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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| Format: | Article |
| Language: | English |
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Elsevier
2020-01-01
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| Series: | NeuroImage: Clinical |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158220300863 |
| _version_ | 1818203134143496192 |
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| author | Motofumi Sumiya Yuko Okamoto Takahiko Koike Tsubasa Tanigawa Hidehiko Okazawa Hirotaka Kosaka Norihiro Sadato |
| author_facet | Motofumi Sumiya Yuko Okamoto Takahiko Koike Tsubasa Tanigawa Hidehiko Okazawa Hirotaka Kosaka Norihiro Sadato |
| author_sort | Motofumi Sumiya |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-12T03:20:31Z |
| format | Article |
| id | doaj.art-759f0cd149cd43859c15452c43dd9146 |
| institution | Directory Open Access Journal |
| issn | 2213-1582 |
| language | English |
| last_indexed | 2024-12-12T03:20:31Z |
| publishDate | 2020-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj.art-759f0cd149cd43859c15452c43dd91462022-12-22T00:40:10ZengElsevierNeuroImage: Clinical2213-15822020-01-0126Attenuated activation of the anterior rostral medial prefrontal cortex on self-relevant social reward processing in individuals with autism spectrum disorderMotofumi Sumiya0Yuko Okamoto1Takahiko Koike2Tsubasa Tanigawa3Hidehiko Okazawa4Hirotaka Kosaka5Norihiro Sadato6Division of Cerebral Integration, National Institute for Physiological Sciences, Aichi, Japan; Research Fellow of the Japan Society for the Promotion of Science, Tokyo, Japan; Graduate School of Informatics, Nagoya University, Aichi, JapanResearch Center for Child Mental Development, University of Fukui, Fukui, Japan; ATR-Promotions, Brain Activity Imaging Center, Kyoto, Japan; Advanced Telecommunications Research Institute International, Kyoto, JapanDivision of Cerebral Integration, National Institute for Physiological Sciences, Aichi, JapanDivision of Cerebral Integration, National Institute for Physiological Sciences, Aichi, JapanBiomedical Imaging Research Center, University of Fukui, Fukui, JapanResearch Center for Child Mental Development, University of Fukui, Fukui, Japan; Department of Neuropsychiatry, University of Fukui, Fukui, JapanDivision of Cerebral Integration, National Institute for Physiological Sciences, Aichi, Japan; Corresponding author: Division of Cerebral Integration, National Institute for Physiological Sciences, 38 Nishigonaka Myodaiji, Okazaki, Aichi, 444-8585, Japan.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.http://www.sciencedirect.com/science/article/pii/S2213158220300863Autism spectrum disorderFunctional magnetic resonance imagingReward processingSelfMedial Prefrontal cortex |
| spellingShingle | Motofumi Sumiya Yuko Okamoto Takahiko Koike Tsubasa Tanigawa Hidehiko Okazawa Hirotaka Kosaka Norihiro Sadato Attenuated activation of the anterior rostral medial prefrontal cortex on self-relevant social reward processing in individuals with autism spectrum disorder NeuroImage: Clinical Autism spectrum disorder Functional magnetic resonance imaging Reward processing Self Medial Prefrontal cortex |
| 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 | Autism spectrum disorder Functional magnetic resonance imaging Reward processing Self Medial Prefrontal cortex |
| url | http://www.sciencedirect.com/science/article/pii/S2213158220300863 |
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