processing in the N1 period in the ASD but not the NT group. LIMITATIONS: The cross-sectional design of this study does not allow us to definitively answer the question of whether developmental differences in attention to biological motion cause disruption in social communication, and the sample was limited to children with average or above cognitive ability. CONCLUSIONS: Together, these data suggest that individuals with ASD are able to discriminate, with explicit attention, biological from non-biological motion but demonstrate diminished automatic neural specificity for biological motion processing, which may have cascading implications for the development of higher-order social cognition. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13229-022-00512-7. BioMed Central 2022-07-18 /pmc/articles/PMC9290301/ /pubmed/35850696 http://dx.doi.org/10.1186/s13229-022-00512-7 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Knight, Emily J.
Krakowski, Aaron I.
Freedman, Edward G.
Butler, John S.
Molholm, Sophie
Foxe, John J.
Attentional influences on neural processing of biological motion in typically developing children and those on the autism spectrum
title Attentional influences on neural processing of biological motion in typically developing children and those on the autism spectrum
title_full Attentional influences on neural processing of biological motion in typically developing children and those on the autism spectrum
title_fullStr Attentional influences on neural processing of biological motion in typically developing children and those on the autism spectrum
title_full_unstemmed Attentional influences on neural processing of biological motion in typically developing children and those on the autism spectrum
title_short Attentional influences on neural processing of biological motion in typically developing children and those on the autism spectrum
title_sort attentional influences on neural processing of biological motion in typically developing children and those on the autism spectrum
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9290301/
https://www.ncbi.nlm.nih.gov/pubmed/35850696
http://dx.doi.org/10.1186/s13229-022-00512-7
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