Neurogenic and myogenic motor activity in the colon of the guinea pig, mouse, rabbit, and rat

Abstract

Costa M, Dodds KN, Wiklendt L, Spencer NJ, Brookes SJ, Dinning PG. Neurogenic and myogenic motor activity in the colon of the guinea pig, mouse, rabbit, and rat. Am J Physiol Gastrointest Liver Physiol 305: G749 -G759, 2013. First published September 19, 2013 doi:10.1152/ajpgi.00227.2013.-Gastrointestinal motility involves interactions between myogenic and neurogenic processes intrinsic to the gut wall. We have compared the presence of propagating myogenic contractions of the isolated colon in four experimental animals (guinea pig, mouse, rabbit, and rat), following blockade of enteric neural activity. Isolated colonic preparations were distended with fluid, with the anal end either closed or open. Spatiotemporal maps of changes in diameter were constructed from video recordings. Distension-induced peristaltic contractions were abolished by tetrodotoxin (TTX; 0.6 M) in all animal species. Subsequent addition of carbachol (0.1-1 M) did not evoke myogenic motor patterns in the mouse or guinea pig, although some activity was observed in rabbit and rat colon. These myogenic contractions propagated both orally and anally and differed from neurogenic propagating contractions in their frequency, extent of propagation, and polarity. Niflumic acid (300 M), used to block myogenic activity, also blocked neural peristalsis and thus cannot be used to discriminate between these mechanisms. In all species, except the mouse colon, small myogenic "ripple" contractions were revealed in TTX, but in both rat and rabbit an additional, higher-frequency ripple-type contraction was superimposed. Following blockade of enteric nerve function, a muscarinic agonist can evoke propulsive myogenic peristaltic contractions in isolated rabbit and rat colon, but not in guinea pig or mouse colon. Marked differences between species exist in the ability of myogenic mechanisms to propel luminal content, but in all species there is normally a complex interplay between neurogenic and myogenic processes. colon motility; enteric neurons; spatiotemporal maps; peristalsis COLONIC MOTILITY IS CONTROLLED by complex interactive processes in the gut, involving both nerve cells (neurogenic) and spontaneous muscle activity (myogenic). A number of studies have characterized fundamental mechanisms in the colon of the guinea pig, mouse, and rabbit and have shown that propagating contractions underlying peristalsis, or other propulsive motor patterns, require activity in the enteric nervous system (8,11,13,14,17,25).In recent papers, Huizinga et al. (20) and Chen et al. (7) produced evidence that challenges this principle. In the rat colon, in vitro, they showed that, after blocking peristalsis with antagonists of enteric neuronal activity [tetrodotoxin (TTX) or lidocaine], addition of a cholinergic agonist induced a recovery in propagating contractions. From these data they suggested that networks of interstitial cells of Cajal (ICC) work cooperatively with the enteric nervous system to create colonic motor patterns and that the main propulsive mechanism is the ...

Spatiotemporal Mapping of Motility in <em>Ex Vivo</em> Preparations of the Intestines

“…While these patterns were identified by earlier experimental methods, the current approach allows a more refined definition of localized contractile movements such as ripples and novel antiperistaltic contractions 9,24,25,30,31,42 . The construction of STmaps and analysis of changes in motility pattern have been applied to key questions in the gastrointestinal motility of intestine and colon.…”

“…Video recording and spatiotemporal mapping of intestinal and colonic segments have been applied to a variety of species including zebrafish 26 , mouse 25,[27][28][29][30] , rat 7,9,[30][31][32][33] , guinea pig 5,6,8,[13][14][15][16][17][18][19]24,30,32,34,35 , brushtail possum 12,36 , rabbit 2,30,37,38 , chicken 39 , pig 40,41 and human 42 . The most widely studied species is the guinea pig.…”

“…Spatiotemporal mapping has been mostly applied to tubular segments of gut from small animals; however, studies in the rabbit and pig using modified systems demonstrate the application of this methodology to larger animals. In the case of the rabbit, the approach is identical to that of smaller animals except that larger segments and organ baths were used 30 . The approach used in the pig was to use an exteriorized loop of intestine from an anesthetized pig rather than immersion of a dissected tissue segment into an organ bath.…”

“…The construction of STmaps and analysis of changes in motility pattern have been applied to key questions in the gastrointestinal motility of intestine and colon. These include: differentiation of neurogenic and myogenic contractions and defining the role of interstitial cells of Cajal 6,9,11,12,16,24,26,27,[29][30][31]33,[37][38][39][40]42 , understanding the complex interactions between the circular and longitudinal muscle layers 2,7,8,11,12,32,39,40 , examining the effects of intraluminal nutrients 10,18,19 , microbial strains 34 , and viscosities 12,36 on various motility patterns, and understanding the role of various endogenous neurohormonal agents and exogenous pharmacological agents 2,[4][5][6][7]9,10,[13][14][15][16][17]28,35,40 in the generation and modification of motility...…”

Targeting Ion Channels: An Important Therapeutic Implication in Gastrointestinal Dysmotility in Patients With Spinal Cord Injury

“…ICC are mainly found in the mesenteric plexus which is located deep to muscular plexus close to smooth muscle 10 forming synapse like junctions with enteric nerve and forming gap junctions with smooth muscle cells. 11 They generate, and transmit signals from enteric neurons to smooth muscles through the gap junctions (Fig.…”