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A Brain‐To‐Brain Mechanism for Social Transmission of Threat Learning

Survival and adaptation in environments require swift and efficacious learning about what is dangerous. Across species, much of such threat learning is acquired socially, e.g., through the observation of others’ (“demonstrators’”) defensive behaviors. However, the specific neural mechanisms responsi...

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Autores principales: Pan, Yafeng, Vinding, Mikkel C., Zhang, Lei, Lundqvist, Daniel, Olsson, Andreas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10558655/
https://www.ncbi.nlm.nih.gov/pubmed/37544901
http://dx.doi.org/10.1002/advs.202304037
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author Pan, Yafeng
Vinding, Mikkel C.
Zhang, Lei
Lundqvist, Daniel
Olsson, Andreas
author_facet Pan, Yafeng
Vinding, Mikkel C.
Zhang, Lei
Lundqvist, Daniel
Olsson, Andreas
author_sort Pan, Yafeng
collection PubMed
description Survival and adaptation in environments require swift and efficacious learning about what is dangerous. Across species, much of such threat learning is acquired socially, e.g., through the observation of others’ (“demonstrators’”) defensive behaviors. However, the specific neural mechanisms responsible for the integration of information shared between demonstrators and observers remain largely unknown. This dearth of knowledge is addressed by performing magnetoencephalography (MEG) neuroimaging in demonstrator‐observer dyads. A set of stimuli are first shown to a demonstrator whose defensive responses are filmed and later presented to an observer, while neuronal activity is recorded sequentially from both individuals who never interacted directly. These results show that brain‐to‐brain coupling (BtBC) in the fronto‐limbic circuit (including insula, ventromedial, and dorsolateral prefrontal cortex) within demonstrator‐observer dyads predict subsequent expressions of learning in the observer. Importantly, the predictive power of BtBC magnifies when a threat is imminent to the demonstrator. Furthermore, BtBC depends on how observers perceive their social status relative to the demonstrator, likely driven by shared attention and emotion, as bolstered by dyadic pupillary coupling. Taken together, this study describes a brain‐to‐brain mechanism for social threat learning, involving BtBC, which reflects social relationships and predicts adaptive, learned behaviors.
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spelling pubmed-105586552023-10-08 A Brain‐To‐Brain Mechanism for Social Transmission of Threat Learning Pan, Yafeng Vinding, Mikkel C. Zhang, Lei Lundqvist, Daniel Olsson, Andreas Adv Sci (Weinh) Research Articles Survival and adaptation in environments require swift and efficacious learning about what is dangerous. Across species, much of such threat learning is acquired socially, e.g., through the observation of others’ (“demonstrators’”) defensive behaviors. However, the specific neural mechanisms responsible for the integration of information shared between demonstrators and observers remain largely unknown. This dearth of knowledge is addressed by performing magnetoencephalography (MEG) neuroimaging in demonstrator‐observer dyads. A set of stimuli are first shown to a demonstrator whose defensive responses are filmed and later presented to an observer, while neuronal activity is recorded sequentially from both individuals who never interacted directly. These results show that brain‐to‐brain coupling (BtBC) in the fronto‐limbic circuit (including insula, ventromedial, and dorsolateral prefrontal cortex) within demonstrator‐observer dyads predict subsequent expressions of learning in the observer. Importantly, the predictive power of BtBC magnifies when a threat is imminent to the demonstrator. Furthermore, BtBC depends on how observers perceive their social status relative to the demonstrator, likely driven by shared attention and emotion, as bolstered by dyadic pupillary coupling. Taken together, this study describes a brain‐to‐brain mechanism for social threat learning, involving BtBC, which reflects social relationships and predicts adaptive, learned behaviors. John Wiley and Sons Inc. 2023-08-06 /pmc/articles/PMC10558655/ /pubmed/37544901 http://dx.doi.org/10.1002/advs.202304037 Text en © 2023 The Authors. Advanced Science published by Wiley‐VCH GmbH https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://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
Pan, Yafeng
Vinding, Mikkel C.
Zhang, Lei
Lundqvist, Daniel
Olsson, Andreas
A Brain‐To‐Brain Mechanism for Social Transmission of Threat Learning
title A Brain‐To‐Brain Mechanism for Social Transmission of Threat Learning
title_full A Brain‐To‐Brain Mechanism for Social Transmission of Threat Learning
title_fullStr A Brain‐To‐Brain Mechanism for Social Transmission of Threat Learning
title_full_unstemmed A Brain‐To‐Brain Mechanism for Social Transmission of Threat Learning
title_short A Brain‐To‐Brain Mechanism for Social Transmission of Threat Learning
title_sort brain‐to‐brain mechanism for social transmission of threat learning
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10558655/
https://www.ncbi.nlm.nih.gov/pubmed/37544901
http://dx.doi.org/10.1002/advs.202304037
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