Neural mechanisms of peristalsis in the isolated rabbit distal colon: a neuromechanical loop hypothesis
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 p...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2014-04-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fnins.2014.00075/full |
| _version_ | 1818237689860718592 |
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| author | Phil eDinning Phil eDinning Lukasz eWiklendt Taher eOmari Taher eOmari John eArkwright Nicholas eSpencer Simon J H Brookes Marcello eCosta |
| author_facet | Phil eDinning Phil eDinning Lukasz eWiklendt Taher eOmari Taher eOmari John eArkwright Nicholas eSpencer Simon J H Brookes Marcello eCosta |
| author_sort | Phil eDinning |
| collection | DOAJ |
| description | 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 polarised 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 ± 1.4mm v 1.6 ± 1.2mm; 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. |
| first_indexed | 2024-12-12T12:29:45Z |
| format | Article |
| id | doaj.art-6a1dd0bcb71447929b4062db555da11d |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-12-12T12:29:45Z |
| publishDate | 2014-04-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-6a1dd0bcb71447929b4062db555da11d2022-12-22T00:24:26ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2014-04-01810.3389/fnins.2014.0007568307Neural mechanisms of peristalsis in the isolated rabbit distal colon: a neuromechanical loop hypothesisPhil eDinning0Phil eDinning1Lukasz eWiklendt2Taher eOmari3Taher eOmari4John eArkwright5Nicholas eSpencer6Simon J H Brookes7Marcello eCosta8Flinders Medical CentreFlinders UniversityFlinders UniversityFlinders UniversityChild, Youth and Women’s Health ServiceCSIROFlinders UniversityFlinders UniversityFlinders UniversityPropulsive 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 polarised 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 ± 1.4mm v 1.6 ± 1.2mm; 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.http://journal.frontiersin.org/Journal/10.3389/fnins.2014.00075/fullNeural PathwaysPeristalsiscolon motilityactive contractionactive relaxation |
| spellingShingle | Phil eDinning Phil eDinning Lukasz eWiklendt Taher eOmari Taher eOmari John eArkwright Nicholas eSpencer Simon J H Brookes Marcello eCosta Neural mechanisms of peristalsis in the isolated rabbit distal colon: a neuromechanical loop hypothesis Frontiers in Neuroscience Neural Pathways Peristalsis colon motility active contraction active relaxation |
| title | Neural mechanisms of peristalsis in the isolated rabbit distal colon: a neuromechanical loop hypothesis |
| title_full | Neural mechanisms of peristalsis in the isolated rabbit distal colon: a neuromechanical loop hypothesis |
| title_fullStr | Neural mechanisms of peristalsis in the isolated rabbit distal colon: a neuromechanical loop hypothesis |
| title_full_unstemmed | Neural mechanisms of peristalsis in the isolated rabbit distal colon: a neuromechanical loop hypothesis |
| title_short | Neural mechanisms of peristalsis in the isolated rabbit distal colon: a neuromechanical loop hypothesis |
| title_sort | neural mechanisms of peristalsis in the isolated rabbit distal colon a neuromechanical loop hypothesis |
| topic | Neural Pathways Peristalsis colon motility active contraction active relaxation |
| url | http://journal.frontiersin.org/Journal/10.3389/fnins.2014.00075/full |
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