Rhythmic membrane potential changes in hamster parasympathetic neurons.

Two types of rhythmic membrane potentials in hamster submandibular neurons: (i) slow oscillations of membrane potential (SOMP); and (ii) spontaneous or caffeine-induced rhythmic hyperpolarizing potentials (C-HPs), have been analyzed. SOMPs occurred spontaneously, roughly in sinusoidal forms, between the subthreshold range and the potassium equilibrium potential (EK, approximately -85 mV). The average amplitude of SOMPs from crest to trough was 12 mV with an average crest to crest interval of 6 min. The largest amplitude of SOMPs was seen when their median membrane potentials were between -65 and -70 mV; values outside this range attenuated the amplitude of SOMPs. SOMPs were hardly discernible at or near EK. The membrane resistance was, in general, higher at the crest than at the trough. In eserine-treated preparations, SOMPs of varying durations following postsynaptic potentials were triggered by preganglionic repetitive stimulation. Reduction of extracellular K+ concentration increased the amplitude of SOMP without changing its frequency. This effect was noted at times before K+-free induced membrane depolarization occurred. The amplitude of the SOMP decreased in Ca2+-free saline with concomitant depolarization; conversely, in saline in which the Ca2+ concentration was doubled the membrane potential (Em) was found to be again stable near the EK level. A transient hyperpolarization occurred following intracellular Ca2+ injection when the Em of the preinjected state was between -45 and -60 mV. Among K+-conductance (GK) blockers (TEA, 3- and 4-aminopyridine, Cs+ and Ba2+) examined, only Ba2+ at 5 mM reduced both amplitude and frequency of C-HPs significantly. All Ca2+-conductance (GCa) blockers (Co2+ and Mn2+ at 5 mM, Cd2+ and La3+ at 1 mM, and D-600 at 0.4 mg/ml) prevented synaptic transmission and abolished spike-induced late hyperpolarizing afterpotential. C-HPs were nearly abolished by these agents in 4 mM Ca2+-containing saline. Mitochondrial inhibitors (DNP, CCCP, KCN, NaN3) in a concentration range between 10(-4) M and 10(-5) M, hyperpolarized the membrane before depolarizing and abolishing C-HPs. However, the plasma membrane Na+-pump inhibitor ouabain, at concentrations up to 5 X 10(-4) M, did not affect C-HPs during 1 h perfusion in the majority of neurons; no membrane hyperpolarization was induced, although a gradual depolarization did occur. Both ruthenium red (5 mM) and quinine (5 X 10(-4) M) abolished C-HPs. It is assumed that the two above types of membrane potential changes are generated by the Ca2+-activated GK increase, which, in turn, is under the control of mitochondrial Ca2+ regulatory activity.