Electrical activities of the muscle layers of the canine colon.

Abstract

SUMMARY1. The spontaneous electrical and mechanical activities of the circular and longitudinal muscle layers of the canine colon were studied.2. The smooth muscle cells of the circular muscle layer exhibited regular, omnipresent myogenic slow-wave activity at a frequency ranging from 4 to 7 c/min. With intracellular micro-electrodes, the slow-wave amplitude was 21-38 mV and its duration 3-6 sec. The 'resting' membrane potential was -60 to -76 mV. Some slow waves had superimposed spike bursts on their peak depolarizations and only these were associated with phasic contractions. It is concluded that they serve a pace-maker function similar to their counterpart in the small intestine.3. The longitudinal muscle layer exhibited periods ofelectrical activity alternating with periods ofelectrical quiescence. During the activity periods electrical oscillations occurred at a frequency of c/min with spikes on top of them. Each electrical activity period was associated with a prolonged 'tonic' contraction. The duration of these periods was 30-120 sec and their frequency 0A4-1 1 period/min. This activity is similar to that recorded from the longitudinal muscle of the guinea-pig caecum despite the anatomical differences.4. The electrical activity periods of the longitudinal muscle appeared to require an excitatory input (stretch and/or acetylcholine release). Provided the strips were not excessively stretched, atropine abolished all electrical and motor activity.Stretching prolonged the electrical activity periods until they eventually fused together and the muscle developed maintained tone.5. Simultaneously recording from both layers showed that, although electrotonic spread between the two layers is probably insignificant, the activity of the two layers was co-ordinated. Only those slow waves of the circular layer that occurred during the electrical activity periods of the longitudinal layer had superimposed spikes. It is suggested that this co-ordination may indicate that the two muscle layers may be commanded by a common input from periodically active, cholinergic intramural neurones.It is proposed that the complex patterns of colonic electrical and motor activities may be explained as consisting of two major components: one arising from the longitudinal (long spike bursts, high-frequency oscillations and tonic contractions) and the other from the circular layer (slow waves, short spike and phasic contractions).T. Y. EL-SHARKA WY 7. Simultaneous electrical records from the two muscle layers and the mucosa failed to show a consistent relationship between the mucosal record and the activity ofeither layer. Caution should be exercised in the interpretation of intraluminally derived electrical recordings.

Enteric neural regulation of slow waves in circular muscle of the canine proximal colon.

“…In contrast to the slow waves in the small intestine and stomach, which appear to be generated within or near the longitudinal muscle and propagate into the circular muscle layer (Bortoff, 1965;Kobayashi, Nagai & Prosser, 1966; Connor, Prosser & Weems, 1974;Connor, Kreulen, Prosser & Weigel, 1977; Bauer, Publicover & Sanders, 1985), slow waves of colonic circular muscle appear to be generated in the circular layer (Christensen et al 1969;Caprilli & Onori, 1972;El-Sharkawy, 1983;Huizinga et al 1983) adjacent to the submucosal border (Caprilli & Onori, 1972;Chambers et al 1984). Unlike the small bowel and stomach, the longitudinal and circular muscles of the colon exhibit different electrical activities (Christensen et al 1969;El-Sharkawy, 1983;Huizinga et al 1983). Circular muscle generates slow wave activity as described above, whereas longitudinal muscles of the dog and pig colon generate pre-potentials and action potentials that are not associated with slow waves but appear to be dependent on external stimuli such as stretch or acetylcholine (El-Sharkawy, 1983;Huizinga et al 1983).…”

“…Previous studies have shown that canine, feline, and porcine colonic circular smooth muscle cells exhibit rhythmic, myogenic depolarizations and repolarizations of the membrane potential or 'slow waves' (Christensen, Caprilli & Lund, 1969;El-Sharkawy, 1983;Huizinga, Diamant & El-Sharkawy, 1983;Chambers, Kingma & Bowes, 1984). In contrast to the slow waves in the small intestine and stomach, which appear to be generated within or near the longitudinal muscle and propagate into the circular muscle layer (Bortoff, 1965;Kobayashi, Nagai & Prosser, 1966; Connor, Prosser & Weems, 1974;Connor, Kreulen, Prosser & Weigel, 1977; Bauer, Publicover & Sanders, 1985), slow waves of colonic circular muscle appear to be generated in the circular layer (Christensen et al 1969;Caprilli & Onori, 1972;El-Sharkawy, 1983;Huizinga et al 1983) adjacent to the submucosal border (Caprilli & Onori, 1972;Chambers et al 1984).…”

“…Unlike the small bowel and stomach, the longitudinal and circular muscles of the colon exhibit different electrical activities (Christensen et al 1969;El-Sharkawy, 1983;Huizinga et al 1983). Circular muscle generates slow wave activity as described above, whereas longitudinal muscles of the dog and pig colon generate pre-potentials and action potentials that are not associated with slow waves but appear to be dependent on external stimuli such as stretch or acetylcholine (El-Sharkawy, 1983;Huizinga et al 1983). Christensen et al (1969) reported that the duration of spontaneous slow waves of the circular muscle of the cat colon in vitro was variable (3-19 s).…”

Neurogenic slow depolarizations and rapid oscillations in the membrane potential of circular muscle of mouse colon.

“…Between species the frequency of slow waves shows some variation; for example in the dog the frequency is about 5 cycles min-' (El-Sharkawy, 1983;Smith et al 1987 a, b) whereas in the pig the frequency is 0-5-3 5 cycles min-' (Huizinga et al 1983. Action potentials may or may not accompany the slow waves.…”

“…In colonic longitudinal muscle of several species including the guinea-pig, dog, pig and human, the.application of stretch appears to promote the onset of membrane potential oscillations. The onset of oscillatory activity appears to be controlled by both myogenic and neurogenic mechanisms (Biilbring, 1955;Gillespie, 1962;El-Sharkawy, 1983;Huizinga, Diamant & El-Sharkawy, 1983;Huizinga, Stern, Chow, Diamant & El-Sharkawy, 1985;Huizinga, Chow, Diamant & El-Sharkawy, 1987;Smith et al 1987 a).…”