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Type: Journal article
Title: Neural mechanisms of peristalsis in the isolated rabbit distal colon: a neuromechanical loop hypothesis
Author: Dinning, P.
Wiklendt, L.
Omari, T.
Arkwright, J.
Spencer, N.
Brookes, S.
Costa, M.
Citation: Frontiers in Neuroscience, 2014; 8(8 APR):75-1-75-15
Publisher: Frontiers Research Foundation
Issue Date: 2014
ISSN: 1662-4548
Statement of
Phil G. Dinning, Lukasz Wiklendt, Taher Omari, John W. Arkwright, Nick J. Spencer, Simon J. H. Brookes and Marcello Costa
Abstract: Propulsive contractions of circular muscle are largely responsible for the movements of content along the digestive tract. Mechanical and electrophysiological recordings of isolated colonic circular muscle have demonstrated that localized distension activates ascending and descending interneuronal pathways, evoking contraction orally and relaxation anally. These polarized enteric reflex pathways can theoretically be sequentially activated by the mechanical stimulation of the advancing contents. Here, we test the hypothesis that initiation and propagation of peristaltic contractions involves a neuromechanical loop; that is an initial gut distension activates local and oral reflex contraction and anal reflex relaxation, the subsequent movement of content then acts as new mechanical stimulus triggering sequentially reflex contractions/relaxations at each point of the gut resulting in a propulsive peristaltic contraction. In fluid filled isolated rabbit distal colon, we combined spatiotemporal mapping of gut diameter and intraluminal pressure with a new analytical method, allowing us to identify when and where active (neurally-driven) contraction or relaxation occurs. Our data indicate that gut dilation is associated with propagating peristaltic contractions, and that the associated level of dilation is greater than that preceding non-propagating contractions (2.7 ± 1.4 mm vs. 1.6 ± 1.2 mm; P < 0.0001). These propagating contractions lead to the formation of boluses that are propelled by oral active neurally driven contractions. The propelled boluses also activate neurally driven anal relaxations, in a diameter dependent manner. These data support the hypothesis that neural peristalsis is the consequence of the activation of a functional loop involving mechanical dilation which activates polarized enteric circuits. These produce propulsion of the bolus which activates further anally, polarized enteric circuits by distension, thus closing the neuromechanical loop.
Keywords: colon motility; peristalsis; neural pathways; active contraction; active relaxation
Description: Published online: 16 April 2014.
Rights: © 2014 Dinning, Wiklendt, Omari, Arkwright, Spencer, Brookes and Costa. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
DOI: 10.3389/fnins.2014.00075
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