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Characterizing cardiac autonomic dynamics of fear learning in humans

Understanding transient dynamics of the autonomic nervous system during fear learning remains a critical step to translate basic research into treatment of fear‐related disorders. In humans, it has been demonstrated that fear learning typically elicits transient heart rate deceleration. However, cla...

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Autores principales: Battaglia, Simone, Orsolini, Stefano, Borgomaneri, Sara, Barbieri, Riccardo, Diciotti, Stefano, di Pellegrino, Giuseppe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9787647/
https://www.ncbi.nlm.nih.gov/pubmed/35671393
http://dx.doi.org/10.1111/psyp.14122
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author Battaglia, Simone
Orsolini, Stefano
Borgomaneri, Sara
Barbieri, Riccardo
Diciotti, Stefano
di Pellegrino, Giuseppe
author_facet Battaglia, Simone
Orsolini, Stefano
Borgomaneri, Sara
Barbieri, Riccardo
Diciotti, Stefano
di Pellegrino, Giuseppe
author_sort Battaglia, Simone
collection PubMed
description Understanding transient dynamics of the autonomic nervous system during fear learning remains a critical step to translate basic research into treatment of fear‐related disorders. In humans, it has been demonstrated that fear learning typically elicits transient heart rate deceleration. However, classical analyses of heart rate variability (HRV) fail to disentangle the contribution of parasympathetic and sympathetic systems, and crucially, they are not able to capture phasic changes during fear learning. Here, to gain deeper insight into the physiological underpinnings of fear learning, a novel frequency‐domain analysis of heart rate was performed using a short‐time Fourier transform, and instantaneous spectral estimates extracted from a point‐process modeling algorithm. We tested whether spectral transient components of HRV, used as a noninvasive probe of sympathetic and parasympathetic mechanisms, can dissociate between fear conditioned and neutral stimuli. We found that learned fear elicited a transient heart rate deceleration in anticipation of noxious stimuli. Crucially, results revealed a significant increase in spectral power in the high frequency band when facing the conditioned stimulus, indicating increased parasympathetic (vagal) activity, which distinguished conditioned and neutral stimuli during fear learning. Our findings provide a proximal measure of the involvement of cardiac vagal dynamics into the psychophysiology of fear learning and extinction, thus offering new insights for the characterization of fear in mental health and illness.
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spelling pubmed-97876472022-12-28 Characterizing cardiac autonomic dynamics of fear learning in humans Battaglia, Simone Orsolini, Stefano Borgomaneri, Sara Barbieri, Riccardo Diciotti, Stefano di Pellegrino, Giuseppe Psychophysiology Original Articles Understanding transient dynamics of the autonomic nervous system during fear learning remains a critical step to translate basic research into treatment of fear‐related disorders. In humans, it has been demonstrated that fear learning typically elicits transient heart rate deceleration. However, classical analyses of heart rate variability (HRV) fail to disentangle the contribution of parasympathetic and sympathetic systems, and crucially, they are not able to capture phasic changes during fear learning. Here, to gain deeper insight into the physiological underpinnings of fear learning, a novel frequency‐domain analysis of heart rate was performed using a short‐time Fourier transform, and instantaneous spectral estimates extracted from a point‐process modeling algorithm. We tested whether spectral transient components of HRV, used as a noninvasive probe of sympathetic and parasympathetic mechanisms, can dissociate between fear conditioned and neutral stimuli. We found that learned fear elicited a transient heart rate deceleration in anticipation of noxious stimuli. Crucially, results revealed a significant increase in spectral power in the high frequency band when facing the conditioned stimulus, indicating increased parasympathetic (vagal) activity, which distinguished conditioned and neutral stimuli during fear learning. Our findings provide a proximal measure of the involvement of cardiac vagal dynamics into the psychophysiology of fear learning and extinction, thus offering new insights for the characterization of fear in mental health and illness. John Wiley and Sons Inc. 2022-06-07 2022-12 /pmc/articles/PMC9787647/ /pubmed/35671393 http://dx.doi.org/10.1111/psyp.14122 Text en © 2022 The Authors. Psychophysiology published by Wiley Periodicals LLC on behalf of Society for Psychophysiological Research. 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 Original Articles
Battaglia, Simone
Orsolini, Stefano
Borgomaneri, Sara
Barbieri, Riccardo
Diciotti, Stefano
di Pellegrino, Giuseppe
Characterizing cardiac autonomic dynamics of fear learning in humans
title Characterizing cardiac autonomic dynamics of fear learning in humans
title_full Characterizing cardiac autonomic dynamics of fear learning in humans
title_fullStr Characterizing cardiac autonomic dynamics of fear learning in humans
title_full_unstemmed Characterizing cardiac autonomic dynamics of fear learning in humans
title_short Characterizing cardiac autonomic dynamics of fear learning in humans
title_sort characterizing cardiac autonomic dynamics of fear learning in humans
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9787647/
https://www.ncbi.nlm.nih.gov/pubmed/35671393
http://dx.doi.org/10.1111/psyp.14122
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