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Cognitive processing of a common stimulus synchronizes brains, hearts, and eyes

Neural, physiological, and behavioral signals synchronize between human subjects in a variety of settings. Multiple hypotheses have been proposed to explain this interpersonal synchrony, but there is no clarity under which conditions it arises, for which signals, or whether there is a common underly...

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Autores principales: Madsen, Jens, Parra, Lucas C
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9802497/
https://www.ncbi.nlm.nih.gov/pubmed/36712806
http://dx.doi.org/10.1093/pnasnexus/pgac020
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author Madsen, Jens
Parra, Lucas C
author_facet Madsen, Jens
Parra, Lucas C
author_sort Madsen, Jens
collection PubMed
description Neural, physiological, and behavioral signals synchronize between human subjects in a variety of settings. Multiple hypotheses have been proposed to explain this interpersonal synchrony, but there is no clarity under which conditions it arises, for which signals, or whether there is a common underlying mechanism. We hypothesized that cognitive processing of a shared stimulus is the source of synchrony between subjects, measured here as intersubject correlation (ISC). To test this, we presented informative videos to participants in an attentive and distracted condition and subsequently measured information recall. ISC was observed for electro-encephalography, gaze position, pupil size, and heart rate, but not respiration and head movements. The strength of correlation was co-modulated in the different signals, changed with attentional state, and predicted subsequent recall of information presented in the videos. There was robust within-subject coupling between brain, heart, and eyes, but not respiration or head movements. The results suggest that ISC is the result of effective cognitive processing, and thus emerges only for those signals that exhibit a robust brain–body connection. While physiological and behavioral fluctuations may be driven by multiple features of the stimulus, correlation with other individuals is co-modulated by the level of attentional engagement with the stimulus.
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spelling pubmed-98024972023-01-26 Cognitive processing of a common stimulus synchronizes brains, hearts, and eyes Madsen, Jens Parra, Lucas C PNAS Nexus Biological, Health, and Medical Sciences Neural, physiological, and behavioral signals synchronize between human subjects in a variety of settings. Multiple hypotheses have been proposed to explain this interpersonal synchrony, but there is no clarity under which conditions it arises, for which signals, or whether there is a common underlying mechanism. We hypothesized that cognitive processing of a shared stimulus is the source of synchrony between subjects, measured here as intersubject correlation (ISC). To test this, we presented informative videos to participants in an attentive and distracted condition and subsequently measured information recall. ISC was observed for electro-encephalography, gaze position, pupil size, and heart rate, but not respiration and head movements. The strength of correlation was co-modulated in the different signals, changed with attentional state, and predicted subsequent recall of information presented in the videos. There was robust within-subject coupling between brain, heart, and eyes, but not respiration or head movements. The results suggest that ISC is the result of effective cognitive processing, and thus emerges only for those signals that exhibit a robust brain–body connection. While physiological and behavioral fluctuations may be driven by multiple features of the stimulus, correlation with other individuals is co-modulated by the level of attentional engagement with the stimulus. Oxford University Press 2022-03-10 /pmc/articles/PMC9802497/ /pubmed/36712806 http://dx.doi.org/10.1093/pnasnexus/pgac020 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of the National Academy of Sciences. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Biological, Health, and Medical Sciences
Madsen, Jens
Parra, Lucas C
Cognitive processing of a common stimulus synchronizes brains, hearts, and eyes
title Cognitive processing of a common stimulus synchronizes brains, hearts, and eyes
title_full Cognitive processing of a common stimulus synchronizes brains, hearts, and eyes
title_fullStr Cognitive processing of a common stimulus synchronizes brains, hearts, and eyes
title_full_unstemmed Cognitive processing of a common stimulus synchronizes brains, hearts, and eyes
title_short Cognitive processing of a common stimulus synchronizes brains, hearts, and eyes
title_sort cognitive processing of a common stimulus synchronizes brains, hearts, and eyes
topic Biological, Health, and Medical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9802497/
https://www.ncbi.nlm.nih.gov/pubmed/36712806
http://dx.doi.org/10.1093/pnasnexus/pgac020
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