High-definition spatiotemporal mapping of contractile activity in the isolated proximal colon of the rabbit

Abstract

Four types of contractile activity were identified and characterised in the isolated triple haustrated proximal colon of the rabbit using high-definition spatiotemporal mapping techniques. Mass peristalses were hexamethonium-sensitive deep circular contractions with associated taenial longitudinal contractile activity that occurred irregularly and propagated rapidly aborad, preceded by a zone of local lumen distension. They were sufficiently sustained for each event to occupy the length of the isolated colonic segment and the contraction persisted longer orally than aborally, the difference being more pronounced when lumen contents were viscous. Haustra were bounded by deep even-spaced ring contractions that progressed slowly aborad (haustral progression). Haustral formation and progression were hexamethonium-sensitive and coordinated across intertaenial domains. Ripples were hexamethonium-resistant phasic circular contractions that propagated predominantly orad at varying rates. In the presence of haustra, they were uncoordinated across intertaenial domains but were more coordinated when haustra were absent. Fast phasic contractions were relatively shallow hexamethonium-resistant contractions that propagated rapidly in a predominantly aborad direction. Fast phasic circular contractions were accompanied by taenial longitudinal muscle contractions which increased in amplitude prior to a mass peristaltic event and following the administration of hexamethonium. On the basis of the concurrence and interaction of these contractile activities, we hypothesise that dual pacemakers are present with fast phasic contractions being modulated by the interstitial cells of Cajal in the Auerbach's plexus (ICC-MY) while ripples are due to the submucosal ICC (ICC-SM). Further, that ICC-SM mediate the enteric motor neurons that generate haustral progression, while the intramuscular ICC (ICC-IM) mediate mass peristalsis. The orad movement of watery fluid was possibly due to ripples in the absence of haustra.

Neurogenic and myogenic motor patterns of rabbit proximal, mid, and distal colon

“…The deep indentations that delineated the haustra did not change in location during experiments, indicating that these are probably fixed points, probably due to connective tissue structures. This is at variance from Lentle et al who reported that all haustral indentations appear to propagate (28). We are currently unable to explain the difference between our results.…”

“…Such activity is likely to form the characteristic shape of the fecal pellets (16,17,35). The effect of hexamethonium indicates that nicotinic transmission is required for this cyclic motor activity (28). Nicotinic transmission mediates most fast excitatory synaptic transmission in enteric circuits (9) and thus underlies many neurally dependent enteric motor functions.…”

“…It is likely that different conditions of the luminal content (e.g., greater volume or viscosity) would generate neurally dependent movements on the oral side of the transition zone (28). The CMMCs in this study were found to propagate all the way along the single tenia region of the proximal colon to the colonic flexure (fusus coli) at a remarkably constant velocity, similar to those reported previously as "haustral progression" at 0.1 mm/s (28) and as "segmental contractions" at 0.1-0.3 mm/s (16,17). The characteristics of CMMCs in rabbit colon were similar to those described in other species (6,13,36,37,40).…”

“…Previous studies have investigated the motility in the rabbit proximal colon, both in vitro and in vivo (16,17,28,35). Other studies of isolated segments of rabbit distal colon described neural mechanisms involved in excretion of the fecal pellets (3,6,10,26).…”

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

“…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).…”