Repetitive electrical activity of the muscle membrane induced in chloride-free medium

Abstract

1. Superficial fibres of frog skeletal muscle were electrically stimulated in Ringer solution where the chloride content had been replaced by various weakly permeant anions. Changes of the membrane potential were recorded at three different time scales. The complex response was initiated by a volley of fast repetitive action potentials (10-20 ms cycle length) superimposed on the ascending phase of a transient depolarization to -35 mV. The transient depolarization was followed by a membrane potential oscillation (0.3-0.6 s cycle length). The parameters of the volley and membrane potential oscillation were not greatly affected by the substituent anion. 2. The transient depolarization was fully abolished by tetrodotoxin (3 mumol/L), but left unaffected by nifedipine (5 mumol/L), or by the replacement of extracellular Ca for Ni or Co. Tetraethylammonium (20-40 mmol/L) increased the duration and amplitude of the transient depolarization. The shape of transient depolarization was uniform in a given fibre, in spite of its marked variability under different experimental conditions. 3. Single outward current pulses applied in chloride-free solution containing tetraethylammonium (20-40 mmol/L) evoked prolonged depolarizations to positive membrane potentials accompanied by increases in the specific membrane conductance. This slow response, which was also frequently observed in the absence of TEA, was mediated by Ca ions, as it was insensitive to tetrodotoxin (3 mumol/L) but abolished by nifedipine (10 mumol/L). 4. Two populations of the muscle fibres were observed during the slow response. Some fibres repolarized completely, while others failed to produce complete repolarization but formed a plateau between -20 and -30 mV, lasting for several minutes. When the external K concentration was abruptly increased to 5 or 10 mmol/L during the plateau of the slow response, repolarization and increase in membrane conductance were observed. 5. In muscle fibres, having osmotically disrupted T-system, the duration of transient depolarization was in the range of minutes, in contrast to the range of seconds observed in intact fibres. The volley was preserved in glycerol treated fibres, however, the baseline of discharges was close to the resting potential and the rate of depolarization of the baseline was significantly less in glycerol treated than in intact fibres. 6. These results are consistent with the existence of a second stable membrane potential level in skeletal muscle between -40 and -30 mV. The depolarization and repolarization during the membrane potential oscillation and transient depolarization can be regarded as a partial or full transition, respectively, between these two stable membrane potential levels, possibly due to the conductance changes of the inward rectifier K channels.(ABSTRACT TRUNCATED AT 400 WORDS)