Dynamics and Consequences of Potassium Shifts in Skeletal Muscle and Heart During Exercise

Abstract

Since it became clear that K⁺ shifts with exercise are extensive and can cause more than a doubling of the extracellular [K⁺] ([K⁺]_s) as reviewed here, it has been suggested that these shifts may cause fatigue through the effect on muscle excitability and action potentials (AP). The cause of the K⁺ shifts is a transient or long-lasting mismatch between outward repolarizing K⁺ currents and K⁺influx carried by the Na⁺-K⁺ pump. Several factors modify the effect of raised [K⁺]_sduring exercise on membrane potential (E_m) and force production. 1) Membrane conductance to K⁺is variable and controlled by various K⁺ channels. Low relative K⁺ conductance will reduce the contribution of [K⁺]_s to the E_m. In addition, high Cl⁻ conductance may stabilize theE_m during brief periods of large K⁺shifts. 2) The Na⁺-K⁺ pump contributes with a hyperpolarizing current. 3) Cell swelling accompanies muscle contractions especially in fast-twitch muscle, although little in the heart. This will contribute considerably to the lowering of intracellular [K⁺] ([K⁺]_c) and will attenuate the exercise-induced rise of intracellular [Na⁺] ([Na⁺]_c). 4) The rise of [Na⁺]_c is sufficient to activate the Na⁺-K⁺ pump to completely compensate increased K⁺ release in the heart, yet not in skeletal muscle. In skeletal muscle there is strong evidence for control of pump activity not only through hormones, but through a hitherto unidentified mechanism. 5) Ionic shifts within the skeletal muscle t tubules and in the heart in extracellular clefts may markedly affect excitation-contraction coupling. 6) Age and state of training together with nutritional state modify muscle K⁺content and the abundance of Na⁺-K⁺ pumps. We conclude that despite modifying factors coming into play during muscle activity, the K⁺ shifts with high-intensity exercise may contribute substantially to fatigue in skeletal muscle, whereas in the heart, except during ischemia, the K⁺ balance is controlled much more effectively.