Mechanosensitive enteric neurons in the myenteric plexus of the mouse intestine.

<h4>Background</h4>Within the gut the autonomous enteric nervous system (ENS) is able to sense mechanical stimuli and to trigger gut reflex behaviour. We previously proposed a novel sensory circuit in the ENS which consists of multifunctional rapidly adapting mechanosensitive enteric neu...

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Autores principales:	Gemma Mazzuoli, Michael Schemann
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2012
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/807b4fe3d95546f580ba26687f72e4b0
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spelling	oai:doaj.org-article:807b4fe3d95546f580ba26687f72e4b02021-11-18T07:13:33ZMechanosensitive enteric neurons in the myenteric plexus of the mouse intestine.1932-620310.1371/journal.pone.0039887https://doaj.org/article/807b4fe3d95546f580ba26687f72e4b02012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22768317/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>Within the gut the autonomous enteric nervous system (ENS) is able to sense mechanical stimuli and to trigger gut reflex behaviour. We previously proposed a novel sensory circuit in the ENS which consists of multifunctional rapidly adapting mechanosensitive enteric neurons (RAMEN) in the guinea pig. The aim of this study was to validate this concept by studying its applicability to other species or gut regions.<h4>Methodology/principal findings</h4>We deformed myenteric ganglia in the mouse small and large intestine and recorded spike discharge using voltage sensitive dye imaging. We also analysed expression of markers hitherto proposed to label mouse sensory myenteric neurons in the ileum (NF145kD) or colon (calretinin). RAMEN constituted 22% and 15% of myenteric neurons per ganglion in the ileum and colon, respectively. They encoded dynamic rather than sustained deformation. In the colon, 7% of mechanosensitive neurons fired throughout the sustained deformation, a behaviour typical for slowly adapting echanosensitive neurons (SAMEN). RAMEN and SAMEN responded directly to mechanical deformation as their response remained unchanged after synaptic blockade in low Ca(++)/high Mg(++). Activity levels of RAMEN increased with the degree of ganglion deformation. Recruitment of more RAMEN with stronger stimuli may suggest low and high threshold RAMEN. The majority of RAMEN were cholinergic but most lacked expression of NF145kD or calretinin.<h4>Conclusions/significance</h4>We showed for the first time that fundamental properties of mechanosensitive enteric neurons, such as firing pattern, encoding of dynamic deformation, cholinergic phenotype and their proportion, are conserved across species and regions. We conclude that RAMEN are important for mechanotransduction in the ENS. They directly encode dynamic changes in force as their firing frequency is proportional to the degree of deformation of the ganglion they reside in. The additional existence of SAMEN in the colon is likely an adaptation to colonic motor patterns which consist of phasic and tonic contractions.Gemma MazzuoliMichael SchemannPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 7, Iss 7, p e39887 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Gemma Mazzuoli Michael Schemann Mechanosensitive enteric neurons in the myenteric plexus of the mouse intestine.
description	<h4>Background</h4>Within the gut the autonomous enteric nervous system (ENS) is able to sense mechanical stimuli and to trigger gut reflex behaviour. We previously proposed a novel sensory circuit in the ENS which consists of multifunctional rapidly adapting mechanosensitive enteric neurons (RAMEN) in the guinea pig. The aim of this study was to validate this concept by studying its applicability to other species or gut regions.<h4>Methodology/principal findings</h4>We deformed myenteric ganglia in the mouse small and large intestine and recorded spike discharge using voltage sensitive dye imaging. We also analysed expression of markers hitherto proposed to label mouse sensory myenteric neurons in the ileum (NF145kD) or colon (calretinin). RAMEN constituted 22% and 15% of myenteric neurons per ganglion in the ileum and colon, respectively. They encoded dynamic rather than sustained deformation. In the colon, 7% of mechanosensitive neurons fired throughout the sustained deformation, a behaviour typical for slowly adapting echanosensitive neurons (SAMEN). RAMEN and SAMEN responded directly to mechanical deformation as their response remained unchanged after synaptic blockade in low Ca(++)/high Mg(++). Activity levels of RAMEN increased with the degree of ganglion deformation. Recruitment of more RAMEN with stronger stimuli may suggest low and high threshold RAMEN. The majority of RAMEN were cholinergic but most lacked expression of NF145kD or calretinin.<h4>Conclusions/significance</h4>We showed for the first time that fundamental properties of mechanosensitive enteric neurons, such as firing pattern, encoding of dynamic deformation, cholinergic phenotype and their proportion, are conserved across species and regions. We conclude that RAMEN are important for mechanotransduction in the ENS. They directly encode dynamic changes in force as their firing frequency is proportional to the degree of deformation of the ganglion they reside in. The additional existence of SAMEN in the colon is likely an adaptation to colonic motor patterns which consist of phasic and tonic contractions.
format	article
author	Gemma Mazzuoli Michael Schemann
author_facet	Gemma Mazzuoli Michael Schemann
author_sort	Gemma Mazzuoli
title	Mechanosensitive enteric neurons in the myenteric plexus of the mouse intestine.
title_short	Mechanosensitive enteric neurons in the myenteric plexus of the mouse intestine.
title_full	Mechanosensitive enteric neurons in the myenteric plexus of the mouse intestine.
title_fullStr	Mechanosensitive enteric neurons in the myenteric plexus of the mouse intestine.
title_full_unstemmed	Mechanosensitive enteric neurons in the myenteric plexus of the mouse intestine.
title_sort	mechanosensitive enteric neurons in the myenteric plexus of the mouse intestine.
publisher	Public Library of Science (PLoS)
publishDate	2012
url	https://doaj.org/article/807b4fe3d95546f580ba26687f72e4b0
work_keys_str_mv	AT gemmamazzuoli mechanosensitiveentericneuronsinthemyentericplexusofthemouseintestine AT michaelschemann mechanosensitiveentericneuronsinthemyentericplexusofthemouseintestine
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Mechanosensitive enteric neurons in the myenteric plexus of the mouse intestine.

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