Quantitative analysis of intestinal motor patterns: spatiotemporal organization of nonneural pacemaker sites in the...

Intestinal contractions are triggered by electric activity of pacemaker cells within the smooth muscle. However, the precise spatial organization of the pacemaker system is unknown. We directly assessed the spatiotemporal organization of pacemakers by video image analysis combined with manometry and electromyography.

Isolated segments of rat ileum were perfused arterially with oxygenated fluorocarbon solution and luminally with saline. Luminal end pressures, extracellular electric activity, and images of the intestine were recorded simultaneously. Tetrodotoxin, N(G)-nitro-L-arginine methyl ester (L-NAME), L-arginine, and eserine were administered arterially.

Myogenic contractions originated in discrete areas (dominant pacemakers) and propagated faster in aboral than in oral direction. Dominant pacemakers were distributed along the intestine at regular intervals. The preparations were mostly driven by 1 pacemaker at the time, but 2 or 3 pacemakers with different frequencies could be active simultaneously. Tetrodotoxin decreased aboral propagation velocity and revealed multiple regularly spaced pacemaker areas. Eserine increased, whereas L-arginine decreased, their frequency. After L-NAME, pacemaker activity increased and isolated pacemakers with higher frequency appeared.

Nonneural pacemakers in rat ileum are functionally organized not as a continuous system but show a segmental arrangement, spatially and temporally modulated by neural activity.