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Attenuated activation of the anterior rostral medial prefrontal cortex on self-relevant social reward processing in individuals with autism spectrum disorder

The social motivation hypothesis posits that people with autism spectrum disorder (ASD) find social stimuli less rewarding and are therefore less motivated towards social interaction than people with neuro-typical development (TD). However, the less rewarding social stimuli characteristics during so...

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Autores principales: Sumiya, Motofumi, Okamoto, Yuko, Koike, Takahiko, Tanigawa, Tsubasa, Okazawa, Hidehiko, Kosaka, Hirotaka, Sadato, Norihiro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7176988/
https://www.ncbi.nlm.nih.gov/pubmed/32325424
http://dx.doi.org/10.1016/j.nicl.2020.102249
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author Sumiya, Motofumi
Okamoto, Yuko
Koike, Takahiko
Tanigawa, Tsubasa
Okazawa, Hidehiko
Kosaka, Hirotaka
Sadato, Norihiro
author_facet Sumiya, Motofumi
Okamoto, Yuko
Koike, Takahiko
Tanigawa, Tsubasa
Okazawa, Hidehiko
Kosaka, Hirotaka
Sadato, Norihiro
author_sort Sumiya, Motofumi
collection PubMed
description The social motivation hypothesis posits that people with autism spectrum disorder (ASD) find social stimuli less rewarding and are therefore less motivated towards social interaction than people with neuro-typical development (TD). However, the less rewarding social stimuli characteristics during social interaction for people with ASD are largely unknown. The contingent positive responsiveness of others relevant to self-action motivates the early development of social interaction, thus representing a social reward. As individuals with ASD often exhibit atypical responses to self-relevant stimuli in their early life, we hypothesized that the self-relevant responses of others are less rewarding for individuals with ASD. To test this hypothesis, we conducted a functional magnetic resonance imaging study using a social contingency task. During the task, the participants attempted to make the audience laugh by telling funny jokes and thus activating the anterior rostral medial prefrontal cortex (arMPFC) of TD individuals (Sumiya et al., 2017). We explicitly predicted that the atypical activation of the arMPFC is related to the reduced reward value of self-relevant responses to others in individuals with ASD. Thirty-one adults with ASD and 24 age- and intelligence quotient-matched TD adults participated in the study. Participants with ASD reported significantly lower pleasure after the audience's responses to their own actions than those in the TD group. Correspondingly, the self-related activation of the arMPFC, defined by the results of our previous study, was attenuated in the ASD group compared to the TD group. The present findings indicate that weak self-relevant outcome processing mediated by the arMPFC of individuals with ASD dampens the rewarding nature of social interaction.
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spelling pubmed-71769882020-04-24 Attenuated activation of the anterior rostral medial prefrontal cortex on self-relevant social reward processing in individuals with autism spectrum disorder Sumiya, Motofumi Okamoto, Yuko Koike, Takahiko Tanigawa, Tsubasa Okazawa, Hidehiko Kosaka, Hirotaka Sadato, Norihiro Neuroimage Clin Regular Article The social motivation hypothesis posits that people with autism spectrum disorder (ASD) find social stimuli less rewarding and are therefore less motivated towards social interaction than people with neuro-typical development (TD). However, the less rewarding social stimuli characteristics during social interaction for people with ASD are largely unknown. The contingent positive responsiveness of others relevant to self-action motivates the early development of social interaction, thus representing a social reward. As individuals with ASD often exhibit atypical responses to self-relevant stimuli in their early life, we hypothesized that the self-relevant responses of others are less rewarding for individuals with ASD. To test this hypothesis, we conducted a functional magnetic resonance imaging study using a social contingency task. During the task, the participants attempted to make the audience laugh by telling funny jokes and thus activating the anterior rostral medial prefrontal cortex (arMPFC) of TD individuals (Sumiya et al., 2017). We explicitly predicted that the atypical activation of the arMPFC is related to the reduced reward value of self-relevant responses to others in individuals with ASD. Thirty-one adults with ASD and 24 age- and intelligence quotient-matched TD adults participated in the study. Participants with ASD reported significantly lower pleasure after the audience's responses to their own actions than those in the TD group. Correspondingly, the self-related activation of the arMPFC, defined by the results of our previous study, was attenuated in the ASD group compared to the TD group. The present findings indicate that weak self-relevant outcome processing mediated by the arMPFC of individuals with ASD dampens the rewarding nature of social interaction. Elsevier 2020-03-19 /pmc/articles/PMC7176988/ /pubmed/32325424 http://dx.doi.org/10.1016/j.nicl.2020.102249 Text en © 2020 The Authors http://creativecommons.org/licenses/by/4.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Regular Article
Sumiya, Motofumi
Okamoto, Yuko
Koike, Takahiko
Tanigawa, Tsubasa
Okazawa, Hidehiko
Kosaka, Hirotaka
Sadato, Norihiro
Attenuated activation of the anterior rostral medial prefrontal cortex on self-relevant social reward processing in individuals with autism spectrum disorder
title Attenuated activation of the anterior rostral medial prefrontal cortex on self-relevant social reward processing in individuals with autism spectrum disorder
title_full Attenuated activation of the anterior rostral medial prefrontal cortex on self-relevant social reward processing in individuals with autism spectrum disorder
title_fullStr Attenuated activation of the anterior rostral medial prefrontal cortex on self-relevant social reward processing in individuals with autism spectrum disorder
title_full_unstemmed Attenuated activation of the anterior rostral medial prefrontal cortex on self-relevant social reward processing in individuals with autism spectrum disorder
title_short Attenuated activation of the anterior rostral medial prefrontal cortex on self-relevant social reward processing in individuals with autism spectrum disorder
title_sort attenuated activation of the anterior rostral medial prefrontal cortex on self-relevant social reward processing in individuals with autism spectrum disorder
topic Regular Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7176988/
https://www.ncbi.nlm.nih.gov/pubmed/32325424
http://dx.doi.org/10.1016/j.nicl.2020.102249
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