The Role of Sodium Current in the Radial Spread of Contraction in Frog Muscle Fibers

Abstract

The membrane potential of isolated muscle fibers was controlled with a two-electrode voltage clamp, and the radial extent of contraction elicited by depolarizing pulses of increasing magnitude was observed microscopically. Depolarizations of the fiber surface only 1-2 mv greater than the contraction threshold produced shortening throughout the entire crosssection of the muscle fiber. The radial spread of contraction was less effective in fibers exposed to tetrodotoxin or to a bathing medium with a greatly reduced sodium concentration. The results provide evidence that depolarization of a muscle fiber produces an increase in sodium conductance in the T tubule membrane and that the resultant sodium current contributes to the spread of depolarization along the T system.Although it is generally accepted that the T system of twitch muscle fibers transmits the influence of surface depolarization radially, the mode of transmission within the T system has not been established. Huxley and Taylor (1958) found only a graded inward spread of contraction with increasing depolarization of local sites on the surface membrane, while the results of Gonzales-Serratos (1966) on the temperature dependence of the radial spread of activation were more compatible with active propagation within the T system. Recently Adrian, Costantin, and Peachey ' (1969) reported that the radial spread of contraction with controlled surface depolarizations was not entirely consistent with a passive electrotonic spread of depolarization along the T system; they suggested that delayed rectification, an increase in the potassium conductance with depolarization, might be present in the T tubules. The experiments of ACP were performed on fibers exposed to tetrodotoxin (TTX), so that the presence of a regenerative increase in sodium conductance within the T tubules of a normal muscle fiber could not be ruled out.

Circuit Models of the Passive Electrical Properties of Frog Skeletal Muscle Fibers

“…1 will show that this model is distinguished by the absence of a circuit element to represent the resistance of the solution in the lumen of the tubules. The lumped model then predicts that there should be no radial gradients of potential within the tubular system in disagreement with the straightforward interpretation of the experimental results of GonzAlezSerratos, 1971;Adrian, Costantin, and Peachey, 1969;Costantin, 1970;and b.…”

“…There are a number of theoretical papers which claim, however, that circumferential and radial potential gradients should exist and be significant in cylindrical muscle fibers (Eisenberg and Johnson, 1970;Barcilon et al, 1971;Peskoff et al, 1972; a review of the literature can be found in Peskoff and Eisenberg, 1973). There are some indirect indications of circumferential and radial potential gradients in the experiments of Adrian, Costantin, and Peachey (1969) and Costantin (1970) but there has been no direct experimental evidence concerning the existence of these effects, let alone their quantitative significance, and so we thought it worthwhile to seek such evidence. Impedance measurements were made by the techniques described by Valdiosera et al, 1974 a. Measurements were made at two different circumferential positions of the voltage microelectrode, the longitudinal position being constant, and the radial position being unknown.…”

Voltage—clamp analysis of the early current in frog skeletal muscle fibre using the double sucrose‐gap method

“…Besides, the delayed current in the skeletal muscle fibre is apparently also decreased in presence of tetrodotoxin. Such an effect is rather surprising; it might perhaps result from some regenerative activity in the tubule membrane as suggested by Costantin (1970) …”

Muscular contraction.

“…The electrical conduction in the transverse tubules has recently been shown to be a regenerative process (Costantin, 1970;Costantin & S. R. , similar to the longitudinal propagation along the surface membrane but with much lower safety factor (R. H. Adrian & Peachey, 1973), and this accounts for the remarkable speed with which the onset of shortening spreads inwards within each fibre (GonzalezSerratos, 1971). …”