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

Abstract

The spontaneous electrical activities of circular muscle cells of the canine proximal colon were studied with intracellular micro-electrodes. All circular muscle cells exhibited slow waves at frequencies ranging between 2.8 and 7.0 cycles/min. The slow waves consisted of an upstroke phase followed by a plateau phase of variable duration (2-40 s). Many cells displayed a slow diastolic depolarization, or 'pre-potential' between slow waves. Slow waves spontaneously varied in duration and frequency in most preparations, creating distinctive slow wave patterns. Atropine, 2 X 10(-6) M, decreased the durations of slow waves in many preparations and often changed the pattern to a series of relatively uniform slow waves. A further reduction in mean slow wave duration was produced by additional treatment with tetrodotoxin, 10(-6) M. These results suggested that slow wave duration and pattern were affected by spontaneous discharge from both cholinergic and non-cholinergic excitatory nerves. Transmural nerve stimulation caused a short latency increase in slow wave duration (up to 38 s) that was abolished by atropine. In the presence of atropine, transmural stimulation evoked inhibitory junction potentials that reduced the amplitude and duration of the subsequent slow wave. The slow wave of reduced amplitude was followed by a slow wave of increased duration. The increase in duration of the slow wave did not appear to be related to the size of the preceding hyperpolarization, suggesting it was mediated by the release from non-cholinergic excitatory nerves. All responses to transmural stimulation were blocked by tetrodotoxin. Microejection of acetylcholine on to the muscle adjacent to the micro-electrode also produced an atropine-sensitive increase in slow wave duration. Tissues that had been stored in the cold overnight to reduce intrinsic neural activity exhibited regular slow waves of short duration. It is proposed that the basic myogenic pattern of spontaneous slow wave activity consists of regularly occurring slow waves of short duration (2-5 s). Intrinsic cholinergic and non-cholinergic excitatory nerves appear to modulate slow wave activity in vitro, producing distinctive slow wave patterns of variable instantaneous frequency and duration.