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Aberrant dynamics of cognitive control and motor circuits predict distinct restricted and repetitive behaviors in children with autism

Restricted and repetitive behaviors (RRBs) are a defining clinical feature of autism spectrum disorders (ASD). RRBs are highly heterogeneous with variable expression of circumscribed interests (CI), insistence of sameness (IS) and repetitive motor actions (RM), which are major impediments to effecti...

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Autores principales: Supekar, Kaustubh, Ryali, Srikanth, Mistry, Percy, Menon, Vinod
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8192778/
https://www.ncbi.nlm.nih.gov/pubmed/34112791
http://dx.doi.org/10.1038/s41467-021-23822-5
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author Supekar, Kaustubh
Ryali, Srikanth
Mistry, Percy
Menon, Vinod
author_facet Supekar, Kaustubh
Ryali, Srikanth
Mistry, Percy
Menon, Vinod
author_sort Supekar, Kaustubh
collection PubMed
description Restricted and repetitive behaviors (RRBs) are a defining clinical feature of autism spectrum disorders (ASD). RRBs are highly heterogeneous with variable expression of circumscribed interests (CI), insistence of sameness (IS) and repetitive motor actions (RM), which are major impediments to effective functioning in individuals with ASD; yet, the neurobiological basis of CI, IS and RM is unknown. Here we evaluate a unified functional brain circuit model of RRBs and test the hypothesis that CI and IS are associated with aberrant cognitive control circuit dynamics, whereas RM is associated with aberrant motor circuit dynamics. Using task-free fMRI data from 96 children, we first demonstrate that time-varying cross-network interactions in cognitive control circuit are significantly reduced and inflexible in children with ASD, and predict CI and IS symptoms, but not RM symptoms. Furthermore, we show that time-varying cross-network interactions in motor circuit are significantly greater in children with ASD, and predict RM symptoms, but not CI or IS symptoms. We confirmed these results using cross-validation analyses. Moreover, we show that brain-clinical symptom relations are not detected with time-averaged functional connectivity analysis. Our findings provide neurobiological support for the validity of RRB subtypes and identify dissociable brain circuit dynamics as a candidate biomarker for a key clinical feature of ASD.
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spelling pubmed-81927782021-06-17 Aberrant dynamics of cognitive control and motor circuits predict distinct restricted and repetitive behaviors in children with autism Supekar, Kaustubh Ryali, Srikanth Mistry, Percy Menon, Vinod Nat Commun Article Restricted and repetitive behaviors (RRBs) are a defining clinical feature of autism spectrum disorders (ASD). RRBs are highly heterogeneous with variable expression of circumscribed interests (CI), insistence of sameness (IS) and repetitive motor actions (RM), which are major impediments to effective functioning in individuals with ASD; yet, the neurobiological basis of CI, IS and RM is unknown. Here we evaluate a unified functional brain circuit model of RRBs and test the hypothesis that CI and IS are associated with aberrant cognitive control circuit dynamics, whereas RM is associated with aberrant motor circuit dynamics. Using task-free fMRI data from 96 children, we first demonstrate that time-varying cross-network interactions in cognitive control circuit are significantly reduced and inflexible in children with ASD, and predict CI and IS symptoms, but not RM symptoms. Furthermore, we show that time-varying cross-network interactions in motor circuit are significantly greater in children with ASD, and predict RM symptoms, but not CI or IS symptoms. We confirmed these results using cross-validation analyses. Moreover, we show that brain-clinical symptom relations are not detected with time-averaged functional connectivity analysis. Our findings provide neurobiological support for the validity of RRB subtypes and identify dissociable brain circuit dynamics as a candidate biomarker for a key clinical feature of ASD. Nature Publishing Group UK 2021-06-10 /pmc/articles/PMC8192778/ /pubmed/34112791 http://dx.doi.org/10.1038/s41467-021-23822-5 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This 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 license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license 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 license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Supekar, Kaustubh
Ryali, Srikanth
Mistry, Percy
Menon, Vinod
Aberrant dynamics of cognitive control and motor circuits predict distinct restricted and repetitive behaviors in children with autism
title Aberrant dynamics of cognitive control and motor circuits predict distinct restricted and repetitive behaviors in children with autism
title_full Aberrant dynamics of cognitive control and motor circuits predict distinct restricted and repetitive behaviors in children with autism
title_fullStr Aberrant dynamics of cognitive control and motor circuits predict distinct restricted and repetitive behaviors in children with autism
title_full_unstemmed Aberrant dynamics of cognitive control and motor circuits predict distinct restricted and repetitive behaviors in children with autism
title_short Aberrant dynamics of cognitive control and motor circuits predict distinct restricted and repetitive behaviors in children with autism
title_sort aberrant dynamics of cognitive control and motor circuits predict distinct restricted and repetitive behaviors in children with autism
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8192778/
https://www.ncbi.nlm.nih.gov/pubmed/34112791
http://dx.doi.org/10.1038/s41467-021-23822-5
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