Electrical correlates of peristaltic and nonperistaltic contractions in the opossum smooth muscle esophagus

Abstract

The electrical correlates of peristaltic and nonperistaltic esophageal contractions were characterized in anesthetized opossums using simultaneous suction electrode and intraluminal pressure recordings from sites 1 and 5 cm above the lower esophageal sphincter. Transient midesophageal balloon distention produced peristaltic contractions with faster propagation velocity than swallow-induced peristalsis. This was associated with prompt circular smooth muscle hyperpolarization at both sites, then depolarization, spike burst, and esophageal contraction. At the 5-cm site hyperpolarization was followed by rapid depolarization, whereas at the 1-cm site there was a much slower rate of depolarization after the initial hyperpolarization. Thus the longer latency to contraction at the 1-cm site correlated with the timing of the depolarization phase and not with the duration of the initial hyperpolarization. With prolonged balloon distention the inflation-related membrane hyperpolarization was followed by either partial or complete repolarization during sustained distention. Upon balloon deflation there was rapid membrane depolarization and spike burst at both sites such that the resultant contractions were usually nonperistaltic. In some instances balloon distention evoked contractions of slow peristaltic velocity. These correlated with membrane potential oscillations at the 1-cm site, with threshold depolarization being reached at the second depolarization in the hyperpolarization-depolarization sequences that followed balloon deflation. A similar pattern was seen with swallow-induced peristalsis. These studies demonstrate that differences in timing of the depolarization that follows initial hyperpolarization, and not differences in the duration of the initial hyperpolarization, are important in the genesis of peristaltic esophageal contractions.