Pflügers Archiv

, Volume 406, Issue 5, pp 458–463 | Cite as

Potassium and sodium shifts during in vitro isometric muscle contraction, and the time course of the ion-gradient recovery

  • Carsten Juel
Excitable Tissues and Central Nervous Physiology

Abstract

Intracellular potassium ([K+]i), interstitial potassium ([K+]inter), intracellular sodium ([Na+]i), and resting membrane potential (RMP) were measured before and after repetitive stimulation of mouse soleus and EDL (extensor digitorum longus) muscles. At rest, RMP was −69.8 mV for soleus and −74.9 mV for EDL (37°C). [K+]i was 168 mM and 182 mM, respectively. In soleus, free [Na+]i was 12.7 mM. After repetitive stimulation (960 stimuli) RMP had decreased by 11.9 mV for soleus and by 18.2 mV for EDL. [K+]i was reduced by 32 mM and 48 mM, respectively, whereas [K+]inter was doubled. In soleus [Na+]i had increased by 10.6 mM, demonstrating that the [K+]i-decrease is three times higher than the [Na+]i-increase. It is concluded that this difference reflects different activity induced movements of Na and K, and that the difference is not due to the Na/K pumping ratio. The possible involvement of the potassium loss in muscle fatigue is discussed. After stimulation RMP recovered with a time constant of 0.9 min for soleus and 1.5 min for EDL. Within the first minutes after stimulation the intracellular potassium concentration increased by 20.4 mM/min for soleus and 21.7 mM/min for EDL. Free [Na+]i decreased with less than 10 mM/min. The mechanisms underlying the different rate of changes are discussed.

Key words

Na+- and K+-sensitive microelectrodes Repetitive stimulation Ion-gradients Recovery 

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References

  1. Aickin CC, Thomas RC (1977a) Micro-electrode measurements of the intracellular pH and buffering power of mouse soleus muscle fibres. J Physiol (Lond) 267:791–810Google Scholar
  2. Aickin CC, Thomas RC (1977b) An investigation of the ionic mechanism of intracellular pH regulation in mouse soleus muscle fibres. J Physiol (Lond) 273:295–316Google Scholar
  3. Akaike N (1976) Intracellular ion concentration and electrical activity in potassium-depleted mammalian soleus muscle fibers. Pflügers Arch 362:15–20Google Scholar
  4. Ashley CC, Ridgway EB (1979) On the relationships between membrane potential, calcium transient and tension in single barnacle muscle fibres. J Physiol (Lond) 209:105–130Google Scholar
  5. Campion DS (1974) Resting membrane potential and ionic distribution in fast- and slow-twitch mammalian muscle. J Clint Invest 54:514–518Google Scholar
  6. Donaldson PJ, Leader JP (1984) Intracellular ionic activities in the EDL muscle of the mouse. Pflügers Arch 400:166–170Google Scholar
  7. Fink R, Luttgau HC (1976) An evaluation of the membrane constants and the potassium conductance in metabolically exhausted muscle fibres. J Physiol (Lond) 263:215–238Google Scholar
  8. Fink R, Hase S, Luttgau HC, Wettwer E (1983) The effect of cellular energy reserves and internal calcium ion on the potassium conductance in skeletal muscle of the frog. J Physiol 336:211–228Google Scholar
  9. Gebert G (1972) Messung der K- und Na-Aktivität mit Mikro-Glaselektroden im Extracellularraum des Kaninchenskeletmuskels bei Muskelarbeit. Pflügers Arch 331:204–214Google Scholar
  10. Hanson J (1974) The effect of repetitive stimulation on the action potential and the twitch of rat muscle. Acta Physiol Scand 90:387–400Google Scholar
  11. Harris JB, Luff AR (1970) The resting membrane potential of fast and slow skeletal muscle fibres in the developing mouse. Comp Biochem Physiol 33:923–931Google Scholar
  12. Hinke JAM, Caille JP, Gayton DC (1973) Distribution and state of monovalent ions in skeletal muscle based on ion electrode, isotope, and diffusion analyses. Ann NY Acad Sci 204:274–296Google Scholar
  13. Hirche H, Schumacher E, Hagemann H (1980) Extracellular K+ concentration and K+ balance of the gastrocnemius muscle of the dog during exercise. Pflügers Arch 387:231–237Google Scholar
  14. Hnik K, Holas M, Krekule I, Kriz N, Mejsnar J, Smiesko V, Ujec E, Vyskocil F (1976) Work-induced potassium changes in skeletal muscle and effluent venous blood assessed by liquid ion-exchanger microelectrodes. Pflügers Arch 362:84–95Google Scholar
  15. Holmberg E, Waldeck B (1980) On the possible role of potassium ions in the action of terbutaline on skeletal muscle contraction. Acta Pharmacol Toxicol 46:141–149Google Scholar
  16. Juel C (1985) Intracellular pH recovery after muscle activity. Clin Physiol 5 (suppl 4):142Google Scholar
  17. Juel C, Sjøgaard G (1984) Changes in potassium distribution and membrane potential during in vitro isometric muscle contraction. Acta Physiol Scand 121:P6Google Scholar
  18. Keynes RD, Lewis PR (1951) The sodium and potassium content of cephalopod nerve fibres. J Physiol 114:151–182Google Scholar
  19. Latorre R, Wergara C, Hidalgo C (1982) Reconstitution in planar lipid bilayers of a Ca2+-dependent K+ channel from transverse tubule membranes isolated from rabbit skeletal muscle. Proc Natl Acad Sci, USA 79:805–809Google Scholar
  20. Lee CO, Armstrong WM (1974) State and distribution of potassium and sodium ions in frog skeletal muscle. J Membr Biol 15:331–362Google Scholar
  21. Locke S, Solomon HC (1967) Relation of resting potential of rat gastrocnemius and soleus muscles to innervation, activity, and the Na−K pump. Z Exp Zool 166:377–386Google Scholar
  22. Pallotta BS, Maglely KL, Barrett JN (1981) Single channel recordings of Ca2+-activated K+ current in rat muscle cell culture. Nature 293:471–474Google Scholar
  23. Romey S, Lazdunski M (1984) The coexistence in rat muscle cells of two distinct classes of Ca2+-dependent K+ channels with different pharmacological properties and different physiological function. Biochim Biophys Res Commun 118:669–674Google Scholar
  24. Sahlin K, Alvestrand A, Brandt R, Hultman E (1978) Intracellular pH and bicarbonate concentration in human muscle during recovery from exercise. J Appl Physiol 45:475–480Google Scholar
  25. Sjøgaard G (1983) Electrolytes in slow and fast muscle fibers of humans at rest and with dynamic exercise. Am J Physiol 245:R25-R31Google Scholar
  26. Sjøgaard G, Adams RP, Saltin B (1985) Water and ion shifts in skeletal muscle of humans with intense dynamic knee extension. Am J Physiol 248:R190-R196Google Scholar
  27. Steiner RA, Oehme M, Ammann D, Simon W (1979) Neutral carrier sodium ion-selective microelectrode for intracellular studies. Analyt Chem 51:351–353Google Scholar
  28. Sreter FA (1963) Cell water, sodium, and potassium in stimulated red and white mammalian muscles. Am J Physiol 205:1295–1298Google Scholar
  29. Thomas RC (1978) Ion-sensitive intracellular microelectrodes. Academic Press LondonGoogle Scholar
  30. Tibes U, Haberkorn-Butendeich E, Hammersen F (1977) Effect of contraction on lymphatic, venous and tissue electrolytes and metabolites in rabbit skeletal muscle. Pflügers Arch 368:195–202Google Scholar
  31. Vaughan-Jones, RD (1982) Chloride activity and its control in skeletal and cardiac muscle. Phil Trans R Soc (Lond) B299:537–548Google Scholar
  32. Vyskocil F, Hnik P, Rehfeldt H, Vejsada R, Ujrc E (1983) The measurement of K3+ concentration changes in human muscles during volitional contractions. Pflügers Arch 399:235–237Google Scholar

Copyright information

© Springer-Verlag 1986

Authors and Affiliations

  • Carsten Juel
    • 1
  1. 1.Zoophysiological Lab. BAugust Krogh InstituteCopenhagen ØDenmark

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