Effects of carbon dioxide and tetanus duration on relaxation of frog skeletal muscle

Abstract

Sartorius and semitendinosus muscles of the frog Rana temporaria (0 degrees C) were stimulated under isometric (fixed-end) conditions and force during stimulation and relaxation was recorded. Relaxation time was assessed by measuring the time from the last stimulus until force declined to 90% or 50% of its value at that time. The relaxation time increased linearly with concentration of CO2 in the Ringer's solution (pH 7.2), whereas, at constant CO2, relaxation was hardly affected by changes in extracellular HCO3- and pH. This is consistent with the view that CO2 enters the cells, but H+ and HCO3- do not, and that entry of CO2 causes intracellular acidification and slows relaxation. For tetani lasting between 0.5 and 5s, relaxation is slower the longer the tetanus; further increase in tetanus duration to 10 s has little additional effect. The presence of 3.3 mmol 1(-1) CO2 in the Ringer's solution has a small effect on relaxation after a brief tetanus, but greatly slows relaxation as tetanus duration increases. Experiments with paired tetani (conditioning and test) showed that relaxation from a test tetanus was slower if a conditioning tetanus was given. However, the size of this effect was independent of muscle length during the conditioning tetanus. After a conditioning tetanus, an interval of many minutes is required for the muscle to recover its ability to relax quickly from a test tetanus. The results indicate that changes in metabolite levels caused by contraction itself are not responsible for the slowing of relaxation. Possible mechanisms of the effects of CO2 on relaxation are discussed.

Molecular model of muscle contraction

“…‡ The increase in the ATP splitting rate with sliding velocity is also broadly compatible with the fact that muscle generates heat more rapidly the faster it shortens (8) (the Fenn effect). Note that at negative velocities, very little ATP is consumed, since few power-stroke cycles are completed; this is consistent with the observation that during slow stretching, cross-bridges can develop high tension without splitting ATP (26). Note also that peak efficiency is attained at a velocity that corresponds to the filaments sliding, on average, through displacement d during the time that a head is bound; in this way, the strain generated by the power stroke ‡ It should be noted, however, that filament compliance is not negligible (24,25), so the relation between stiffness and number of attached cross-bridges is not a direct one.…”

Effect of intracellular pH on force and heat production in isometric contraction of frog muscle fibres.

“…This ATPase activity is lowered by increased acidity in vitro (MacLennan, 1970), and in vivo it is probably this effect that causes the obvious slowing of relaxation produced by increasing CO2 concentration (for example Fig. 4, and Curtin, 1986b). This contrasts with the total ATP splitting, which, as we have just seen, is increased by increased acidity in the range pH 7-26-6-82.…”

“…Less force is produced under isometric conditions (Edman & Mattiazzi, 1981;Curtin, 1986 a, b) and during shortening (Renaud & Stevens, 1984;Curtin & Rawlinson, 1984). In addition, there is a reduction in the maximum velocity of shortening (Edman & Mattiazzi, 1981) and in the rate of relaxation (Curtin, 1986b). Are these changes accompanied by changes in the turnover of cross-bridges?…”

Fluo‐3 signals associated with potassium contractures in single amphibian muscle fibres.

“…During fatigue tension output is decreased and the relaxation time course is markedly prolonged, due to altered metabolic conditions, such as decreased pH and/or increased Mg2+ or phosphate (Edman & Mattiazzi, 1981;Curtin, 1986;Allen, Lee & Westerblad, 1991). However, we have shown that the twitch time course during the early stages of recovery from a K+ contracture is similar to that before the contracture.…”