Linear electrical properties of striated muscle fibres observed with intracellular electrodes

Abstract

The linear electrical properties of muscle fibres have been examined using intracellular electrodes for a. c. measurements and analyzing observations on the basis of cable theory. The measurements have covered the frequency range 1 c/s to 10 kc/s. Comparison of the theory for the circular cylindrical fibre with that for the ideal, one-dimensional cable indicates that, under the conditions of the experiments, no serious error would be introduced in the analysis by the geometrical idealization. The impedance locus for frog sartorius and crayfish limb muscle fibres deviates over a wide range of frequencies from that expected for a simple model in which the current path between the inside and the outside of the fibre consists only of a resistance and a capacitance in parallel. A good fit of the experimental results on frog fibres is obtained if the inside-outside admittance is considered to contain, in addition to the parallel elements R m = 3100 Ωcm 2 and C m = 2.6 μF/cm 2 , another path composed of a resistance R e = 330 Ωcm 2 in series with a capacitance C e = 4.1 μF/cm 2 , all referred to unit area of fibre surface. The impedance behaviour of crayfish fibres can be described by a similar model, the corresponding values being R m = 680 Ωcm 2 , C m = 3.9 μF/cm 2 , R e = 35 Ωcm 2 , C e = 17 μF/cm 2 . The response of frog fibres to a step-function current (with the points of voltage recording and current application close together) has been analyzed in terms of the above two-time constant model, and it is shown that neglecting the series resistance would have an appreciable effect on the agreement between theory and experiment only at times less than the halftime of rise of the response. The elements R m and C m are presumed to represent properties of the surface membrane of the fibre. R e and C e are thought to arise not at the surface, but to be indicative of a separate current path from the myoplasm through an intracellular system of channels to the exterior. In the case of crayfish fibres, it is possible that R e (when referred to unit volume) would be a measure of the resistivity of the interior of the channels, and C e the capacitance across the walls of the channels. In the case of frog fibres, it is suggested that the elements R e , C e arise from the properties of adjacent membranes of the triads in the sarcoplasmic reticulum . The possibility is considered that the potential difference across the capacitance C e may control the initiation of contraction.

Elemental distribution in striated muscle and the effects of hypertonicity: Electron probe analysis of cryo sections

“…The apparent correspondence between the size of this kinetically defined compartment and the size of the SR (70,74) led to suggestions (46,79) that the SR is in ionic communication with the extracellular space. This hypothesis is not in agreement with electrophysiological measurements (49) including measurements of membrane capacitance (28,33,36,50), but received support from studies showing the swelling of the SR in muscles fixed after incubation in hypertonic solutions (15,16,53). Therefore, we also examined cryo sections of muscles treated with hypertonic solutions for evidence of compartmentalized extracellular solutes.…”

A Comparison of the Fine Structures of Frog Slow and Twitch Muscle Fibres

“…The value obtained for the membrane capacitance of twitch fibres when measured with internal electrodes is high (5 to 8 #f/cm ~, Fatt and Katz, 1951) compared with squid axon (1 /zf/cm 2, Hodgkin, Huxley and Katz, 1952), for example. Part of this capacitance is thought to arise in the walls of the T system (Falk and Fatt, 1964) whose area may be an estimated 5 to 9 times the fibre surface area. In the slow fibres, on the other hand, the contribution of the walls of the thin tubules to the total surface area is much less, mainly because the fibrils in the slow fibres are much larger.…”

Depolarization of the Internal Membrane System in the Activation of Frog Skeletal Muscle

“…Although an appreciable conductance between the SR and T system does not appear to be present in the intact fiber (Falk and Fatt, 1964), Peachey (1965) has stressed the anatomical similarity of these junctions to the low resistance junctions between epithelial cells (Wiener, Spiro, and Loewenstein, 1964), and the possibility must be considered that, under appropriate conditions, the conductance of these junctions might increase appreciably.…”