Neurogenic slow depolarizations and rapid oscillations in the membrane potential of circular muscle of mouse colon

Abstract

1. Intracellular microelectrodes have been used to record the electrical activity of smooth muscle cells of the circular layer from full length strips of mouse colon in vitro. The membrane potential was unstable and showed slow depolarizations (mean amplitude, 10.9 mV; mean frequency, 0.008 Hz; mean duration, 56.4 s). 2. A variable number (mean fifty-six) of rapid oscillations in membrane potential (mean amplitude, 10.2 mV) with a frequency of approximately 2 Hz and a duration of approximately 400 ms were superimposed on each slow depolarization. Occasionally, action potentials arose from the rapid oscillations. The action potentials, but neither the slow depolarizations nor the rapid oscillations, were abolished by 1.0 microM-nifedipine. 3. The majority of the slow depolarizations and the associated rapid oscillations migrated aborally along the colon at a velocity of between 0.5 and 1.5 mm s-1; in the distal colon the slow depolarization was often preceded by a small hyperpolarization. 4. During the rising and plateau phase of the slow depolarization the amplitude of electronic potentials was decreased. Hyperpolarization induced by passing current during the slow depolarization increased the amplitude of the rapid oscillations. 5. Transmural electrical stimulation (single pulses) in the presence of nifedipine evoked (1 mm anal to the stimulating electrodes) an inhibitory junction potential which was sometimes preceded by an excitatory junction potential. The amplitude, of the evoked inhibitory junction potential was decreased during the rising and plateau phase of the slow depolarization. 6. The slow depolarization and the rapid oscillations were abolished by hexamethonium (500 microM), morphine (1-10 microM) and tetrodotoxin (3.1 microM). Atropine (3.5 microM) abolished the rapid oscillations and reduced the amplitude of the slow depolarization. 7. Atropine (3.5 microM) and morphine (10 microM) abolished the evoked excitatory junction potential whilst tetrodotoxin (3.1 microM) abolished both the excitatory and the inhibitory junction potential. 8. It is suggested that the migrating depolarization and accompanying oscillations, which are neurogenic in origin, represent the electrical correlate in the circular muscle layer of the migrating colonic motor complex which has been associated with the propulsion of faecal pellets along the colon.