Circular muscle lamellae of canine colon are electrically isolated functional units

Abstract

The circular muscle (CM) layer of canine colon consists of circumferentially oriented lamellae separated by connective tissue septa. These lamellae facilitate circumferential ring contractions. Communication between CM lamellae is necessary to generate coordinated, propulsive phasic contractions to create peristaltic movement. Potential roles of the submuscular network of interstitial cells of Cajal and branching smooth muscle cells (ICC-bSM), the myenteric interstitial cells of Cajal network (ICC-AP), and the longitudinal muscle (LM) layer in mediating communication between the CM lamellae were studied by simultaneously recording with three surface electrodes, using different types of muscle strip preparations. When the ICC-bSM network was intact, slow waves were observed to be entrained both along and across CM lamellae. In contrast, the CM layer devoid of the ICC-bSM network, the myenteric plexus, and the longitudinal muscle (CM preparation) was spontaneously quiescent. Spike-like action potentials, evoked in the CM preparations by Ba2+ (0.5 mM), were entrained within CM lamellae but were not coordinated between the CM lamellae. In the LM-CM preparations, in which the longitudinal muscle and the ICC-AP network were intact, the Ba(2+)-evoked action potentials were again not coordinated across septa but entrained within CM lamellae. In a step preparation, in which the ICC-bSM network was removed from part of the muscle strip, slow waves were observed to be entrained in areas with and without the ICC-bSM network when electrodes were positioned along septa. When electrodes were positioned across CM lamellae, synchronized slow wave activity was observed only in areas with the intact ICC-bSM network and quiescent activity was recorded in areas devoid of the ICC-bSM network. These results demonstrate that CM cells are electrically coupled within a CM lamella, but not between CM lamellae. The submuscular ICC-bSM network, but not longitudinal or circular muscle cells, nor the ICC-AP, mediates communication between CM lamellae.