Co‐operation between neural and myogenic mechanisms in the control of distension‐induced peristalsis in the mouse small intestine

Abstract

Myogenic and neural control of intestinal transit were investigated in a model of distension‐induced peristalsis. A comparison was made between the electrical and mechanical activities and outflow of contents observed in control mice and in W/W v mice, which lack the interstitial cells of Cajal associated with Auerbach's plexus. Distension caused a periodic appearance of increased motor activity due to stimulation of enteric nerves in both control and W/W v mice. Excitation was primarily delivered by cholinergic nerves, whereas periodic inhibition was mediated by neuronal nitric oxide. In control mice, outflow was driven by propagating slow‐wave activity and was only in the aboral direction. Outflow only occurred when slow waves carried sufficient action potentials to cause phasic intraluminal pressure increases of ≥ 1 cmH2O through direct stimulation of the musculature or by distension‐induced neurally mediated activation. In W/W v mice, outflow was associated with propagating action potentials that occurred due to either neural stimulation or direct muscle stimulation. Action potential propagation and outflow occurred in both oral and aboral directions. In summary, in both control and W/W v mice, distension induced periodic motor activity through stimulation of the enteric nervous system. Intraluminal contents were not moved in front of such motor activity. Rather, within such periods of activity that occurred concurrently throughout an entire segment, pulsatile outflow was directed by individual propagating slow waves with superimposed action potentials in control tissue, and by propagating action potentials in W/W v mice, which lack interstitial cells of Cajal.

Are interstitial cells of Cajal plurifunction cells in the gut?

“…Others found that the small intestine of the intact W/W v mice and muscle strips in organ bath continue to generate slow waves and RPCs, but both are more irregular in frequency and smaller in amplitude than those in the wild-type mice (Figs. 4, C-F) (45,76,77,80,105). The slow waves and their associated contractions in the W/W v mice propagate over shorter distances than those in the wild-type mice.…”

“…The contraction that is solely due to the membrane depolarization by slow wave is called electromechanical coupling. Although these tiny contractions are recordable in in vitro preparations, they do not effectively constrict the lumen in the intact state, and, therefore, they have little or no effect on motility function (77). A good example of these tiny contractions is the quiescent state in the stomach and the small intestine during phase I of the migrating motor complex (MMC) cycle.…”

Quantitative analysis of peristalsis in the guinea‐pig small intestine using spatio‐temporal maps

“…This was developed further by Bayliss & Starling (1899) with the development of the 'enterograph' which allowed them to record, via a system of levers, movements of the gut wall at several sites simultaneously. Mechanical recordings at several sites along segments of gut have subsequently been made, both in vivo and in vitro, by many workers, allowing some analysis of propagating contractions (Costa & Furness, 1976;Schemann & Ehrlein, 1986;Huizinga et al 1998). An alternative strategy to document gut motility has been to use image analysis of whole segments of gut.…”

“…For example it will be possible to monitor the activity of significant lengths of intestine while at the same time recording spontaneous or physiologically evoked muscle electrical activity (Gonella, 1971;Tsuchiya, 1972;Yokoyama & North, 1983;Lammers et al 1993). It should also be possible to combine spatio-temporal maps with monitoring of intracellular Ca¥, intracellular recordings from neurons, multiple luminal manometry or strain gauges (Summers & Dusdieker, 1981;Bercik et al 1994;Huizinga et al 1998) and intraluminal flow (Bertuzzi et al 1978;Macagno & Christensen, 1980) to improve the understanding of the biomechanical basis of intestinal motor function. The major limitations of the technique relate to the need for high contrast images with well defined edges, which may limit its use in vivo.…”

Gastrointestinal effect of methanol extract ofRadix Aucklandiaeand selected active substances on the transit activity of rat isolated intestinal strips

“…Propulsive motility is termed peristalsis and subserved by a complex pattern of neural reflexes that aim to relax intestinal muscle downstream (descending inhibitory reflex) and contract the muscle upstream (ascending excitatory reflex) of the intestinal bolus. Intestinal transit is controlled by both neural and myogenic mechanisms (Huizinga et al, 1998). Several mediators and neurotransmitters govern these motor patterns.…”