The electrical properties of the circular smooth muscle layer from the North American opossum esophagus (body) were studied in vitro by microelectrode recording techniques, both at rest and during stimulation of intramural inhibitory nerves. All observations were made at 37 degrees C in an Abe-Tomita partitioned bath on muscle strips dissected 2 cm orad of the lower esophageal sphincter. At rest, the potential of the smooth muscle cell membrane was -49 +/- 4 mV (mean +/- SE); the length constant and the time constant were 2.0 +/- 0.6 mm and 120 +/- 16 ms, respectively. The inhibitory junction potential (IJP) elicited by stimulation of intramural nerves was followed by a "rebound" or "off" response, characterized by a membrane depolarization on which spikes were superimposed and concomitant mechanical activity of the preparation that usually caused dislocation of the recording microelectrode. The maximal IJP amplitude was 35 mV, and the response reversed at a membrane polarization to -90 mV, suggesting that the IJP was due to an increase of the permeability toward potassium ions. The invariability of the IJP latency at different distances from the stimulating electrodes (1.25-4 mm) suggests that the latency is largely due to diffusion of transmitter from nerve varicosities to postsynaptic receptor sites. Depending on the rate, prolonged stimulation caused fusion of IJP or a continuous hyperpolarization of the membrane. The hyperpolarization faded with time, but off responses were only observed after terminating stimulation. The passive electrical properties of the membrane are comparable with those of other gastrointestinal smooth muscles.(ABSTRACT TRUNCATED AT 250 WORDS)