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Cardiac sympathetic-vagal activity initiates a functional brain–body response to emotional arousal

A century-long debate on bodily states and emotions persists. While the involvement of bodily activity in emotion physiology is widely recognized, the specificity and causal role of such activity related to brain dynamics has not yet been demonstrated. We hypothesize that the peripheral neural contr...

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Autores principales: Candia-Rivera, Diego, Catrambone, Vincenzo, Thayer, Julian F., Gentili, Claudio, Valenza, Gaetano
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9173754/
https://www.ncbi.nlm.nih.gov/pubmed/35588453
http://dx.doi.org/10.1073/pnas.2119599119
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author Candia-Rivera, Diego
Catrambone, Vincenzo
Thayer, Julian F.
Gentili, Claudio
Valenza, Gaetano
author_facet Candia-Rivera, Diego
Catrambone, Vincenzo
Thayer, Julian F.
Gentili, Claudio
Valenza, Gaetano
author_sort Candia-Rivera, Diego
collection PubMed
description A century-long debate on bodily states and emotions persists. While the involvement of bodily activity in emotion physiology is widely recognized, the specificity and causal role of such activity related to brain dynamics has not yet been demonstrated. We hypothesize that the peripheral neural control on cardiovascular activity prompts and sustains brain dynamics during an emotional experience, so these afferent inputs are processed by the brain by triggering a concurrent efferent information transfer to the body. To this end, we investigated the functional brain–heart interplay under emotion elicitation in publicly available data from 62 healthy subjects using a computational model based on synthetic data generation of electroencephalography and electrocardiography signals. Our findings show that sympathovagal activity plays a leading and causal role in initiating the emotional response, in which ascending modulations from vagal activity precede neural dynamics and correlate to the reported level of arousal. The subsequent dynamic interplay observed between the central and autonomic nervous systems sustains the processing of emotional arousal. These findings should be particularly revealing for the psychophysiology and neuroscience of emotions.
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spelling pubmed-91737542022-06-08 Cardiac sympathetic-vagal activity initiates a functional brain–body response to emotional arousal Candia-Rivera, Diego Catrambone, Vincenzo Thayer, Julian F. Gentili, Claudio Valenza, Gaetano Proc Natl Acad Sci U S A Biological Sciences A century-long debate on bodily states and emotions persists. While the involvement of bodily activity in emotion physiology is widely recognized, the specificity and causal role of such activity related to brain dynamics has not yet been demonstrated. We hypothesize that the peripheral neural control on cardiovascular activity prompts and sustains brain dynamics during an emotional experience, so these afferent inputs are processed by the brain by triggering a concurrent efferent information transfer to the body. To this end, we investigated the functional brain–heart interplay under emotion elicitation in publicly available data from 62 healthy subjects using a computational model based on synthetic data generation of electroencephalography and electrocardiography signals. Our findings show that sympathovagal activity plays a leading and causal role in initiating the emotional response, in which ascending modulations from vagal activity precede neural dynamics and correlate to the reported level of arousal. The subsequent dynamic interplay observed between the central and autonomic nervous systems sustains the processing of emotional arousal. These findings should be particularly revealing for the psychophysiology and neuroscience of emotions. National Academy of Sciences 2022-05-19 2022-05-24 /pmc/articles/PMC9173754/ /pubmed/35588453 http://dx.doi.org/10.1073/pnas.2119599119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Candia-Rivera, Diego
Catrambone, Vincenzo
Thayer, Julian F.
Gentili, Claudio
Valenza, Gaetano
Cardiac sympathetic-vagal activity initiates a functional brain–body response to emotional arousal
title Cardiac sympathetic-vagal activity initiates a functional brain–body response to emotional arousal
title_full Cardiac sympathetic-vagal activity initiates a functional brain–body response to emotional arousal
title_fullStr Cardiac sympathetic-vagal activity initiates a functional brain–body response to emotional arousal
title_full_unstemmed Cardiac sympathetic-vagal activity initiates a functional brain–body response to emotional arousal
title_short Cardiac sympathetic-vagal activity initiates a functional brain–body response to emotional arousal
title_sort cardiac sympathetic-vagal activity initiates a functional brain–body response to emotional arousal
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9173754/
https://www.ncbi.nlm.nih.gov/pubmed/35588453
http://dx.doi.org/10.1073/pnas.2119599119
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