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Preliminary report: parasympathetic tone links to functional brain networks during the anticipation and experience of visceral pain

The mechanisms that underpin the anti-nociceptive effect of the parasympathetic nervous system (PNS) on visceral pain remain incompletely understood. We sought to describe the effect of resting parasympathetic tone on functional brain networks during the anticipation and experience of oesophageal pa...

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Autores principales: Ruffle, James K., Coen, Steven J., Giampietro, Vincent, Williams, Steven C. R., Aziz, Qasim, Farmer, Adam D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6128833/
https://www.ncbi.nlm.nih.gov/pubmed/30194351
http://dx.doi.org/10.1038/s41598-018-31522-2
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author Ruffle, James K.
Coen, Steven J.
Giampietro, Vincent
Williams, Steven C. R.
Aziz, Qasim
Farmer, Adam D.
author_facet Ruffle, James K.
Coen, Steven J.
Giampietro, Vincent
Williams, Steven C. R.
Aziz, Qasim
Farmer, Adam D.
author_sort Ruffle, James K.
collection PubMed
description The mechanisms that underpin the anti-nociceptive effect of the parasympathetic nervous system (PNS) on visceral pain remain incompletely understood. We sought to describe the effect of resting parasympathetic tone on functional brain networks during the anticipation and experience of oesophageal pain. 21 healthy participants had their resting cardiac vagal tone (CVT), a validated measure of the PNS, quantified, and underwent functional magnetic resonance imaging during the anticipation and experience of painful oesophageal distention. The relationship between resting CVT and functional brain networks was examined using 11 hypothesis-driven nodes and network-based statistics. A network comprising all nodes was apparent in individuals with high resting CVT, compared to those with low CVT, during oesophageal pain (family wise error rate (FWER)-corrected p < 0.048). Functional connections included the thalamus-amygdala, thalamus-hypothalamus, hypothalamus-nucleus accumbens, amygdala-pallidum, pallidum-nucleus accumbens and insula-pallidum. A smaller network was seen during pain anticipation, comprising the amygdala, pallidum and anterior insula (FWER-corrected p < 0.049). These findings suggest that PNS tone is associated with functional brain networks during the anticipation and experience of visceral pain. Given the role of these subcortical regions in the descending inhibitory modulation of pain, these networks may represent a potential neurobiological explanation for the anti-nociceptive effect of the PNS.
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spelling pubmed-61288332018-09-10 Preliminary report: parasympathetic tone links to functional brain networks during the anticipation and experience of visceral pain Ruffle, James K. Coen, Steven J. Giampietro, Vincent Williams, Steven C. R. Aziz, Qasim Farmer, Adam D. Sci Rep Article The mechanisms that underpin the anti-nociceptive effect of the parasympathetic nervous system (PNS) on visceral pain remain incompletely understood. We sought to describe the effect of resting parasympathetic tone on functional brain networks during the anticipation and experience of oesophageal pain. 21 healthy participants had their resting cardiac vagal tone (CVT), a validated measure of the PNS, quantified, and underwent functional magnetic resonance imaging during the anticipation and experience of painful oesophageal distention. The relationship between resting CVT and functional brain networks was examined using 11 hypothesis-driven nodes and network-based statistics. A network comprising all nodes was apparent in individuals with high resting CVT, compared to those with low CVT, during oesophageal pain (family wise error rate (FWER)-corrected p < 0.048). Functional connections included the thalamus-amygdala, thalamus-hypothalamus, hypothalamus-nucleus accumbens, amygdala-pallidum, pallidum-nucleus accumbens and insula-pallidum. A smaller network was seen during pain anticipation, comprising the amygdala, pallidum and anterior insula (FWER-corrected p < 0.049). These findings suggest that PNS tone is associated with functional brain networks during the anticipation and experience of visceral pain. Given the role of these subcortical regions in the descending inhibitory modulation of pain, these networks may represent a potential neurobiological explanation for the anti-nociceptive effect of the PNS. Nature Publishing Group UK 2018-09-07 /pmc/articles/PMC6128833/ /pubmed/30194351 http://dx.doi.org/10.1038/s41598-018-31522-2 Text en © The Author(s) 2018 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Ruffle, James K.
Coen, Steven J.
Giampietro, Vincent
Williams, Steven C. R.
Aziz, Qasim
Farmer, Adam D.
Preliminary report: parasympathetic tone links to functional brain networks during the anticipation and experience of visceral pain
title Preliminary report: parasympathetic tone links to functional brain networks during the anticipation and experience of visceral pain
title_full Preliminary report: parasympathetic tone links to functional brain networks during the anticipation and experience of visceral pain
title_fullStr Preliminary report: parasympathetic tone links to functional brain networks during the anticipation and experience of visceral pain
title_full_unstemmed Preliminary report: parasympathetic tone links to functional brain networks during the anticipation and experience of visceral pain
title_short Preliminary report: parasympathetic tone links to functional brain networks during the anticipation and experience of visceral pain
title_sort preliminary report: parasympathetic tone links to functional brain networks during the anticipation and experience of visceral pain
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6128833/
https://www.ncbi.nlm.nih.gov/pubmed/30194351
http://dx.doi.org/10.1038/s41598-018-31522-2
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