Effect of repetitive stimulation on cell volume and its relationship to membrane potential in amphibian skeletal muscle

Abstract

The effect of electrical stimulation on cell volume, V (c), and its relationship to membrane potential, E (m), was investigated in Rana temporaria striated muscle. Confocal microscope xz-plane scanning and histology of plastic sections independently demonstrated significant and reversible increases in V (c) of 19.8+/-0.62% (n=3) and 27.1+/-8.62% (n=3), respectively, after a standard stimulation protocol. Microelectrode measurements demonstrated an accompanying membrane potential change, DeltaE (m), of +23.6+/-0.98 mV (n=3). The extent to which this DeltaE (m) might contribute to the observed changes in V (c) was explored in quiescent muscle exposed to variations in extracellular potassium concentration, [K(+)](e). E (m) and V (c) varied linearly with log [K(+)](e) and [K(+)](e), respectively, in the range 2.5-15 mM (R (2)=0.99 and 0.96), and these results were used to reconstruct an approximately linear relationship between V (c) and E (m) (DeltaV (c)=0.85E (m)+68.53; R (2)=0.99) and hence derive the DeltaV (c) expected from the DeltaE (m) during stimulation. This demonstrated that both the time course and magnitude of the increase and recovery of V (c) observed in active muscles could be reproduced by the corresponding [K(+)](e)-induced depolarisation in quiescent muscles, suggesting that the depolarisation associated with membrane activity makes a substantial contribution to the cell swelling during exercise. Furthermore, conditions of Cl(-) deprivation abolished the relationship between E (m) and V (c), supporting a mechanism in which the depolarisation of E (m) drives a passive redistribution of Cl(-) and hence cellular entry of Cl(-) and K(+) and an accompanying, osmotically driven, increase in V (c).