Time domain spectroscopy of the membrane capacitance in frog skeletal muscle.

Abstract

Dielectric spectra representing the frequency dependence of the complex permitivity at a range of depolarizations were obtained from voltage-clamped frog skeletal muscle membranes. This employed an analysis that derived the Fourier coefficients defining the capacitative transients to 10 mV steps as continuous functions of frequency, and so could examine closely the relevant frequencies at which non-linear components occurred. Non-linear capacitative components were identified through their appearance at lower frequencies than those of the linear components as obtained at the -85 mV control voltage, from spectra representing a logarithmic scale of frequencies. Permitivities from small depolarizing steps between about -75 and -50 mV gave single q beta dielectric loss peaks; the real permitivities declined monotonically with increasing frequency. Simple arc loci were obtained in the complex plane. With further depolarization, an additional q gamma loss peak at low frequencies and a resonant frequency in the real spectra occurred over a narrow voltage range around -45 mV. The complex loci then showed features implying an increased movement of charge not explicable through the simple effect of an electric field on a dielectric species. Spectra from small hyperpolarizing steps possessed only single dielectric loss peaks and real permitivities that declined monotonically with increasing frequency. However, in the complex plane, the loss tangents at the higher frequencies implied a population of two or more dielectric relaxations. The potential dependence of the frequency at maximum dielectric loss obtained from depolarizing steps showed a discontinuity at the onset of q gamma. In contrast, in hyperpolarizing responses, this dependence was smooth. The q beta relaxations obtained after q gamma was abolished by 1 mM-tetracaine gave dielectric spectra that were similar whether to depolarizing or hyperpolarizing potential steps. They gave single dielectric loss peaks and semicircular complex plane loci. The singularities in the dielectric spectra thus result from the q gamma charge movement component. They may reflect co-operative mechanisms that might also produce its steep voltage dependence and kinetics, and consequently those of the physiological processes it may control. These are discussed in terms of the mechanisms expected in allosteric proteins.

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