Cargando…

Parasympathetic activity correlates with subjective and brain responses to rectal distension in healthy subjects but not in non-constipated patients with irritable bowel syndrome

The nociceptive and autonomic nervous systems (ANS) are significantly intertwined. Decoupling of these systems may occur in pathological pain conditions, including irritable bowel syndrome (IBS). We investigated ANS activity and its association with visceral perception and brain activity during rect...

Descripción completa

Detalles Bibliográficos
Autores principales: Kano, Michiko, Yoshizawa, Makoto, Kono, Keiji, Muratsubaki, Tomohiko, Morishita, Joe, Van Oudenhove, Lukas, Yagihashi, Mao, Mugikura, Shunji, Dupont, Patrick, Takase, Kei, Kanazawa, Motoyori, Fukudo, Shin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6517375/
https://www.ncbi.nlm.nih.gov/pubmed/31089154
http://dx.doi.org/10.1038/s41598-019-43455-5
_version_ 1783418262816555008
author Kano, Michiko
Yoshizawa, Makoto
Kono, Keiji
Muratsubaki, Tomohiko
Morishita, Joe
Van Oudenhove, Lukas
Yagihashi, Mao
Mugikura, Shunji
Dupont, Patrick
Takase, Kei
Kanazawa, Motoyori
Fukudo, Shin
author_facet Kano, Michiko
Yoshizawa, Makoto
Kono, Keiji
Muratsubaki, Tomohiko
Morishita, Joe
Van Oudenhove, Lukas
Yagihashi, Mao
Mugikura, Shunji
Dupont, Patrick
Takase, Kei
Kanazawa, Motoyori
Fukudo, Shin
author_sort Kano, Michiko
collection PubMed
description The nociceptive and autonomic nervous systems (ANS) are significantly intertwined. Decoupling of these systems may occur in pathological pain conditions, including irritable bowel syndrome (IBS). We investigated ANS activity and its association with visceral perception and brain activity during rectal distention in 27 patients with non-constipated IBS and 33 controls by assessing heart rate variability (HRV) using electrocardiography at rest, before, and during colorectal distention. Brain responses to colorectal distention were measured using functional magnetic resonance imaging and correlated with individual ANS function parameters. The IBS group displayed blunted sympathovagal balance [low/high-frequency ratio (LF:HF) of HRV] in response to colorectal distention compared with controls (P = 0.003). In controls, basal parasympathetic tone (HF component of HRV) was significantly negatively correlated with toleration threshold to the rectal distention, but not in patients with IBS (group comparison P = 0.04). Further, a positive correlation between baseline HF values and neural responses to rectal distension was found in the right caudate, bilateral dorsolateral anterior cingulate cortex, and pregenual anterior cingulate cortex in the control group but not in the IBS group. The results indicate abnormal interactions between ANS activity and the brain mechanisms underlying visceral perception in patients with IBS.
format Online
Article
Text
id pubmed-6517375
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-65173752019-05-24 Parasympathetic activity correlates with subjective and brain responses to rectal distension in healthy subjects but not in non-constipated patients with irritable bowel syndrome Kano, Michiko Yoshizawa, Makoto Kono, Keiji Muratsubaki, Tomohiko Morishita, Joe Van Oudenhove, Lukas Yagihashi, Mao Mugikura, Shunji Dupont, Patrick Takase, Kei Kanazawa, Motoyori Fukudo, Shin Sci Rep Article The nociceptive and autonomic nervous systems (ANS) are significantly intertwined. Decoupling of these systems may occur in pathological pain conditions, including irritable bowel syndrome (IBS). We investigated ANS activity and its association with visceral perception and brain activity during rectal distention in 27 patients with non-constipated IBS and 33 controls by assessing heart rate variability (HRV) using electrocardiography at rest, before, and during colorectal distention. Brain responses to colorectal distention were measured using functional magnetic resonance imaging and correlated with individual ANS function parameters. The IBS group displayed blunted sympathovagal balance [low/high-frequency ratio (LF:HF) of HRV] in response to colorectal distention compared with controls (P = 0.003). In controls, basal parasympathetic tone (HF component of HRV) was significantly negatively correlated with toleration threshold to the rectal distention, but not in patients with IBS (group comparison P = 0.04). Further, a positive correlation between baseline HF values and neural responses to rectal distension was found in the right caudate, bilateral dorsolateral anterior cingulate cortex, and pregenual anterior cingulate cortex in the control group but not in the IBS group. The results indicate abnormal interactions between ANS activity and the brain mechanisms underlying visceral perception in patients with IBS. Nature Publishing Group UK 2019-05-14 /pmc/articles/PMC6517375/ /pubmed/31089154 http://dx.doi.org/10.1038/s41598-019-43455-5 Text en © The Author(s) 2019 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
Kano, Michiko
Yoshizawa, Makoto
Kono, Keiji
Muratsubaki, Tomohiko
Morishita, Joe
Van Oudenhove, Lukas
Yagihashi, Mao
Mugikura, Shunji
Dupont, Patrick
Takase, Kei
Kanazawa, Motoyori
Fukudo, Shin
Parasympathetic activity correlates with subjective and brain responses to rectal distension in healthy subjects but not in non-constipated patients with irritable bowel syndrome
title Parasympathetic activity correlates with subjective and brain responses to rectal distension in healthy subjects but not in non-constipated patients with irritable bowel syndrome
title_full Parasympathetic activity correlates with subjective and brain responses to rectal distension in healthy subjects but not in non-constipated patients with irritable bowel syndrome
title_fullStr Parasympathetic activity correlates with subjective and brain responses to rectal distension in healthy subjects but not in non-constipated patients with irritable bowel syndrome
title_full_unstemmed Parasympathetic activity correlates with subjective and brain responses to rectal distension in healthy subjects but not in non-constipated patients with irritable bowel syndrome
title_short Parasympathetic activity correlates with subjective and brain responses to rectal distension in healthy subjects but not in non-constipated patients with irritable bowel syndrome
title_sort parasympathetic activity correlates with subjective and brain responses to rectal distension in healthy subjects but not in non-constipated patients with irritable bowel syndrome
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6517375/
https://www.ncbi.nlm.nih.gov/pubmed/31089154
http://dx.doi.org/10.1038/s41598-019-43455-5
work_keys_str_mv AT kanomichiko parasympatheticactivitycorrelateswithsubjectiveandbrainresponsestorectaldistensioninhealthysubjectsbutnotinnonconstipatedpatientswithirritablebowelsyndrome
AT yoshizawamakoto parasympatheticactivitycorrelateswithsubjectiveandbrainresponsestorectaldistensioninhealthysubjectsbutnotinnonconstipatedpatientswithirritablebowelsyndrome
AT konokeiji parasympatheticactivitycorrelateswithsubjectiveandbrainresponsestorectaldistensioninhealthysubjectsbutnotinnonconstipatedpatientswithirritablebowelsyndrome
AT muratsubakitomohiko parasympatheticactivitycorrelateswithsubjectiveandbrainresponsestorectaldistensioninhealthysubjectsbutnotinnonconstipatedpatientswithirritablebowelsyndrome
AT morishitajoe parasympatheticactivitycorrelateswithsubjectiveandbrainresponsestorectaldistensioninhealthysubjectsbutnotinnonconstipatedpatientswithirritablebowelsyndrome
AT vanoudenhovelukas parasympatheticactivitycorrelateswithsubjectiveandbrainresponsestorectaldistensioninhealthysubjectsbutnotinnonconstipatedpatientswithirritablebowelsyndrome
AT yagihashimao parasympatheticactivitycorrelateswithsubjectiveandbrainresponsestorectaldistensioninhealthysubjectsbutnotinnonconstipatedpatientswithirritablebowelsyndrome
AT mugikurashunji parasympatheticactivitycorrelateswithsubjectiveandbrainresponsestorectaldistensioninhealthysubjectsbutnotinnonconstipatedpatientswithirritablebowelsyndrome
AT dupontpatrick parasympatheticactivitycorrelateswithsubjectiveandbrainresponsestorectaldistensioninhealthysubjectsbutnotinnonconstipatedpatientswithirritablebowelsyndrome
AT takasekei parasympatheticactivitycorrelateswithsubjectiveandbrainresponsestorectaldistensioninhealthysubjectsbutnotinnonconstipatedpatientswithirritablebowelsyndrome
AT kanazawamotoyori parasympatheticactivitycorrelateswithsubjectiveandbrainresponsestorectaldistensioninhealthysubjectsbutnotinnonconstipatedpatientswithirritablebowelsyndrome
AT fukudoshin parasympatheticactivitycorrelateswithsubjectiveandbrainresponsestorectaldistensioninhealthysubjectsbutnotinnonconstipatedpatientswithirritablebowelsyndrome