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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Published inProceedings of the National Academy of Sciences - PNAS Vol. 119; no. 21; pp. 1 - 12
Main Authors Candia-Rivera, Diego, Catrambone, Vincenzo, Thayer, Julian F., Gentili, Claudio, Valenza, Gaetano
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 24.05.2022
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Summary: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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Author contributions: G.V. designed research; D.C.-R., V.C., J.F.T., C.G., and G.V. performed research; D.C.-R. and V.C. analyzed data; and D.C., V.C., J.F.T., C.G., and G.V. wrote the paper.
Edited by Joseph LeDoux, New York University, New York, NY; received November 3, 2021; accepted March 28, 2022
ISSN:0027-8424
1091-6490
1091-6490
DOI:10.1073/pnas.2119599119