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Social reward network connectivity differs between autistic and neurotypical youth during social interaction

A core feature of autism is difficulties with social interaction. Atypical social motivation is proposed to underlie these difficulties. However, prior work testing this hypothesis has shown mixed support and has been limited in its ability to understand real-world social-interactive processes in au...

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Autores principales: Xie, Hua, Moraczewski, Dustin, McNaughton, Kathryn A., Warnell, Katherine R., Alkire, Diana, Merchant, Junaid S., Kirby, Laura A., Yarger, Heather A., Redcay, Elizabeth
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10274709/
https://www.ncbi.nlm.nih.gov/pubmed/37333161
http://dx.doi.org/10.1101/2023.06.05.543807
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author Xie, Hua
Moraczewski, Dustin
McNaughton, Kathryn A.
Warnell, Katherine R.
Alkire, Diana
Merchant, Junaid S.
Kirby, Laura A.
Yarger, Heather A.
Redcay, Elizabeth
author_facet Xie, Hua
Moraczewski, Dustin
McNaughton, Kathryn A.
Warnell, Katherine R.
Alkire, Diana
Merchant, Junaid S.
Kirby, Laura A.
Yarger, Heather A.
Redcay, Elizabeth
author_sort Xie, Hua
collection PubMed
description A core feature of autism is difficulties with social interaction. Atypical social motivation is proposed to underlie these difficulties. However, prior work testing this hypothesis has shown mixed support and has been limited in its ability to understand real-world social-interactive processes in autism. We attempted to address these limitations by scanning neurotypical and autistic youth (n = 86) during a text-based reciprocal social interaction that mimics a “live” chat and elicits social reward processes. We focused on task-evoked functional connectivity (FC) of regions responsible for motivational-reward and mentalizing processes within the broader social reward circuitry. We found that task-evoked FC between these regions was significantly modulated by social interaction and receipt of social-interactive reward. Compared to neurotypical peers, autistic youth showed significantly greater task-evoked connectivity of core regions in the mentalizing network (e.g., posterior superior temporal sulcus) and the amygdala, a key node in the reward network. Furthermore, across groups, the connectivity strength between these mentalizing and reward regions was negatively correlated with self-reported social motivation and social reward during the scanner task. Our results highlight an important role of FC within the broader social reward circuitry for social-interactive reward. Specifically, greater context-dependent FC (i.e., differences between social engagement and non-social engagement) may indicate an increased “neural effort” during social reward and relate to differences in social motivation within autistic and neurotypical populations.
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spelling pubmed-102747092023-06-17 Social reward network connectivity differs between autistic and neurotypical youth during social interaction Xie, Hua Moraczewski, Dustin McNaughton, Kathryn A. Warnell, Katherine R. Alkire, Diana Merchant, Junaid S. Kirby, Laura A. Yarger, Heather A. Redcay, Elizabeth bioRxiv Article A core feature of autism is difficulties with social interaction. Atypical social motivation is proposed to underlie these difficulties. However, prior work testing this hypothesis has shown mixed support and has been limited in its ability to understand real-world social-interactive processes in autism. We attempted to address these limitations by scanning neurotypical and autistic youth (n = 86) during a text-based reciprocal social interaction that mimics a “live” chat and elicits social reward processes. We focused on task-evoked functional connectivity (FC) of regions responsible for motivational-reward and mentalizing processes within the broader social reward circuitry. We found that task-evoked FC between these regions was significantly modulated by social interaction and receipt of social-interactive reward. Compared to neurotypical peers, autistic youth showed significantly greater task-evoked connectivity of core regions in the mentalizing network (e.g., posterior superior temporal sulcus) and the amygdala, a key node in the reward network. Furthermore, across groups, the connectivity strength between these mentalizing and reward regions was negatively correlated with self-reported social motivation and social reward during the scanner task. Our results highlight an important role of FC within the broader social reward circuitry for social-interactive reward. Specifically, greater context-dependent FC (i.e., differences between social engagement and non-social engagement) may indicate an increased “neural effort” during social reward and relate to differences in social motivation within autistic and neurotypical populations. Cold Spring Harbor Laboratory 2023-06-07 /pmc/articles/PMC10274709/ /pubmed/37333161 http://dx.doi.org/10.1101/2023.06.05.543807 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Xie, Hua
Moraczewski, Dustin
McNaughton, Kathryn A.
Warnell, Katherine R.
Alkire, Diana
Merchant, Junaid S.
Kirby, Laura A.
Yarger, Heather A.
Redcay, Elizabeth
Social reward network connectivity differs between autistic and neurotypical youth during social interaction
title Social reward network connectivity differs between autistic and neurotypical youth during social interaction
title_full Social reward network connectivity differs between autistic and neurotypical youth during social interaction
title_fullStr Social reward network connectivity differs between autistic and neurotypical youth during social interaction
title_full_unstemmed Social reward network connectivity differs between autistic and neurotypical youth during social interaction
title_short Social reward network connectivity differs between autistic and neurotypical youth during social interaction
title_sort social reward network connectivity differs between autistic and neurotypical youth during social interaction
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10274709/
https://www.ncbi.nlm.nih.gov/pubmed/37333161
http://dx.doi.org/10.1101/2023.06.05.543807
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