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Autonomic and brain responses associated with empathy deficits in autism spectrum disorder

Accumulating evidence suggests that autonomic signals and their cortical representations are closely linked to emotional processes, and that related abnormalities could lead to social deficits. Although socio‐emotional impairments are a defining feature of autism spectrum disorder (ASD), empirical e...

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Autores principales: Gu, Xiaosi, Eilam‐Stock, Tehila, Zhou, Thomas, Anagnostou, Evdokia, Kolevzon, Alexander, Soorya, Latha, Hof, Patrick R., Friston, Karl J., Fan, Jin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4545680/
https://www.ncbi.nlm.nih.gov/pubmed/25995134
http://dx.doi.org/10.1002/hbm.22840
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author Gu, Xiaosi
Eilam‐Stock, Tehila
Zhou, Thomas
Anagnostou, Evdokia
Kolevzon, Alexander
Soorya, Latha
Hof, Patrick R.
Friston, Karl J.
Fan, Jin
author_facet Gu, Xiaosi
Eilam‐Stock, Tehila
Zhou, Thomas
Anagnostou, Evdokia
Kolevzon, Alexander
Soorya, Latha
Hof, Patrick R.
Friston, Karl J.
Fan, Jin
author_sort Gu, Xiaosi
collection PubMed
description Accumulating evidence suggests that autonomic signals and their cortical representations are closely linked to emotional processes, and that related abnormalities could lead to social deficits. Although socio‐emotional impairments are a defining feature of autism spectrum disorder (ASD), empirical evidence directly supporting the link between autonomic, cortical, and socio‐emotional abnormalities in ASD is still lacking. In this study, we examined autonomic arousal indexed by skin conductance responses (SCR), concurrent cortical responses measured by functional magnetic resonance imaging, and effective brain connectivity estimated by dynamic causal modeling in seventeen unmedicated high‐functioning adults with ASD and seventeen matched controls while they performed an empathy‐for‐pain task. Compared to controls, adults with ASD showed enhanced SCR related to empathetic pain, along with increased neural activity in the anterior insular cortex, although their behavioral empathetic pain discriminability was reduced and overall SCR was decreased. ASD individuals also showed enhanced correlation between SCR and neural activities in the anterior insular cortex. Importantly, significant group differences in effective brain connectivity were limited to greater reduction in the negative intrinsic connectivity of the anterior insular cortex in the ASD group, indicating a failure in attenuating anterior insular responses to empathetic pain. These results suggest that aberrant interoceptive precision, as indexed by abnormalities in autonomic activity and its central representations, may underlie empathy deficits in ASD. Hum Brain Mapp 36:3323–3338, 2015. © 2015 The Authors Human Brain Mapping Published byWiley Periodicals, Inc.
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spelling pubmed-45456802016-02-11 Autonomic and brain responses associated with empathy deficits in autism spectrum disorder Gu, Xiaosi Eilam‐Stock, Tehila Zhou, Thomas Anagnostou, Evdokia Kolevzon, Alexander Soorya, Latha Hof, Patrick R. Friston, Karl J. Fan, Jin Hum Brain Mapp Research Articles Accumulating evidence suggests that autonomic signals and their cortical representations are closely linked to emotional processes, and that related abnormalities could lead to social deficits. Although socio‐emotional impairments are a defining feature of autism spectrum disorder (ASD), empirical evidence directly supporting the link between autonomic, cortical, and socio‐emotional abnormalities in ASD is still lacking. In this study, we examined autonomic arousal indexed by skin conductance responses (SCR), concurrent cortical responses measured by functional magnetic resonance imaging, and effective brain connectivity estimated by dynamic causal modeling in seventeen unmedicated high‐functioning adults with ASD and seventeen matched controls while they performed an empathy‐for‐pain task. Compared to controls, adults with ASD showed enhanced SCR related to empathetic pain, along with increased neural activity in the anterior insular cortex, although their behavioral empathetic pain discriminability was reduced and overall SCR was decreased. ASD individuals also showed enhanced correlation between SCR and neural activities in the anterior insular cortex. Importantly, significant group differences in effective brain connectivity were limited to greater reduction in the negative intrinsic connectivity of the anterior insular cortex in the ASD group, indicating a failure in attenuating anterior insular responses to empathetic pain. These results suggest that aberrant interoceptive precision, as indexed by abnormalities in autonomic activity and its central representations, may underlie empathy deficits in ASD. Hum Brain Mapp 36:3323–3338, 2015. © 2015 The Authors Human Brain Mapping Published byWiley Periodicals, Inc. John Wiley and Sons Inc. 2015-05-21 /pmc/articles/PMC4545680/ /pubmed/25995134 http://dx.doi.org/10.1002/hbm.22840 Text en © 2015 The Authors Human Brain Mapping Published by Wiley Periodicals, Inc. This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Articles
Gu, Xiaosi
Eilam‐Stock, Tehila
Zhou, Thomas
Anagnostou, Evdokia
Kolevzon, Alexander
Soorya, Latha
Hof, Patrick R.
Friston, Karl J.
Fan, Jin
Autonomic and brain responses associated with empathy deficits in autism spectrum disorder
title Autonomic and brain responses associated with empathy deficits in autism spectrum disorder
title_full Autonomic and brain responses associated with empathy deficits in autism spectrum disorder
title_fullStr Autonomic and brain responses associated with empathy deficits in autism spectrum disorder
title_full_unstemmed Autonomic and brain responses associated with empathy deficits in autism spectrum disorder
title_short Autonomic and brain responses associated with empathy deficits in autism spectrum disorder
title_sort autonomic and brain responses associated with empathy deficits in autism spectrum disorder
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4545680/
https://www.ncbi.nlm.nih.gov/pubmed/25995134
http://dx.doi.org/10.1002/hbm.22840
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