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Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain

Empathy for pain engages both shared affective responses and self-other distinction. In this study, we addressed the highly debated question of whether neural responses previously linked to affect sharing could result from the perception of salient affective displays. Moreover, we investigated how t...

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Autores principales: Zhao, Yili, Zhang, Lei, Rütgen, Markus, Sladky, Ronald, Lamm, Claus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8443248/
https://www.ncbi.nlm.nih.gov/pubmed/34409940
http://dx.doi.org/10.7554/eLife.69994
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author Zhao, Yili
Zhang, Lei
Rütgen, Markus
Sladky, Ronald
Lamm, Claus
author_facet Zhao, Yili
Zhang, Lei
Rütgen, Markus
Sladky, Ronald
Lamm, Claus
author_sort Zhao, Yili
collection PubMed
description Empathy for pain engages both shared affective responses and self-other distinction. In this study, we addressed the highly debated question of whether neural responses previously linked to affect sharing could result from the perception of salient affective displays. Moreover, we investigated how the brain network involved in affect sharing and self-other distinction underpinned our response to a pain that is either perceived as genuine or pretended (while in fact both were acted for reasons of experimental control). We found stronger activations in regions associated with affect sharing (anterior insula [aIns] and anterior mid-cingulate cortex) as well as with affective self-other distinction (right supramarginal gyrus [rSMG]), in participants watching video clips of genuine vs. pretended facial expressions of pain. Using dynamic causal modeling, we then assessed the neural dynamics between the right aIns and rSMG in these two conditions. This revealed a reduced inhibitory effect on the aIns to rSMG connection for genuine pain compared to pretended pain. For genuine pain only, brain-to-behavior regression analyses highlighted a linkage between this inhibitory effect on the one hand, and pain ratings as well as empathic traits on the other. These findings imply that if the pain of others is genuine and thus calls for an appropriate empathic response, neural responses in the aIns indeed seem related to affect sharing and self-other distinction is engaged to avoid empathic over-arousal. In contrast, if others merely pretend to be in pain, the perceptual salience of their painful expression results in neural responses that are down-regulated to avoid inappropriate affect sharing and social support.
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spelling pubmed-84432482021-09-17 Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain Zhao, Yili Zhang, Lei Rütgen, Markus Sladky, Ronald Lamm, Claus eLife Neuroscience Empathy for pain engages both shared affective responses and self-other distinction. In this study, we addressed the highly debated question of whether neural responses previously linked to affect sharing could result from the perception of salient affective displays. Moreover, we investigated how the brain network involved in affect sharing and self-other distinction underpinned our response to a pain that is either perceived as genuine or pretended (while in fact both were acted for reasons of experimental control). We found stronger activations in regions associated with affect sharing (anterior insula [aIns] and anterior mid-cingulate cortex) as well as with affective self-other distinction (right supramarginal gyrus [rSMG]), in participants watching video clips of genuine vs. pretended facial expressions of pain. Using dynamic causal modeling, we then assessed the neural dynamics between the right aIns and rSMG in these two conditions. This revealed a reduced inhibitory effect on the aIns to rSMG connection for genuine pain compared to pretended pain. For genuine pain only, brain-to-behavior regression analyses highlighted a linkage between this inhibitory effect on the one hand, and pain ratings as well as empathic traits on the other. These findings imply that if the pain of others is genuine and thus calls for an appropriate empathic response, neural responses in the aIns indeed seem related to affect sharing and self-other distinction is engaged to avoid empathic over-arousal. In contrast, if others merely pretend to be in pain, the perceptual salience of their painful expression results in neural responses that are down-regulated to avoid inappropriate affect sharing and social support. eLife Sciences Publications, Ltd 2021-08-19 /pmc/articles/PMC8443248/ /pubmed/34409940 http://dx.doi.org/10.7554/eLife.69994 Text en © 2021, Zhao et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Zhao, Yili
Zhang, Lei
Rütgen, Markus
Sladky, Ronald
Lamm, Claus
Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain
title Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain
title_full Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain
title_fullStr Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain
title_full_unstemmed Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain
title_short Neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain
title_sort neural dynamics between anterior insular cortex and right supramarginal gyrus dissociate genuine affect sharing from perceptual saliency of pretended pain
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8443248/
https://www.ncbi.nlm.nih.gov/pubmed/34409940
http://dx.doi.org/10.7554/eLife.69994
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