Propagation and neural regulation of calcium waves in longitudinal and circular muscle layers of guinea pig small intestine.

BACKGROUND & AIMS: The relative movements of longitudinal muscle (LM) and circular muscle (CM) and the role that nerves play in coordinating their activities has been a subject of controversy. We used fluorescent video imaging techniques to study the origin and propagation of excitability simultaneously in LM and CM of the small intestine.

METHODS

Opened segments of guinea pig ileum were loaded with the Ca(2+) indicator fluo-3. Mucosal reflexes were elicited by lightly depressing the mucosa with a sponge.

RESULTS

Spontaneous Ca(2+) waves occurred frequently in LM (1.2 s(-1)) and less frequently in CM (3.2 min(-1)). They originated from discrete pacing sites and propagated at rates 8-9 times faster parallel (LM, 87 mm/s; CM, 77 mm/s) compared with transverse to the long axis of muscle fibers. The presence of Ca(2+) waves in one muscle layer did not affect the origin, rate of conduction, or range of propagation in the other layer. The extent of propagation was limited by collisions with neighboring waves or recently excited regions. Simultaneous excitation of both muscle layers could be elicited by mucosal stimulation of either ascending or descending reflex pathways. Neural excitation resulted in an increase in the frequency of Ca(2+) waves and induction of new pacing sites without eliciting direct coupling between layers.

CONCLUSIONS

Localized, spontaneous Ca(2+) waves occur independently in both muscle layers, promoting mixing (pendular or segmental) movements, whereas activation of neural reflexes stimulates Ca(2+) waves synchronously in both layers, resulting in strong peristaltic or propulsive movements.