Mechanisms underlying distension-evoked peristalsis in guinea pig distal colon: is there a role for enterochromaffin cells?

Abstract

The mechanisms underlying distension-evoked peristalsis in the colon are incompletely understood. It is well known that, following colonic distension, 5-hydroxytryptamine (5-HT) is released from enterochromaffin (EC) cells in the intestinal mucosa. It is also known that exogenous 5-HT can stimulate peristalsis. These observations have led some investigators to propose that endogenous 5-HT release from EC cells might be involved in the initiation of colonic peristalsis, following distension. However, because no direct evidence exists to support this hypothesis, the aim of this study was to determine directly whether release of 5-HT from EC cells was required for distension-evoked colonic peristalsis. Real-time amperometric recordings of 5-HT release and video imaging of colonic wall movements were performed on isolated segments of guinea pig distal colon, during distension-evoked peristalsis. Amperometric recordings revealed basal and transient release of 5-HT from EC cells before and during the initiation of peristalsis, respectively. However, removal of mucosa (and submucosal plexus) abolished 5-HT release but did not inhibit the initiation of peristalsis nor prevent the propagation of fecal pellets or intraluminal fluid. Maintained colonic distension by fecal pellets induced repetitive peristaltic waves, whose intrinsic frequency was also unaffected by removal of the submucosal plexus and mucosa, although their propagation velocities were slower. In conclusion, the mechanoreceptors and sensory neurons activated by radial distension to initiate peristalsis lie in the myenteric plexus and/or muscularis externa, and their activation does not require the submucosal plexus, release of 5-HT from EC cells, nor the presence of the mucosa. The propagation of peristalsis and propulsion of liquid or solid content along the colon is entrained by activity within the myenteric plexus and/or muscularis externa and does not require sensory feedback from the mucosa, nor neural inputs arising from submucosal ganglia.

Characterization of the motor inhibitory role of colonic mucosa under chemical stimulation in mice

“…In keeping with the motor regulatory role of the mucosa described herein, a study from our group shows an excitatory effect of the mucosa on spontaneous phasic contractions (Martin-Cano, Camello, and Pozo, unpublished observation) that agrees with the excitatory role of the mucosa in distensionevoked peristalsis (10) and fecal pellet propulsion (24). In fact, herein both effects of the mucosa controlling the colonic motility can be observed in Fig.…”

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

“…While the use of STmaps of luminal diameter have improved the ability to visualize and analyze full motility patterns over a region of intestine, the technique is best used when coupled with functional measurements of pressure or muscle contraction 2,15,20 . For instance, while some muscle contractions may change luminal diameter slightly and be visible on some STmaps (i.e., myogenic ripples) they may not actually cause any propulsion or mixing of intestinal contents 25 .…”

“…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.…”

“…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...…”

“…While many groups have generated their own software packages or plugins, they all analyze diameters of a tissue segment and convert those various diameters to grayscale representation. A commercially available recording and analysis system called the GastroIntestinal Motility Monitoring system (GIMM) provides a turnkey approach that allows for analysis of both propulsive motility via fecal pellet velocity determination in the guinea pig distal colon 13 as well as analysis of propulsive and mixing motility patterns with a fluid stimulus in intact intestinal segments 4,5,[14][15][16][17][18][19] 4. General Experimental Procedures 1.…”