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Clearance Of Extracellular K+ During Muscle Contraction—Roles Of Membrane Transport And Diffusion

Torben Clausen

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Excitation of muscle often leads to a net loss of cellular K+ and a rise in extracellular K+ ([ K+ ]o), which in turn inhibits excitability and contractility. It is important, therefore, to determine how this K+ is cleared by diffusion into the surroundings or by reaccumulation into the muscle cells. The inhibitory effects of the rise in [K+ ]o may be assessed from the time course of changes in tetanic force in isolated muscles where diffusional clearance of K+ is eliminated by removing the incubation medium and allowing the muscles to contract in air. Measurements of tetanic force, endurance, and force recovery showed that in rat soleus and extensor digitorum longus (EDL) muscles there was no significant difference between the performance of muscles contracting in buffer or in air for up to 8 min. Ouabain-induced inhibition of K+ clearance via the Na+,K+ pumps markedly reduced contractile endurance and force recovery in air. Incubation in buffer containing 10 mM K+ clearly inhibited force development and endurance, and these effects were considerably reduced by stimulating Na+,K+ pumps with the β2-agonist salbutamol. Following 30–60 s of continuous stimulation at 60 Hz, the amount of K+ released into the extracellular space was assessed from washout experiments. The release of intracellular K+ per pulse was fourfold larger in EDL than in soleus, and in the two muscles, the average [K+ ]o reached 52.4 and 26.0 mM, respectively, appreciably higher than previously detected. In conclusion, prevention of diffusion of K+ from the extracellular space of isolated working muscles causes only modest interference with contractile performance. The Na+,K+ pumps play a major role in the clearance of K+ and the maintenance of force. This new information is important for the evaluation of K+-induced inhibition in muscles, where diffusional clearance of K+ is reduced by tension development sufficient to suppress circulation.