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Sports Medicine

, Volume 13, Issue 2, pp 134–145 | Cite as

The Roles of Ionic Processes in Muscular Fatigue During Intense Exercise

  • Michael J. McKenna
Issues in Fatigue in Sport and Exercise

Summary

Muscular fatigue is manifested by a decline in force- or power-generating capacity and may be prominent in both submaximal and maximal contractions. Disturbances in muscle electrolytes play an important role in the development of muscular fatigue. Intense muscular contraction is accompanied by an increased muscle water content, distributed in both intracellular and extra-cellular spaces. This water influx will modify ionic changes in both compartments. Changes in muscle intracellular electrolyte concentrations with intense contraction may be summarised as including decreases in potassium (6 to 20%) and in creatine phosphate (up to 70 to 100%) and increases in lactate (more than 10-fold), sodium (2-fold) and small, variable increases in chloride. The net result of these intracellular ionic concentration changes with exercise will be a reduction in the intracellular strong ion difference, with a consequent marked rise in intracellular hydrogen ion concentration. This intracellular acidosis has been linked with fatigue via impairment of regulatory and contractile protein function, calcium regulation and metabolism. Potassium efflux from the contracting muscle cell dramatically decreases the intracellular to extracellular potassium ratio, leading to depolarisation of sarcolemmal and t-tubular membranes. Surprisingly little research has investigated the effects of intense exercise training on electrolyte regulation and fatigue. Intense sprint training in man attenuates muscular fatigue during short term maximal exercise. This is accompanied by improved potassium homeostasis and possibly, improved regulation of muscular acidosis, both factors which may reduce muscular fatigue.

Keywords

Apply Physiology Intense Exercise Muscle Compound Action Potential Muscular Fatigue Single Muscle Fibre 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Adrian RH. The effect of internal and external potassium concentrations on the membrane potential of frog muscle. Journal of Physiology 133: 631–658, 1956PubMedGoogle Scholar
  2. Adrian RH, Peachey LD. Reconstruction of the action potential of frog sartorius muscle. Journal of Physiology 235: 103–131, 1973PubMedGoogle Scholar
  3. Ahlborg B, Bergstrom J, Ekelund L, Hultman E. Muscle glycogen and muscle electrolytes during prolonged physical exercise. Acta Physiologica Scandinavica 70: 129–142, 1967CrossRefGoogle Scholar
  4. Aickin CC, Thomas RC. An investigation of the ionic mechanism of intracellular pH regulation in mouse soleus muscle fibres. Journal of Physiology 273: 295–316, 1977PubMedGoogle Scholar
  5. Allen DG, Lee JA, Westerblad H. Intracellular calcium and tension during fatigue in isolated single muscle fibres from Xenopus Laevis. Journal of Physiology 415: 433–458, 1989PubMedGoogle Scholar
  6. Ashley GC, Ridgway EB. On the relationships between membrane potential, calcium transient and tension in single barnacle muscle fibres. Journal of Physiology 209: 105–130, 1990Google Scholar
  7. Bang O. The lactate content of the blood during and after muscular exercise in man. Skandinavian Archives of Physiology (Suppl. 10): 51–81, 1936CrossRefGoogle Scholar
  8. Bellemare F, Garzaniti N. Failure of neuromuscular propagation during human maximal voluntary contraction. Journal of Applied Physiology 64, 1084–1093, 1988PubMedGoogle Scholar
  9. Bergstrom J, Guarniera G, Hultman E. Carbohydrate metabolism and electrolyte changes in human muscle tissue during heavy work. Journal of Applied Physiology 30: 122–125, 1971PubMedGoogle Scholar
  10. Bigland-Ritchie B. EMG and fatigue of human voluntary and stimulated contractions. In Human muscle fatigue: physiological mechanisms, pp. 130–156, Pitman Medical, London (Ciba Foundation symposium 82), 1981Google Scholar
  11. Byrd SK, Bode AK, Klug GA. Effects of exercise of varying duration on sarcoplasmic reticulum function. Journal of Applied Physiology 66: 1383–1389, 1989aPubMedGoogle Scholar
  12. Byrd SK, McCutcheon LJ, Hodgson DR, Gollnick PD. Altered sarcoplasmic reticulum function after high intensity exercise. Journal of Applied Physiology 67: 2072–2077, 1989bPubMedGoogle Scholar
  13. Castle NA, Haylett DG. Effect of channel blockers on potassium efflux from metabolically exhausted frog skeletal muscle. Jour nal of Physiology 383: 31–43, 1987Google Scholar
  14. Chasiotis D, Hultman E, Sahlin K. Acidotic depression of cyclic AMP accumulation and phosphorylase b to a transformation in skeletal muscle of man. Journal of Physiology 335: 197–204, 1982Google Scholar
  15. Cheetham ME, Boobis LH, Brooks S, Williams C. Human muscle metabolism during sprint running. Journal of Applied Physiology 61: 54–60, 1986PubMedGoogle Scholar
  16. Christy RK. The migrations of chlorine ions. Journal of Physiology 63: X, 1927Google Scholar
  17. Clausen T. Regulation of active Na+−K+ transport in skeletal muscle. Physiological Reviews 66: 542–580, 1986PubMedGoogle Scholar
  18. Cooke R, Franks K, Luciani GB, Pate E. The inhibition of rabbit skeletal muscle contraction by hydrogen ions and phosphate. Journal of Physiology 395: 77–97, 1988PubMedGoogle Scholar
  19. Costill DL, Saltin B. Muscle glycogen and electrolytes following exercise and thermal dehydration. In Howald H & Poortmans JR (Eds) Metabolic adaptation to prolonged physical exercise, Biochemistry of exercise II, pp. 352–360. Birkhauser Verlag, Basel, 1975Google Scholar
  20. Davies NW. Modulation of ATP-sensitive K+ channels in skeletal muscle by intracellular protons. Nature 343: 375–377, 1990PubMedCrossRefGoogle Scholar
  21. Dill DB, Talbot JH, Edwards HT. Studies in muscular activity. VI. Response of several individuals to a fixed task. Journal of Physiology 69: 268–305, 1930Google Scholar
  22. Donaldson SKB, Hermansen L. Differential, direct effects of H+ on Ca2+-activated force of skinned fibres from the soleus, cardiac and adductor magnus muscles of rabbits. Pfliigers Archiv 376: 55–65, 1978CrossRefGoogle Scholar
  23. Edwards RHT. Human muscle function and fatigue. In Human muscle fatigue: physiological mechanisms, pp. 1–18, Pitman Medical, London (Ciba Foundation Symposium 82), 1981Google Scholar
  24. Fabiato A, Fabiato F. Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiac and skeletal muscles. Journal of Physiology 276, 233–255, 1978PubMedGoogle Scholar
  25. Fenn WO. Electrolytes in muscle. Physiological Reviews 16: 450–487, 1936Google Scholar
  26. Fenn WO, Cobb DM. Electrolyte changes in muscle during activity. American Journal of Physiology 115: 345–356, 1936Google Scholar
  27. Fink R, Luttgau HC. An evaluation of the membrane constants and the potassium conductance in metabolically exhausted muscle fibres. Journal of Physiology 263: 215–238, 1976PubMedGoogle Scholar
  28. Gollnick PD, Korge P, Karpakka J, Saltin B. Elongation of skeletal muscle relaxation during exercise is linked to reduced calcium uptake by the sarcoplasmic reticulum in man. Acta Physiologica Scandinavica 142: 135–136, 1991PubMedCrossRefGoogle Scholar
  29. Hermansen L, Osnes J. Blood and muscle pH after maximal exercise in man. Journal of Applied Physiology 32: 304–308, 1972PubMedGoogle Scholar
  30. Hermansen L, Orheim A, Sejersted OM. Metabolic acidosis and changes in water and electrolyte balance in relation to fatigue during maximal exercise of short duration. International Journal of Sports Medicine 5: 110–115, 1984CrossRefGoogle Scholar
  31. Hill AV, Lupton H. Muscular exercise, lactic acid, and the supply and utilization of oxygen. Quarterly Journal of Medicine, 135–171, 1923Google Scholar
  32. Hirche H, Schumacher & Hagemann H. Extracellular K+ concentration and K+ balance of the gastrocnemius muscle of the dog during exercise. Pflügers Archiv 387: 231–237, 1980PubMedCrossRefGoogle Scholar
  33. Hnik P, Vyskocil F, Ujec E, Vojsada R, Rehfeldt H. Work-induced potassium loss from skeletal muscles and its physiological implications. Biochemistry of Exercise. VI. International Series Sport Science 16: 345–364, 1976Google Scholar
  34. Hodgkin AL, Horowitcz P. Movements of Na and K in single muscle fibres. Journal of Physiology 145: 405–432, 1959aPubMedGoogle Scholar
  35. Hodgkin AL, Horowitcz P. The influence of potassium on single muscle fibres. Journal of Physiology 148: 127–160, 1959bPubMedGoogle Scholar
  36. Hodgkin AL, Huxley AF. Current carried by sodium and potassium ions through the membrane of the giant axon of Loligo. Journal of Physiology 116: 449–472, 1952aPubMedGoogle Scholar
  37. Hodgkin AL, Huxley AF. The dual effect of membrane potential on sodium conductance in the giant axon of Loligo. Journal of Physiology 116: 497–506, 1952bPubMedGoogle Scholar
  38. Hodgkin AL, Katz B. The effect of sodium ions on the electrical activity of the giant axon of the squid. Journal of Physiology 108: 37–77, 1949PubMedGoogle Scholar
  39. Jones DA. Muscle fatigue due to changes beyond the neuromuscular junction. In Human muscle fatigue: physiological mechanisms, pp. 178–196, Pitman Medical, London (Ciba Foundation Symposium 82), 1981Google Scholar
  40. Jones DA, Bigland-Ritchie B. Electrical and contractile changes in muscle fatigue. Biochemistry of exercise. VI. International Series Sport Science 16: 377–392, 1986Google Scholar
  41. Jones NL, [H+] Control in exercise: concepts and controversies. Biochemistry of exercise. VII. International Series Sport Science 21: 333–340, 1990Google Scholar
  42. Juel C. Potassium and sodium shifts during in vitro isometric muscle contraction, and the time course of the ion-gradient recovery. Pflügers Archiv 406: 458–463, 1986PubMedCrossRefGoogle Scholar
  43. Juel C. The effect of beta2-adrenoceptor activation on ion-shifts and fatigue in mouse soleus muscles stimulated in vitro. Acta Physiologica Scandinavica 134: 209–216, 1988PubMedCrossRefGoogle Scholar
  44. Katz A, Sahlin K, Juhlin-Dannfelt A. Effect of beta-adrenoceptor blockade on H+ and K+ flux in exercising humans. Journal of Applied Physiology 59: 336–341, 1985PubMedGoogle Scholar
  45. Keys A. Exchanges between blood plasma and tissue fluid in man. Science 85: 317–318, 1937PubMedCrossRefGoogle Scholar
  46. Kowalchuk JM, Heigenhauser GJF, Lindinger MI, Sutton JR, Jones NL. Factors influencing hydrogen ion concentration in muscle after intense exercise. Journal of Applied Physiology 65: 2080–2089, 1988PubMedGoogle Scholar
  47. Lannergren J, Westerblad H. Maximum tension and force-velocity properties of fatigued single Xenopus muscle fibres studies by caffeine and high K+. Journal of Physiology 409: 473–490, 1989PubMedGoogle Scholar
  48. Laurell H, Pernow B. Effect of exercise on plasma potassium in man. Acta Physiologica Scandinavica 66: 241–242, 1966PubMedCrossRefGoogle Scholar
  49. Lindinger MI, Heigenhauser GJF. Intracellular ion content of skeletal muscle measured by instrumental neutron activation analysis. Journal of Applied Physiology 63: 426–433, 1987PubMedGoogle Scholar
  50. Lindinger MI, Heigenhauser GJF. Ion fluxes during tetanic stimulation in isolated perfused rat hindlimb. American Journal of Physiology 254: R117–R126, 1988PubMedGoogle Scholar
  51. Lindinger MI, Heigenhauser GJF. Acid-base systems in skeletal muscle and their response to exercise. Biochemistry of exercise. VII. International Series Sport Science 21: 341–358, 1990Google Scholar
  52. Lindinger MI, Heigenhauser GJF. The roles of ion fluxes in skeletal muscle fatigue. Canadian Journal of Physiology and Pharmacology 69: 246–253, 1991PubMedCrossRefGoogle Scholar
  53. Lindinger MI, Heigenhauser GJF, Spriet LL. Effects of intense swimming and tetanic electrical stimulation on skeletal muscle ions and metabolites. Journal of Applied Physiology 63: 2331–2339, 1987PubMedGoogle Scholar
  54. Lindinger MI, Sjogaard G. Potassium regulation during exercise and recovery. Sports Medicine 11: 382–401, 1991PubMedCrossRefGoogle Scholar
  55. Lynch GS, McKenna MJ, Williams DA. Sprint-training and the effect of lowered pH on some contractile properties of human skeletal muscle fibres. Proceedings of the Australian Physiology and Pharmacology Society 20: 165P, 1989Google Scholar
  56. McKenna MJ. The effects of sprint training on electrolyte, acid-base regulation and fatigue during intense exercise in man. Ph.D. Thesis, University of Melbourne, Victoria, 1991Google Scholar
  57. McKenna MJ, Heigenhauser GJF, McKelvie RS, Sutton JR, MacDougall JD, Jones NL. The effects of sprint training upon changes in plasma electrolyte concentrations across active muscle during intense exercise. Proceedings of the Australian Physiology and Pharmacology Society 20: 120P, 1989Google Scholar
  58. McKenna MJ, Schmidt TA, Hargreaves M, Cameron L, Skinner SL, Kjeldsen K. Sprint training improves potassium regulation and reduces muscular fatigue during intense exercise. Proceedings of the Australian Physiology and Pharmacology Society 21: 138P, 1990Google Scholar
  59. Medbø JI, Sejersted OM. Acid-base and electrolyte balance after exhausting exercise in endurance trained and sprint-trained subjects. Acta Physiologica Scandinavica 125: 97–109, 1985PubMedCrossRefGoogle Scholar
  60. Medbø JI, Sejersted OM. Plasma potassium changes with high intensity exercise. Journal of Physiology 421: 105–122, 1990PubMedGoogle Scholar
  61. Merton PA, Hill DK, Morton HB. Indirect and direct stimulation of fatigued human muscle. In Human muscle fatigue: physiological mechanisms, pp 120–129, Pitman Medical, London (Ciba Foundation Symposium 82), 1981Google Scholar
  62. Metzger JM, Moss RL. Greater hydrogen ion induced depression of tension and velocity in skinned single fibres of rat fast than slow muscles. Journal of Physiology 393, 727–742, 1987PubMedGoogle Scholar
  63. Milner-Brown HS, Miller RG. Muscle membrane excitation and impulse propagation velocity are reduced during muscle fatigue. Muscle and Nerve 9: 367–374, 1986PubMedCrossRefGoogle Scholar
  64. Nevill ME, Boobis LH, Brooks S, Williams C. Effect of training on muscle metabolism during treadmill sprinting. Journal of Applied Physiology 67: 2376–2382, 1989PubMedGoogle Scholar
  65. Nosek TM, Fender KY, Godt RE. It is diprotonated inorganic phosphate that depresses force in skinned skeletal muscle fibres. Science 236: 191–193, 1987PubMedCrossRefGoogle Scholar
  66. Owles WH. Alterations in the lactic acid content of the blood as a result of light exercise, and associated changes in the CO2 combining power of the blood and in the alveolar CO2 pressure. Journal of Physiology 69: 214–237, 1930PubMedGoogle Scholar
  67. Pallotta BS, Magleby KL, Barrett JN. Single channel recordings of Ca2+-activated K+ currents in rat muscle cell culture. Nature 293: 471–474, 1981PubMedCrossRefGoogle Scholar
  68. Rolett EL, Strange S, Sjogaard G, Kiens B, Saltin B. Beta2-Adrenergic stimulation does not prevent potassium loss from exercising quadriceps muscle. American Journal of Physiology 258: R1192–R1200, 1990PubMedGoogle Scholar
  69. Ryffel JH. Experiments in lactic acid formation in man. Journal of Physiology 39: 29P–32P, 1909Google Scholar
  70. Sahlin K, Alverstrand A, Brandt R, Hultman E. Intracellular pH and bicarbonate concentration in human muscle during recovery from exercise. Journal of Applied Physiology 45: 474–480, 1978PubMedGoogle Scholar
  71. Saltin B, Sjogaard G, Strange S, Juel C. Redistribution of potassium in the human body during muscular exercise; its role to maintain whole body homeostasis. In Shiraki K, Yousef MK (Eds) Man in stressful environments; thermal and work physiology, Charles C Thomas, Springfield, 111., 1987Google Scholar
  72. Sejersted OM, Hallen J. Na, K homeostasis of skeletal muscle during activation. Medicine and Sport Science 26: pp. 1–11, Karger, Basel, 1987Google Scholar
  73. Sejerted OM, Vollestad NK, Medbo JI. Muscle fluid and electrolyte balance during and following exercise. Acta Physiologica Scandinavica 128 (Suppl. 556): 119–127, 1986Google Scholar
  74. Sembrowich WL, Johnson D, Wang E, Hutchinson TE. Electron microprobe analysis of fatigued fast- and slow-twitch mucle. In Knuttgen et al. (Eds) Biochemistry of Exercise, International Series on Sport Science, Vol. 13, pp. 571–576, Human Kinetics Publishers, Champaign, 111. 1983Google Scholar
  75. Sharp RL, Costill DL, Fink WJ, King DS. Effects of eight weeks of bicycle ergometer sprint training on human muscle buffer capacity. International Journal of Sports Medicine 7: 13–17, 1986PubMedCrossRefGoogle Scholar
  76. Sjøgaard G. Electrolytes in slow and fast muscle fibres of humans at rest and with dynamic exercise. American Journal of Physiology 245: R25–R31, 1983PubMedGoogle Scholar
  77. Sjøgaard G. Water and electrolyte fluxes during exercise and their relation to muscle fatigue. Acta Physiologica Scandinavica 128 (Suppl. 556): 129–136, 1986Google Scholar
  78. Sjøgaard G. Exercise-induced muscle fatigue; the significance of potassium. Acta Physiologica Scandinavica 140 (Suppl. 593), 1–63, 1990Google Scholar
  79. Sjøgaard G. Role of exercise-induced potassium fluxes underlying muscle fatigue: a brief review. Canadian Journal of Physiology and Pharmacology 69: 238–245, 1991PubMedCrossRefGoogle Scholar
  80. Sjøgaard G, Adams RP, Saltin B. Water and ion shifts in skeletal muscle of humans with intense dynamic knee extension. American Journal of Physiology 248: R190–R196, 1985PubMedGoogle Scholar
  81. Sjøgaard G, Saltin B. Extra- and intracellular water spaces in muscles of man at rest and with dynamic exercise. American Journal of Physiology 243: R271–R280, 1982PubMedGoogle Scholar
  82. Skinner SL. A cause of erroneous potassium concentrations. Lancet 2: 478–480, 1961CrossRefGoogle Scholar
  83. Spriet LL, Lindinger MI, McKelvie RS, Heigenhauser GJF, Jones NL. Muscle glycogenosis and H+ concentration during maximal intermittent cycling. Journal of Applied Physiology 66: 8–13, 1989PubMedGoogle Scholar
  84. Spruce AE, Standen NB, Stanfield PR. Voltage-dependent ATP-sensitive potassium channels of skeletal muscle membrane. Nature 316: 736–738, 1985PubMedCrossRefGoogle Scholar
  85. Sreter FA. Cell water, sodium and potassium in red and white mammalian muscles. American Journal of Physiology 205: 1295–1298, 1963PubMedGoogle Scholar
  86. Stewart CA, Bretag AH. Membrane conductance of metabolically exhausted mammalian muscle. Proceedings of the Australian Physiology and Pharmacology Society 21: 28P, 1991Google Scholar
  87. Stewart PA. How to understand acid-base: a quantitative acid-base primer for biology and medicine, Elsevier North Holland, New York, 1981Google Scholar
  88. Stewart PA. Modern quantitative acid-base chemistry. Canadian Journal of Physiology and Pharmacology 61: 1444–1461, 1983PubMedCrossRefGoogle Scholar
  89. Sutton JR, Jones NL, Toews CJ. Effect of pH on muscle glycolysis during exercise. Clinical Science 61: 331–338, 1981PubMedGoogle Scholar
  90. van Beaumont W, Strand JC, Petrovsky JS, Hipskind SG, Greenleaf JE. Changes in total plasma content of electrolytes and proteins with maximal exercise. Journal of Applied Physiology 34: 102–106, 1973PubMedGoogle Scholar
  91. Vollestad N, Sejersted OM. Biochemical correlates of fatigue: a brief review. European Journal of Applied Physiology 57: 336–347, 1988CrossRefGoogle Scholar
  92. Vyskocil F, Hnik P, Vejsada R, Ujec E. The measurement of K+ e concentration changes in human muscles during volitional contractions. Pflugers Archiv 399: 235–237, 1983PubMedCrossRefGoogle Scholar
  93. Westerblad H, Lannergren J. Force and membrane potential during and after fatiguing, intermittent stimulation of single Xenopus muscle fibres. Acta Physiologica Scandinavica 128: 369–378, 1986PubMedCrossRefGoogle Scholar
  94. Westerblad H, Lee JA, Lamb AG, Bolsover SR, Allen DG. Spatial gradients of intracellular calcium in skeletal muscle during fatigue. Pflugers Archiv 415: 734–740, 1990PubMedCrossRefGoogle Scholar

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© Adis International Limited 1992

Authors and Affiliations

  • Michael J. McKenna
    • 1
  1. 1.Department of Biological Sciences, Faculty of Health SciencesThe University of SydneyLidcombeAustralia

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