Dysfunction in interpersonal neural synchronization as a mechanism for social impairment in autism spectrum disorder
Social deficits in autism spectrum disorder (ASD) have been linked to atypical activation of the mentalizing network. This work, however, has been limited by a focus on the brain activity of a single person during computerized social tasks rather than exploring brain activity during in vivo interact...
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Veröffentlicht in: | Autism research 2021-08, Vol.14 (8), p.1585-1596 |
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description | Social deficits in autism spectrum disorder (ASD) have been linked to atypical activation of the mentalizing network. This work, however, has been limited by a focus on the brain activity of a single person during computerized social tasks rather than exploring brain activity during in vivo interactions. The current study assessed neural synchronization during a conversation as a mechanism for social impairment in adults with ASD (n = 24) and matched controls (n = 26). Functional near‐infrared spectroscopy (fNIRS) data were collected from the prefrontal cortex (PFC) and tempoparietal junction (TPJ). Participants self‐reported on their social communication and videos of the interaction were coded for utterances and conversational turns. As expected, controls showed more neural synchrony than participants with ASD in the TPJ. Also as expected, controls showed less social communication impairment than participants with ASD. However, participants with ASD did not have fewer utterances compared with control subjects. Overall, less neural synchrony in the TPJ was associated with higher social impairment and marginally fewer utterances. Our findings advance our understanding of social difficulties in ASD by linking them to decreased neural synchronization of the TPJ.
Lay Summary
The coordination of brain responses is important for efficient social interactions. The current study explored the coordination of brain responses in neurotypical adults and adults with ASD to investigate if difficulties in social interactions are related to difficulties coordinating brain responses in ASD. We found that participants with ASD had more difficulties coordinating brain responses during a conversation with an interacting partner. Additionally, we found that the level of coordination in brain responses was linked to problems with social communication. |
doi_str_mv | 10.1002/aur.2513 |
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Lay Summary
The coordination of brain responses is important for efficient social interactions. The current study explored the coordination of brain responses in neurotypical adults and adults with ASD to investigate if difficulties in social interactions are related to difficulties coordinating brain responses in ASD. We found that participants with ASD had more difficulties coordinating brain responses during a conversation with an interacting partner. Additionally, we found that the level of coordination in brain responses was linked to problems with social communication.</description><identifier>ISSN: 1939-3792</identifier><identifier>ISSN: 1939-3806</identifier><identifier>EISSN: 1939-3806</identifier><identifier>DOI: 10.1002/aur.2513</identifier><identifier>PMID: 33847461</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Adult ; Adults ; ASD ; Autism ; Autism Spectrum Disorder ; Brain ; Brain Mapping ; Coordination ; Humans ; Impairment ; In vivo methods and tests ; Infrared spectroscopy ; Mentalization ; Near infrared radiation ; neural synchrony ; Prefrontal cortex ; social communication impairment ; social deficits ; Social factors ; Social interactions ; Spectroscopy, Near-Infrared ; Spectrum analysis ; Synchronism ; Synchronization ; TPJ ; Verbal communication</subject><ispartof>Autism research, 2021-08, Vol.14 (8), p.1585-1596</ispartof><rights>2021 International Society for Autism Research and Wiley Periodicals LLC.</rights><rights>2021 International Society for Autism Research, Wiley Periodicals LLC</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3833-5cdc7698723ed1d20ec30ca9b63e9d1b901c3a80b0e54e929112d0e988b1c95a3</citedby><cites>FETCH-LOGICAL-c3833-5cdc7698723ed1d20ec30ca9b63e9d1b901c3a80b0e54e929112d0e988b1c95a3</cites><orcidid>0000-0001-7135-9019 ; 0000-0001-5125-210X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Faur.2513$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Faur.2513$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33847461$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Quiñones‐Camacho, Laura E.</creatorcontrib><creatorcontrib>Fishburn, Frank A.</creatorcontrib><creatorcontrib>Belardi, Katherine</creatorcontrib><creatorcontrib>Williams, Diane L.</creatorcontrib><creatorcontrib>Huppert, Theodore J.</creatorcontrib><creatorcontrib>Perlman, Susan B.</creatorcontrib><title>Dysfunction in interpersonal neural synchronization as a mechanism for social impairment in autism spectrum disorder</title><title>Autism research</title><addtitle>Autism Res</addtitle><description>Social deficits in autism spectrum disorder (ASD) have been linked to atypical activation of the mentalizing network. This work, however, has been limited by a focus on the brain activity of a single person during computerized social tasks rather than exploring brain activity during in vivo interactions. The current study assessed neural synchronization during a conversation as a mechanism for social impairment in adults with ASD (n = 24) and matched controls (n = 26). Functional near‐infrared spectroscopy (fNIRS) data were collected from the prefrontal cortex (PFC) and tempoparietal junction (TPJ). Participants self‐reported on their social communication and videos of the interaction were coded for utterances and conversational turns. As expected, controls showed more neural synchrony than participants with ASD in the TPJ. Also as expected, controls showed less social communication impairment than participants with ASD. However, participants with ASD did not have fewer utterances compared with control subjects. Overall, less neural synchrony in the TPJ was associated with higher social impairment and marginally fewer utterances. Our findings advance our understanding of social difficulties in ASD by linking them to decreased neural synchronization of the TPJ.
Lay Summary
The coordination of brain responses is important for efficient social interactions. The current study explored the coordination of brain responses in neurotypical adults and adults with ASD to investigate if difficulties in social interactions are related to difficulties coordinating brain responses in ASD. We found that participants with ASD had more difficulties coordinating brain responses during a conversation with an interacting partner. Additionally, we found that the level of coordination in brain responses was linked to problems with social communication.</description><subject>Adult</subject><subject>Adults</subject><subject>ASD</subject><subject>Autism</subject><subject>Autism Spectrum Disorder</subject><subject>Brain</subject><subject>Brain Mapping</subject><subject>Coordination</subject><subject>Humans</subject><subject>Impairment</subject><subject>In vivo methods and tests</subject><subject>Infrared spectroscopy</subject><subject>Mentalization</subject><subject>Near infrared radiation</subject><subject>neural synchrony</subject><subject>Prefrontal cortex</subject><subject>social communication impairment</subject><subject>social deficits</subject><subject>Social factors</subject><subject>Social interactions</subject><subject>Spectroscopy, Near-Infrared</subject><subject>Spectrum analysis</subject><subject>Synchronism</subject><subject>Synchronization</subject><subject>TPJ</subject><subject>Verbal communication</subject><issn>1939-3792</issn><issn>1939-3806</issn><issn>1939-3806</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kV1LwzAUhoMoTqfgL5CCN9505mNtk8sxP2EgiLsuaXrGMtqkJg1Sf73tPhQE4cB74Dw8F-9B6IrgCcGY3sngJjQh7AidEcFEzDhOjw97JugInXu_wTjFLKGnaMQYn2bTlJyh9r7zq2BUq62J9DAtuAact0ZWkYHg-vCdUWtnjf6SW076SEY1qLU02tfRyrrIW6V7UteN1K4G0w4yGdrh7htQrQt1VGpvXQnuAp2sZOXhcp9jtHx8eJ8_x4vXp5f5bBErxhmLE1WqLBU8owxKUlIMimElRZEyECUpBCaKSY4LDMkUBBWE0BKD4LwgSiSSjdHtzts4-xHAt3mtvYKqkgZs8HlfGe2r4IL16M0fdGOD6zsYqCSjU0Ix_xUqZ713sMobp2vpupzgfPhE3n9i0A7C670wFDWUP-Ch-h6Id8CnrqD7V5TPlm9b4TccC5PH</recordid><startdate>202108</startdate><enddate>202108</enddate><creator>Quiñones‐Camacho, Laura E.</creator><creator>Fishburn, Frank A.</creator><creator>Belardi, Katherine</creator><creator>Williams, Diane L.</creator><creator>Huppert, Theodore J.</creator><creator>Perlman, Susan B.</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7TK</scope><scope>K9.</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-7135-9019</orcidid><orcidid>https://orcid.org/0000-0001-5125-210X</orcidid></search><sort><creationdate>202108</creationdate><title>Dysfunction in interpersonal neural synchronization as a mechanism for social impairment in autism spectrum disorder</title><author>Quiñones‐Camacho, Laura E. ; Fishburn, Frank A. ; Belardi, Katherine ; Williams, Diane L. ; Huppert, Theodore J. ; Perlman, Susan B.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3833-5cdc7698723ed1d20ec30ca9b63e9d1b901c3a80b0e54e929112d0e988b1c95a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Adult</topic><topic>Adults</topic><topic>ASD</topic><topic>Autism</topic><topic>Autism Spectrum Disorder</topic><topic>Brain</topic><topic>Brain Mapping</topic><topic>Coordination</topic><topic>Humans</topic><topic>Impairment</topic><topic>In vivo methods and tests</topic><topic>Infrared spectroscopy</topic><topic>Mentalization</topic><topic>Near infrared radiation</topic><topic>neural synchrony</topic><topic>Prefrontal cortex</topic><topic>social communication impairment</topic><topic>social deficits</topic><topic>Social factors</topic><topic>Social interactions</topic><topic>Spectroscopy, Near-Infrared</topic><topic>Spectrum analysis</topic><topic>Synchronism</topic><topic>Synchronization</topic><topic>TPJ</topic><topic>Verbal communication</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Quiñones‐Camacho, Laura E.</creatorcontrib><creatorcontrib>Fishburn, Frank A.</creatorcontrib><creatorcontrib>Belardi, Katherine</creatorcontrib><creatorcontrib>Williams, Diane L.</creatorcontrib><creatorcontrib>Huppert, Theodore J.</creatorcontrib><creatorcontrib>Perlman, Susan B.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Autism research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Quiñones‐Camacho, Laura E.</au><au>Fishburn, Frank A.</au><au>Belardi, Katherine</au><au>Williams, Diane L.</au><au>Huppert, Theodore J.</au><au>Perlman, Susan B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dysfunction in interpersonal neural synchronization as a mechanism for social impairment in autism spectrum disorder</atitle><jtitle>Autism research</jtitle><addtitle>Autism Res</addtitle><date>2021-08</date><risdate>2021</risdate><volume>14</volume><issue>8</issue><spage>1585</spage><epage>1596</epage><pages>1585-1596</pages><issn>1939-3792</issn><issn>1939-3806</issn><eissn>1939-3806</eissn><abstract>Social deficits in autism spectrum disorder (ASD) have been linked to atypical activation of the mentalizing network. This work, however, has been limited by a focus on the brain activity of a single person during computerized social tasks rather than exploring brain activity during in vivo interactions. The current study assessed neural synchronization during a conversation as a mechanism for social impairment in adults with ASD (n = 24) and matched controls (n = 26). Functional near‐infrared spectroscopy (fNIRS) data were collected from the prefrontal cortex (PFC) and tempoparietal junction (TPJ). Participants self‐reported on their social communication and videos of the interaction were coded for utterances and conversational turns. As expected, controls showed more neural synchrony than participants with ASD in the TPJ. Also as expected, controls showed less social communication impairment than participants with ASD. However, participants with ASD did not have fewer utterances compared with control subjects. Overall, less neural synchrony in the TPJ was associated with higher social impairment and marginally fewer utterances. Our findings advance our understanding of social difficulties in ASD by linking them to decreased neural synchronization of the TPJ.
Lay Summary
The coordination of brain responses is important for efficient social interactions. The current study explored the coordination of brain responses in neurotypical adults and adults with ASD to investigate if difficulties in social interactions are related to difficulties coordinating brain responses in ASD. We found that participants with ASD had more difficulties coordinating brain responses during a conversation with an interacting partner. Additionally, we found that the level of coordination in brain responses was linked to problems with social communication.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>33847461</pmid><doi>10.1002/aur.2513</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-7135-9019</orcidid><orcidid>https://orcid.org/0000-0001-5125-210X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adult Adults ASD Autism Autism Spectrum Disorder Brain Brain Mapping Coordination Humans Impairment In vivo methods and tests Infrared spectroscopy Mentalization Near infrared radiation neural synchrony Prefrontal cortex social communication impairment social deficits Social factors Social interactions Spectroscopy, Near-Infrared Spectrum analysis Synchronism Synchronization TPJ Verbal communication |
title | Dysfunction in interpersonal neural synchronization as a mechanism for social impairment in autism spectrum disorder |
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