Multiple neural oscillators and muscle feedback are required for the intestinal fed state motor program.

After a meal, the gastrointestinal tract exhibits a set of behaviours known as the fed state. A major feature of the fed state is a little understood motor pattern known as segmentation, which is essential for digestion and nutrient absorption. Segmentation manifests as rhythmic local constrictions...

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Autores principales:	Jordan D Chambers, Joel C Bornstein, Evan A Thomas
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2011
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/eacebae1dc894c20a411b68d07feae5b
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spelling	oai:doaj.org-article:eacebae1dc894c20a411b68d07feae5b2021-11-18T06:54:25ZMultiple neural oscillators and muscle feedback are required for the intestinal fed state motor program.1932-620310.1371/journal.pone.0019597https://doaj.org/article/eacebae1dc894c20a411b68d07feae5b2011-05-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21573176/?tool=EBIhttps://doaj.org/toc/1932-6203After a meal, the gastrointestinal tract exhibits a set of behaviours known as the fed state. A major feature of the fed state is a little understood motor pattern known as segmentation, which is essential for digestion and nutrient absorption. Segmentation manifests as rhythmic local constrictions that do not propagate along the intestine. In guinea-pig jejunum in vitro segmentation constrictions occur in short bursts together with other motor patterns in episodes of activity lasting 40-60 s and separated by quiescent episodes lasting 40-200 s. This activity is induced by luminal nutrients and abolished by blocking activity in the enteric nervous system (ENS). We investigated the enteric circuits that regulate segmentation focusing on a central feature of the ENS: a recurrent excitatory network of intrinsic sensory neurons (ISNs) which are characterized by prolonged after-hyperpolarizing potentials (AHPs) following their action potentials. We first examined the effects of depressing AHPs with blockers of the underlying channels (TRAM-34 and clotrimazole) on motor patterns induced in guinea-pig jejunum, in vitro, by luminal decanoic acid. Contractile episode durations increased markedly, but the frequency and number of constrictions within segmenting bursts and quiescent period durations were unaffected. We used these observations to develop a computational model of activity in ISNs, excitatory and inhibitory motor neurons and the muscle. The model predicted that: i) feedback to ISNs from contractions in the circular muscle is required to produce alternating activity and quiescence with the right durations; ii) transmission from ISNs to excitatory motor neurons is via fast excitatory synaptic potentials (EPSPs) and to inhibitory motor neurons via slow EPSPs. We conclude that two rhythm generators regulate segmentation: one drives contractions within segmentation bursts, the other the occurrence of bursts. The latter depends on AHPs in ISNs and feedback to these neurons from contraction of the circular muscle.Jordan D ChambersJoel C BornsteinEvan A ThomasPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 6, Iss 5, p e19597 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Jordan D Chambers Joel C Bornstein Evan A Thomas Multiple neural oscillators and muscle feedback are required for the intestinal fed state motor program.
description	After a meal, the gastrointestinal tract exhibits a set of behaviours known as the fed state. A major feature of the fed state is a little understood motor pattern known as segmentation, which is essential for digestion and nutrient absorption. Segmentation manifests as rhythmic local constrictions that do not propagate along the intestine. In guinea-pig jejunum in vitro segmentation constrictions occur in short bursts together with other motor patterns in episodes of activity lasting 40-60 s and separated by quiescent episodes lasting 40-200 s. This activity is induced by luminal nutrients and abolished by blocking activity in the enteric nervous system (ENS). We investigated the enteric circuits that regulate segmentation focusing on a central feature of the ENS: a recurrent excitatory network of intrinsic sensory neurons (ISNs) which are characterized by prolonged after-hyperpolarizing potentials (AHPs) following their action potentials. We first examined the effects of depressing AHPs with blockers of the underlying channels (TRAM-34 and clotrimazole) on motor patterns induced in guinea-pig jejunum, in vitro, by luminal decanoic acid. Contractile episode durations increased markedly, but the frequency and number of constrictions within segmenting bursts and quiescent period durations were unaffected. We used these observations to develop a computational model of activity in ISNs, excitatory and inhibitory motor neurons and the muscle. The model predicted that: i) feedback to ISNs from contractions in the circular muscle is required to produce alternating activity and quiescence with the right durations; ii) transmission from ISNs to excitatory motor neurons is via fast excitatory synaptic potentials (EPSPs) and to inhibitory motor neurons via slow EPSPs. We conclude that two rhythm generators regulate segmentation: one drives contractions within segmentation bursts, the other the occurrence of bursts. The latter depends on AHPs in ISNs and feedback to these neurons from contraction of the circular muscle.
format	article
author	Jordan D Chambers Joel C Bornstein Evan A Thomas
author_facet	Jordan D Chambers Joel C Bornstein Evan A Thomas
author_sort	Jordan D Chambers
title	Multiple neural oscillators and muscle feedback are required for the intestinal fed state motor program.
title_short	Multiple neural oscillators and muscle feedback are required for the intestinal fed state motor program.
title_full	Multiple neural oscillators and muscle feedback are required for the intestinal fed state motor program.
title_fullStr	Multiple neural oscillators and muscle feedback are required for the intestinal fed state motor program.
title_full_unstemmed	Multiple neural oscillators and muscle feedback are required for the intestinal fed state motor program.
title_sort	multiple neural oscillators and muscle feedback are required for the intestinal fed state motor program.
publisher	Public Library of Science (PLoS)
publishDate	2011
url	https://doaj.org/article/eacebae1dc894c20a411b68d07feae5b
work_keys_str_mv	AT jordandchambers multipleneuraloscillatorsandmusclefeedbackarerequiredfortheintestinalfedstatemotorprogram AT joelcbornstein multipleneuraloscillatorsandmusclefeedbackarerequiredfortheintestinalfedstatemotorprogram AT evanathomas multipleneuraloscillatorsandmusclefeedbackarerequiredfortheintestinalfedstatemotorprogram
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Multiple neural oscillators and muscle feedback are required for the intestinal fed state motor program.

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