Determinants of surface membrane and transverse-tubular excitability in skeletal muscle: implications for high-intensity exercise

Abstract

AbstractThe fatigue of high-intensity exercise is now believed to reside primarily within the excitation–contraction coupling processes associated with the plasma membrane of skeletal muscle (sarcolemm) and calcium-mediated events leading to myofilament sliding. This paper summarizes recent developments and advances in the identification of factors that contribute to changes in sarcolemmal excitability of mammalian skeletal muscle as a consequence of high-intensity exercise. There is an increasing recognition of the probable role that is played by the transverse tubular system (T-system), a system that comprisesc. 80% of the total sarcolemmal surface capable of ion exchange. Furthermore, the fluid within the T-system has limited access to interstitial fluid bathing myofibres; hence, T-system fluid is probably markedly different from interstitial fluid during high-intensity exercise. Mechanically skinned fibre preparation is providing many new insights into functions of the surface membrane and T-system in fatigue. A scenario is developed whereby accumulation of potassium within the T-system ([K+]o) contributes to reduced membrane excitability, as well as lowering of T-system sodium and chloride, concomitant with loss of intracellular potassium ([K+]i) and accumulation of intracellular sodium ([Na+]) and chloride ([Cl−]). Lowering the [Na+]o/[Na+]iratio and raising myoplasmic [Na+]ihave been shown to decrease membrane excitability and impair action potential propagation. Maintained high [Cl−]omay also have a protective effect in maintaining membrane excitability, and this effect appears to be very pronounced in the presence of raised [K+]o. In contrast to dogma associating high [H+] to fatigue, recent studies have also shown that induced acidosis that results in increased [H+]oand [H+]irestores force production in muscles and skinned fibres fatigued by intermittent tetanic stimulation. This effect may be due to a decrease in surface membrane Cl−permeability that serves to restore membrane excitability. During high-intensity exercise, simultaneous changes in trans-membrane ion concentrations and membrane ion conductances may serve to reduce impairment of membrane excitability that provides for a maintained, though reduced, contractile function.