A smooth muscle tone-dependent stretch-activated migrating motor pattern in isolated guinea-pig distal colon.

We have investigated the tone dependence of the intrinsic nervous activity generated by localized wall distension in isolated segments of guinea-pig distal colon using mechanical recordings and video imaging of wall movements. A segment of colon was threaded through two partitions, which divided the colon for pharmacological purposes into oral, stimulation and anal regions. An intraluminal balloon was located in the stimulation region between the two partitions (12 mm apart). Maintained colonic distension by an intraluminal balloon or an artificial faecal pellet held at a fixed location generated rhythmic (frequency 0.3 contractions min(-1); duration approximately 60 s) peristaltic waves of contraction. Video imaging of colonic wall movements or the selective application of pharmacological agents suggested that peristaltic waves originated just oral (< or = 4 mm) to the pellet and propagated both orally (approximately 11 mm s(-1)) and anally (approximately 1 mm s(-1)). Also, during a peristaltic wave the colon appears to passively shorten in front of a pellet, as a result of an active contraction of the longitudinal muscle oral to the pellet. Faecal pellet movement only occurred when a rhythmic peristaltic wave was generated. Rhythmic peristaltic waves were abolished in all regions by the smooth muscle relaxants isoproterenol (1 microM), nicardipine (1 microM) or papavarine (10 microM), and by the neural antagonists tetrodotoxin (TTX; 0.6 microM), hexamethonium (100 microM) or atropine (1 microM), when added selectively to the stimulation region. Nicardipine, atropine, TTX, or hexamethonium (100 microM) also blocked the evoked peristaltic waves when selectively added to the oral region. Nomega-nitro-L-arginine (L-NA; 100 microM) added to the anal region reduced the anal relaxation but increased the anal contraction, leading to an increase in the apparent conduction velocity of each peristaltic wave. In conclusion, maintained distension by a fixed artificial pellet generates propulsive, rhythmic peristaltic waves, whose enteric neural activity is critically dependent upon smooth muscle tone. These peristaltic waves usually originate just oral to the pellet, and their apparent conduction velocity is generated by activation of descending inhibitory nerve pathways.