Fatigue pp 101-108 | Cite as

The Role of the Sarcolemma Action Potential in Fatigue

  • A. J. Fuglevand
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 384)

Abstract

A prevalent feature of neuromuscular fatigue is a decline in the extracellularly recorded myoelectric signal. One factor that could underlie this change is a decrease in the amplitude of the sarcolemmal action potential. Based on observed reductions in action potential amplitude without effect on force, it has been argued that changes in the action potential during sustained activity would be unlikely to contribute to fatigue. However, those observations were primarily from experiments in which 1) high frequency stimulation may have caused signal cancellation due to action potential overlap; or 2) sustained membrane depolarization may have directly activated excitation-contraction coupling. The relatively low and narrow range of membrane depolarization required for full activation of amphibian and slow-twitch mammalian fibers makes them resistant to incomplete activation if action potentials are depressed during fatigue. Mammalian fast-twitch fibers, on the other hand, require greater depolarization for full activation and also exhibit a greater decrease in action potential amplitude with fatigue. Therefore, it seems probable that fatigue-related decline in action potential amplitude in these fibers leads to incomplete activation and loss of force.

Keywords

Motor Unit Apply Physiology Action Potential Amplitude Single Muscle Fibre Single Motor Unit 
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. Albers BA, Put JHM, Wallinga W & Wirtz P (1989). Quantitative analysis of single muscle fibre action potentials recorded at known distances. Electroencephalography and Clinical Neurophysiology 73, 245–253.PubMedCrossRefGoogle Scholar
  2. Balog EM, Thompson LV & Fitts RH (1994). Role of sarcolemma action potentials and excitability in muscle fatigue. Journal of Applied Physiology 76, 2157–2162.PubMedCrossRefGoogle Scholar
  3. Benzanilla F, Caputo C, Gonzalez-Serratos H & Venosa RA (1972). Sodium dependence of the inward spread of activation in isolated twitch muscle fibres of the frog. Journal of Physiology (London) 223, 507–523.Google Scholar
  4. Bigland-Ritchie B, Johansson R, Lippold OCJ & Woods JJ (1983). Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. Journal of Neurophysiology 50, 313–324.PubMedGoogle Scholar
  5. Bigland-Ritchie B, Kukulka CG, Lippold OCJ & Woods JJ (1982). The absence of neuromuscular transmission failure in sustained maximal voluntary contractions. Journal of Physiology (London) 330, 265–278.Google Scholar
  6. Caputo C (1972). The time course of potassium contractures of single muscle fibres. Journal of Physiology (London) 223, 483–505.Google Scholar
  7. Caputo C & de Bolaños PF (1979). Membrane potential, contractile activation and relaxation rates in voltage clamped short muscle fibres of the frog. Journal of Physiology (London) 289, 175–189.Google Scholar
  8. Chandler WK, Schneider MF, Rakowski RF & Adrian RH (1975). Charge movements in skeletal muscle. Philosophical Transactions of the Royal Society of London, Series B 270, 501–505.CrossRefGoogle Scholar
  9. Chapman JB (1969). Potentiating effect of potassium on skeletal muscle twitch. American Journal of Physiology 217, 898–902.PubMedGoogle Scholar
  10. Clamann HP & Robinson AJ (1985). A comparison of electromyographic and mechanical fatigue properties in motor units of the cat hindlimb. Brain Research 327, 203–219.PubMedCrossRefGoogle Scholar
  11. Duchateau J & Hainaut K (1987). Electrical and mechanical failure during sustained and intermittent contractions in humans. Journal of Applied Physiology 58, 942–947.Google Scholar
  12. Dulhunty AF (1980). Potassium contractures and mechanical activation in mammalian skeletal muscles. Journal of Membrane Biology 57, 223–233.PubMedCrossRefGoogle Scholar
  13. Dulhunty AF (1982). Effects of membrane potential on mechanical activation in skeletal muscle. Journal of General Physiology 79, 233–251.PubMedCrossRefGoogle Scholar
  14. Dulhunty AF (1992). The voltage-activation of contraction in skeletal muscle. Progress in Biophysics and Molecular Biology 57, 181–223.PubMedCrossRefGoogle Scholar
  15. Dulhunty AF & Gage PW (1983). Asymmetrical charge movement in slow-and fast-twitch mammalian muscle fibres in normal and paraplegic rats. Journal of Physiology (London) 341, 213–231.Google Scholar
  16. Dulhunty AF & Gage PW (1985). Excitation-contraction coupling and charge movement in denervated rat extensor digitorum longus and soleus muscles. Journal of Physiology (London) 358, 75–89.Google Scholar
  17. Enoka RM, Rankin LL, Stuart DG & Volz KA (1989). Fatigability of rat hindlimb muscle: associations between electromyogram and force during a fatigue test. Journal of Physiology (London) 408, 251–270.Google Scholar
  18. Enoka RM & Stuart DG (1992). Neurobiology of muscle fatigue. Journal of Applied Physiology 72, 1631–1648.PubMedCrossRefGoogle Scholar
  19. Fuglevand AJ, Winter DA, Patla AE & Stashuk D (1992). Detection of motor unit action potentials with surface electrodes: influence of electrode size and spacing. Biological Cybernetics 67, 143–153.PubMedCrossRefGoogle Scholar
  20. Fuglevand AJ, Zackowski KM, Huey KA & Enoka RM (1993). Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. Journal of Physiology (London) 460, 549–572.Google Scholar
  21. Fujimoto T & Nishizono H (1993). Involvement of membrane excitation failure in fatigue induced by intermittent submaximal voluntary contraction of the first dorsal interosseous muscle. Journal of Sports Medicine and Physical Fitness 33, 107–117.PubMedGoogle Scholar
  22. Garcia MDC, Gonzalez-Serratos H, Morgan JP, Perreault CL & Rozycka M (1991). Differential activation of myofibrils during fatigue in phasic skeletal muscle cells. Journal of Muscle Research and Cell Motility 12, 412–424.PubMedCrossRefGoogle Scholar
  23. Gardiner PF & Olha AE (1987). Contractile and electromyographic characteristics of rat plantaris motor unit types during fatigue in situ. Journal of Physiology (London) 385, 13–34.Google Scholar
  24. Gath I & Stålberg E (1978). The calculated radial decline of the extracellular action potential compared with in situ measurements in the human brachial biceps. Electroencephalography and Clinical Neurophysiology 44, 547–552.PubMedCrossRefGoogle Scholar
  25. Hamm TM, Reinking RM & Stuart DG (1989). Electromyographic responses of mammalian motor units to a fatigue test. Electromyography and Clinical Neurophysiology 29, 485–494.PubMedGoogle Scholar
  26. Hanson J (1974). The effects of repetitive stimulation on the action potential and the twitch of rat muscle. Acta Physiologica Scandinavica 90, 387–400.PubMedCrossRefGoogle Scholar
  27. Hanson J & Persson A (1971). Changes in the action potential and contraction of isolated frog muscle after receptive stimulation. Acta Physiologica Scandinavica 81, 340–348.PubMedCrossRefGoogle Scholar
  28. Heistracher P & Hunt CC (1969). The relation of membrane changes to contraction in twitch muscle fibres. Journal of Physiology (London) 201, 589–611.Google Scholar
  29. Hirche H, Schumacher E & Hagemann H (1980). Extracellular K+ concentration and K+ balance of the gastrocnemius of the dog during exercise. Pflügers Archiv 387, 231–237.PubMedCrossRefGoogle Scholar
  30. Hodgkin AL & Horowicz P (1960). Potassium contractures in single muscle fibres. Journal of Physiology (London) 153, 386–403.Google Scholar
  31. Jones DA (1981). Muscle fatigue due to changes beyond the neuromuscular junction. In: Edwards RHT (ed.), Human Muscle Fatigue: Physiological Mechanisms. Ciba Foundation Symposium, pp. 178–196. London: Pitman Medical.Google Scholar
  32. Jones DA & Bigland-Ritchie B (1986). Electrical and contractile changes in muscle fatigue. In: Saltin B (ed.), International Series on Sport Sciences. Biochemistry of Exercise VI, pp. 377–392. Champaign IL: Human Kinetics.Google Scholar
  33. Juel C (1986). Potassium and sodium shifts during in vitro isometric muscle contraction, and the time course of the ion-gradient recovery. Pflügers Archives 406, 458–463.CrossRefGoogle Scholar
  34. Juel C (1988). Muscle action potential propagation velocity changes during activity. Muscle & Nerve 11, 714–719.CrossRefGoogle Scholar
  35. Kovács L, Ríos E & Schneider MF (1979). Calcium transients and intramembrane charge movement in skeletal muscle fibres. Nature 279, 391–396.PubMedCrossRefGoogle Scholar
  36. Kranz H, Williams AW, Cassel J, Caddy DJ & Silberstein RB (1983). Factors determining the frequency content of the electromyogram. Journal of Applied Physiology 55, 392–399.PubMedGoogle Scholar
  37. Kugelberg E & Lindegren B (1979). Transmission and contraction fatigue of rat motor units in relation to succinate dehydrogenase activity of motor unit fibers. Journal of Physiology (London) 288, 285–300.Google Scholar
  38. Kwiecinski H, Lehmann-Horn F & Rudel R (1984). The resting membrane parameters of human intercostal muscle at low, normal, and high extracellular potassium. Muscle & Nerve 7, 60–65.CrossRefGoogle Scholar
  39. Lännergren J & Westerblad H (1986). Force and membrane potential during and after fatiguing, continuous high-frequency stimulation of single Xenopus muscle fibers. Acta Physiologica Scandinavica 128, 359–368.PubMedCrossRefGoogle Scholar
  40. Lännergren J & Westerblad H (1987). Action potential fatigue in single skeletal muscle fibres of Xenopus. Acta Physiologica Scandinavica 129, 311–318.PubMedCrossRefGoogle Scholar
  41. Larsson L, Edström L, Lindegren B, Gorza L & Schiaffino, S (1991). MHC composition and enzyme-histochemical and physiological properties of a novel fast-twitch motor unit type. American Journal of Physiology 261, C93–C101.PubMedGoogle Scholar
  42. Light PE, Comtois AS & Renaud JM (1994). The effect of glibenclamide on frog skeletal muscle: evidence for KATP + channel activation during fatigue. Journal of Physiology (London) 475, 495–507.Google Scholar
  43. Lindinger MI & Heigenhauser GJF (1991). The roles of ion fluxes in skeletal muscle fatigue. Canadian Journal of Physiology and Pharmacology 69, 246–253.PubMedCrossRefGoogle Scholar
  44. Lindström L, Kadefors R & Petersén I (1977). An electromyographic index for localized muscle fatigue. Journal of Applied Physiology 43, 750–754.PubMedGoogle Scholar
  45. Lüttgau HC (1963). The action of calcium ions on potassium contractures of single muscle fibres. Journal of Physiology (London) 168, 679–697.Google Scholar
  46. Lüttgau HC (1965). The effect of metabolic inhibitors on the fatigue of the action potential in single muscle fibres. Journal of Physiology (London) 178, 45–67.Google Scholar
  47. Lüttgau HC & Oetliker H (1968). The action of caffeine on the activation of the contractile mechanism in striated muscle fibres. Journal of Physiology (London) 194, 51–74.Google Scholar
  48. Metzger JM & Fitts RH (1986). Fatigue from high-and low-frequency muscle stimulation: role of sarcolemma action potentials. Experimental Neurology 93, 320–333.PubMedCrossRefGoogle Scholar
  49. Pagala M, Ravindran K, Amaladevi B, Namba T & Grob D (1994). Potassium and caffeine contractures of mouse muscles before and after fatiguing stimulation. Muscle & Nerve 17, 852–859.CrossRefGoogle Scholar
  50. Radicheva N, Gerilovsky L & Gydikov A (1986). Changes in the muscle fibre extracellular action potentials in long-lasting (fatiguing) activity. European Journal of Applied Physiology 55, 545–552.CrossRefGoogle Scholar
  51. Reinking RM, Stephens JA & Stuart DG (1975). The motor units of cat medial gastrocnemius: problem of their categorisation on the basis of mechanical properties. Experimental Brain Research 23, 301–313.CrossRefGoogle Scholar
  52. Sandercock TG, Faulkner JA, Albers JW & Abbrecht PH (1985). Single motor unit and fiber action potentials during fatigue. Journal of Applied Physiology 58, 1073–1079.PubMedGoogle Scholar
  53. Sandow A (1952). Excitation-contraction coupling in muscular response. Yale Journal of Biology and Medicine 25, 176–201.PubMedGoogle Scholar
  54. Schneider MF & Chandler WK (1973). Voltage dependent charge movement in skeletal muscle: a possible step in excitation-contraction coupling. Nature 242, 244–246.PubMedCrossRefGoogle Scholar
  55. Sjøgaard G (1990). Exercise-induced muscle fatigue: the significance of potassium. Acta Physiologica Scandinavica Supplement 593, 1–63.Google Scholar
  56. Sjøgaard G (1991). Role of exercise-induced potassium fluxes underlying muscle fatigue: a brief review. Canadian Journal of Physiology and Pharmacology 69, 238–245.PubMedCrossRefGoogle Scholar
  57. Vyskocil F, Hník P, Rehfeldt H, Vejsada R & Ujec E (1983). The measurement of Ke+ concentration changes in human muscles during volitional contractions. Pflügers Archiv 399, 235–237.PubMedCrossRefGoogle Scholar
  58. Westerblad H & Lännergren J (1986). Force and membrane potential during and after fatiguing, intermittent tetanic stimulation of single Xenopus muscle fibers. Acta Physiologica Scandinavica 128, 369–378.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • A. J. Fuglevand
    • 1
  1. 1.The John B. Pierce LaboratoryNew HavenUSA

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