Origin and propagation of electrical slow waves in circular muscle of canine proximal colon

Abstract

Experiments to determine the site of slow-wave origin and the mechanism of propagation were performed on muscles of the canine proximal colon. Cells along the submucosal border of the circular layer had resting membrane potentials (RMP) averaging -78 mV, and slow waves, 40 mV in amplitude. The RMP of cells through the thickness of the circular layer decreased exponentially with distance from the submucosal border, such that RMPs of circular cells at the myenteric border were only -43 mV. Slow waves decreased in amplitude through the thickness such that slow waves could not be detected adjacent to the myenteric border. When a thin strip of muscle along the submucosal border was removed, slow waves were not recorded from the bulk of the circular layer and could not be evoked by acetylcholine. Slow waves were still present in the excised strip. Experiments to determine the rate of slow-wave propagation were also performed. Two cells were impaled, one at the submucosal surface, and another at some distance through the circular layer. Slow waves occurred nearly simultaneously at both sites. What latency was observed could be explained on the basis of electrotonic conduction. The results support the hypothesis that in the canine proximal colon slow waves are generated at the extreme submucosal surface of the circular layer. The bulk of the circular layer does not possess either pacemaker or regenerative mechanisms, and slow waves propagate passively toward the myenteric border. The cable properties of the circular muscle syncytium furnish a barrier to invasion of the longitudinal layer by the slow wave event.

Inward rectifier potassium conductance regulates membrane potential of canine colonic smooth muscle

“…The expression of Kir2.1 was significantly higher in SCM preparations (which contained the ICC from which inward rectifier currents were measured) than in either ICM or MyCM preparations. Our study suggests that a significant portion of the membrane potential gradient across the thickness of the circular muscle layer (see Smith et al 1987) is due to the heterogeneous expression of Kir2.1 in colonic muscles. In the present study we reproduced the large depolarization caused by ouabain (see Burke et al 1988), although the effects of ouabain were significantly reduced after prior application of Ba¥.…”

“…Regional differences in expression of an inward rectifier conductance may contribute to the gradient in resting membrane potential within the circular muscle layer (Smith et al 1987). …”

Are interstitial cells of Cajal plurifunction cells in the gut?

“…The physical separation of the myenteric plexus in the stomach and the small intestine, or that of the submucosal plexus in the colon, abolishes or disorganizes the slow waves in the remaining circular smooth muscle cells (8,36,96,124,143,151,159). Taken together, the findings in these studies and those in the mutant animals suggest that the potential role of the ICC-MY in the stomach and the small intestine and of ICC-SM in the colon may be to stabilize the slow waves generated spontaneously in the circular muscle cells, rather than to pace them.…”

Properties of spontaneous contractions and their modulation by transmural nerve stimulation in circular smooth muscle isolated from the pacemaker area in the flexure region of the guinea-pig colon

“…However in the colon, rhythmic activity of smooth muscle is paced by ICC-SMP in the dog (Smith et al, 1987;Kobayashi et al, 1995) and guinea-pig (Kobayashi et al, 1996;Nahar et al, 1998), while it is carried out by ICC-MP in the rat (Plujà et al, 2001;Kato et al, 2009) and mouse (Yoneda et al, 2004). In the guinea-pig, a group of ICC-SMP with a dense distribution in the flexure region at the boundary between proximal and distal divisions of colon produces regular periodic activity of 10-12 cycle per min in the circular smooth muscle (Kobayashi et al, 1995;Nahar et al, 1996).…”