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Long range synchronization within the enteric nervous system underlies propulsion along the large intestine in mice
How the Enteric Nervous System (ENS) coordinates propulsion of content along the gastrointestinal (GI)-tract has been a major unresolved issue. We reveal a mechanism that explains how ENS activity underlies propulsion of content along the colon. We used a recently developed high-resolution video ima...
Autores principales: | , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Nature Publishing Group UK
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8355373/ https://www.ncbi.nlm.nih.gov/pubmed/34376798 http://dx.doi.org/10.1038/s42003-021-02485-4 |
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author | Spencer, Nick J. Travis, Lee Wiklendt, Lukasz Costa, Marcello Hibberd, Timothy J. Brookes, Simon J. Dinning, Phil Hu, Hongzhen Wattchow, David A. Sorensen, Julian |
author_facet | Spencer, Nick J. Travis, Lee Wiklendt, Lukasz Costa, Marcello Hibberd, Timothy J. Brookes, Simon J. Dinning, Phil Hu, Hongzhen Wattchow, David A. Sorensen, Julian |
author_sort | Spencer, Nick J. |
collection | PubMed |
description | How the Enteric Nervous System (ENS) coordinates propulsion of content along the gastrointestinal (GI)-tract has been a major unresolved issue. We reveal a mechanism that explains how ENS activity underlies propulsion of content along the colon. We used a recently developed high-resolution video imaging approach with concurrent electrophysiological recordings from smooth muscle, during fluid propulsion. Recordings showed pulsatile firing of excitatory and inhibitory neuromuscular inputs not only in proximal colon, but also distal colon, long before the propagating contraction invades the distal region. During propulsion, wavelet analysis revealed increased coherence at ~2 Hz over large distances between the proximal and distal regions. Therefore, during propulsion, synchronous firing of descending inhibitory nerve pathways over long ranges aborally acts to suppress smooth muscle from contracting, counteracting the excitatory nerve pathways over this same region of colon. This delays muscle contraction downstream, ahead of the advancing contraction. The mechanism identified is more complex than expected and vastly different from fluid propulsion along other hollow smooth muscle organs; like lymphatic vessels, portal vein, or ureters, that evolved without intrinsic neurons. |
format | Online Article Text |
id | pubmed-8355373 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | Nature Publishing Group UK |
record_format | MEDLINE/PubMed |
spelling | pubmed-83553732021-08-30 Long range synchronization within the enteric nervous system underlies propulsion along the large intestine in mice Spencer, Nick J. Travis, Lee Wiklendt, Lukasz Costa, Marcello Hibberd, Timothy J. Brookes, Simon J. Dinning, Phil Hu, Hongzhen Wattchow, David A. Sorensen, Julian Commun Biol Article How the Enteric Nervous System (ENS) coordinates propulsion of content along the gastrointestinal (GI)-tract has been a major unresolved issue. We reveal a mechanism that explains how ENS activity underlies propulsion of content along the colon. We used a recently developed high-resolution video imaging approach with concurrent electrophysiological recordings from smooth muscle, during fluid propulsion. Recordings showed pulsatile firing of excitatory and inhibitory neuromuscular inputs not only in proximal colon, but also distal colon, long before the propagating contraction invades the distal region. During propulsion, wavelet analysis revealed increased coherence at ~2 Hz over large distances between the proximal and distal regions. Therefore, during propulsion, synchronous firing of descending inhibitory nerve pathways over long ranges aborally acts to suppress smooth muscle from contracting, counteracting the excitatory nerve pathways over this same region of colon. This delays muscle contraction downstream, ahead of the advancing contraction. The mechanism identified is more complex than expected and vastly different from fluid propulsion along other hollow smooth muscle organs; like lymphatic vessels, portal vein, or ureters, that evolved without intrinsic neurons. Nature Publishing Group UK 2021-08-10 /pmc/articles/PMC8355373/ /pubmed/34376798 http://dx.doi.org/10.1038/s42003-021-02485-4 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/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/ (https://creativecommons.org/licenses/by/4.0/) . |
spellingShingle | Article Spencer, Nick J. Travis, Lee Wiklendt, Lukasz Costa, Marcello Hibberd, Timothy J. Brookes, Simon J. Dinning, Phil Hu, Hongzhen Wattchow, David A. Sorensen, Julian Long range synchronization within the enteric nervous system underlies propulsion along the large intestine in mice |
title | Long range synchronization within the enteric nervous system underlies propulsion along the large intestine in mice |
title_full | Long range synchronization within the enteric nervous system underlies propulsion along the large intestine in mice |
title_fullStr | Long range synchronization within the enteric nervous system underlies propulsion along the large intestine in mice |
title_full_unstemmed | Long range synchronization within the enteric nervous system underlies propulsion along the large intestine in mice |
title_short | Long range synchronization within the enteric nervous system underlies propulsion along the large intestine in mice |
title_sort | long range synchronization within the enteric nervous system underlies propulsion along the large intestine in mice |
topic | Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8355373/ https://www.ncbi.nlm.nih.gov/pubmed/34376798 http://dx.doi.org/10.1038/s42003-021-02485-4 |
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