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Neuroanatomical substrates for the volitional regulation of heart rate

The control of physiological arousal can assist in the regulation of emotional state. A subset cortical and subcortical brain regions are implicated in autonomic control of bodily arousal during emotional behaviors. Here, we combined human functional neuroimaging with autonomic monitoring to identif...

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Autores principales: Jones, Catherine L., Minati, Ludovico, Nagai, Yoko, Medford, Nick, Harrison, Neil A., Gray, Marcus, Ward, Jamie, Critchley, Hugo D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4373272/
https://www.ncbi.nlm.nih.gov/pubmed/25992711
http://dx.doi.org/10.3389/fpsyg.2015.00300
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author Jones, Catherine L.
Minati, Ludovico
Nagai, Yoko
Medford, Nick
Harrison, Neil A.
Gray, Marcus
Ward, Jamie
Critchley, Hugo D.
author_facet Jones, Catherine L.
Minati, Ludovico
Nagai, Yoko
Medford, Nick
Harrison, Neil A.
Gray, Marcus
Ward, Jamie
Critchley, Hugo D.
author_sort Jones, Catherine L.
collection PubMed
description The control of physiological arousal can assist in the regulation of emotional state. A subset cortical and subcortical brain regions are implicated in autonomic control of bodily arousal during emotional behaviors. Here, we combined human functional neuroimaging with autonomic monitoring to identify neural mechanisms that support the volitional regulation of heart rate, a process that may be assisted by visual feedback. During functional magnetic resonance imaging (fMRI), 15 healthy adults performed an experimental task in which they were prompted voluntarily to increase or decrease cardiovascular arousal (heart rate) during true, false, or absent visual feedback. Participants achieved appropriate changes in heart rate, without significant modulation of respiratory rate, and were overall not influenced by the presence of visual feedback. Increased activity in right amygdala, striatum and brainstem occurred when participants attempted to increase heart rate. In contrast, activation of ventrolateral prefrontal and parietal cortices occurred when attempting to decrease heart rate. Biofeedback enhanced activity within occipito-temporal cortices, but there was no significant interaction with task conditions. Activity in regions including pregenual anterior cingulate and ventral striatum reflected the magnitude of successful task performance, which was negatively related to subclinical anxiety symptoms. Measured changes in respiration correlated with posterior insula activation and heart rate, at a more lenient threshold, change correlated with insula, caudate, and midbrain activity. Our findings highlight a set of brain regions, notably ventrolateral prefrontal cortex, supporting volitional control of cardiovascular arousal. These data are relevant to understanding neural substrates supporting interaction between intentional and interoceptive states related to anxiety, with implications for biofeedback interventions, e.g., real-time fMRI, that target emotional regulation.
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spelling pubmed-43732722015-04-09 Neuroanatomical substrates for the volitional regulation of heart rate Jones, Catherine L. Minati, Ludovico Nagai, Yoko Medford, Nick Harrison, Neil A. Gray, Marcus Ward, Jamie Critchley, Hugo D. Front Psychol Psychology The control of physiological arousal can assist in the regulation of emotional state. A subset cortical and subcortical brain regions are implicated in autonomic control of bodily arousal during emotional behaviors. Here, we combined human functional neuroimaging with autonomic monitoring to identify neural mechanisms that support the volitional regulation of heart rate, a process that may be assisted by visual feedback. During functional magnetic resonance imaging (fMRI), 15 healthy adults performed an experimental task in which they were prompted voluntarily to increase or decrease cardiovascular arousal (heart rate) during true, false, or absent visual feedback. Participants achieved appropriate changes in heart rate, without significant modulation of respiratory rate, and were overall not influenced by the presence of visual feedback. Increased activity in right amygdala, striatum and brainstem occurred when participants attempted to increase heart rate. In contrast, activation of ventrolateral prefrontal and parietal cortices occurred when attempting to decrease heart rate. Biofeedback enhanced activity within occipito-temporal cortices, but there was no significant interaction with task conditions. Activity in regions including pregenual anterior cingulate and ventral striatum reflected the magnitude of successful task performance, which was negatively related to subclinical anxiety symptoms. Measured changes in respiration correlated with posterior insula activation and heart rate, at a more lenient threshold, change correlated with insula, caudate, and midbrain activity. Our findings highlight a set of brain regions, notably ventrolateral prefrontal cortex, supporting volitional control of cardiovascular arousal. These data are relevant to understanding neural substrates supporting interaction between intentional and interoceptive states related to anxiety, with implications for biofeedback interventions, e.g., real-time fMRI, that target emotional regulation. Frontiers Media S.A. 2015-03-25 /pmc/articles/PMC4373272/ /pubmed/25992711 http://dx.doi.org/10.3389/fpsyg.2015.00300 Text en Copyright © 2015 Jones, Minati, Nagai, Medford, Harrison, Gray, Ward and Critchley. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Psychology
Jones, Catherine L.
Minati, Ludovico
Nagai, Yoko
Medford, Nick
Harrison, Neil A.
Gray, Marcus
Ward, Jamie
Critchley, Hugo D.
Neuroanatomical substrates for the volitional regulation of heart rate
title Neuroanatomical substrates for the volitional regulation of heart rate
title_full Neuroanatomical substrates for the volitional regulation of heart rate
title_fullStr Neuroanatomical substrates for the volitional regulation of heart rate
title_full_unstemmed Neuroanatomical substrates for the volitional regulation of heart rate
title_short Neuroanatomical substrates for the volitional regulation of heart rate
title_sort neuroanatomical substrates for the volitional regulation of heart rate
topic Psychology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4373272/
https://www.ncbi.nlm.nih.gov/pubmed/25992711
http://dx.doi.org/10.3389/fpsyg.2015.00300
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