Fatigue pp 481-494 | Cite as

Historical Perspective: A Framework for Interpreting Pathobiological Ideas on Human Muscle Fatigue

  • R. H. T. Edwards
  • V. Toescu
  • H. Gibson
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 384)

Abstract

The flow of ideas on the causes of human muscle fatigue appear to have been established in the literature during the last century. Critical analysis had to await innovative experimental designs or techniques. Progress has come particularly from the recognition of inconsistencies, particularly in clinical conditions in which there are alterations in the supply of energy or contractile function. While there is a continuing search for a unique cause of fatigue, much evidence points to there being different causes according to the type of muscular activity or clinical condition. “Nature’s experiments” (patients exhibiting isolated defects of function or metabolism) offer unique opportunities for understanding the relative importance of particular levels of metabolic organization or physiological control. Theories of limiting biochemical processes and the Ca- kinetic basis of electromechanical coupling defects are both essentially “single-cell” models of fatigue. Functional requirements appear to determine the diversity of structure and organization of motor units. This would suggest that a “muscle cell population” approach would take into account the consequences of disease altering the number, type of functioning fibers or intrinsic strength of individual fibers. A graphical model is offered to allow a possible interpretation of the cause of fatigue in different forms of exercise and clinical conditions.

Keywords

Motor Unit Chronic Fatigue Syndrome Muscle Fatigue Central Fatigue Peripheral Fatigue 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adrian ED & Bronk DW (1929). The discharge of impulses in motor nerve fibres. Journal of Physiology (London) 67, 119–151.Google Scholar
  2. Althaus J (1873). Theoretical and practical paralysis, neuralgia and other diseases In: A Treatise on Medical Electricity, 3rd Ed. London: Longmans, Green, and Co.Google Scholar
  3. Bainbridge FA (1931). The Physiology of Muscular Exercise, p. 235. London: Longmans, Green & Co.Google Scholar
  4. Belanger AY & McComas J (1981). Extent of motor unit activation during effort. Journal of Applied Physiology 51, 1131–1135.PubMedGoogle Scholar
  5. Bergström J (1962). Muscle electrolytes in man. Scandinavian Journal of Clinical Laboratory Investigation 14 (suppl 68), 9–88.Google Scholar
  6. Bigland-Ritchie B, Dawson NH, Johansson RS & Lippold OCJ (1986). Reflex origin for the slowing of motoneurone firing rates in fatigue in human voluntary contractions. Journal of Physiology (London) 379, 451–459.Google Scholar
  7. 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
  8. Bigland-Ritchie B, Jones DA & Woods JJ (1979). Excitation frequency and muscle fatigue: electrical responses during human voluntary and stimulated contractions. Experimental Neurology 64, 414–427.PubMedCrossRefGoogle Scholar
  9. Burke RE, Levine DN, Tsairis P & Zajac FE (1973). Physiological types and histochemical profiles in motor units of the cat gastrocnemius. Journal of Physiology (London) 234, 723–748.Google Scholar
  10. Da Costa JKM (1871). On irritable heart: a clinical study of a form of functional cardiac disorder and its consequences. American Journal of Medical Science 61, 17–52.Google Scholar
  11. Davis H & Davis PA (1932). Fatigue in skeletal muscle in relation to the frequency of stimulation. American Journal of Physiology (London) 101, 339–356.Google Scholar
  12. De Jesus PV (1974). Neuromuscular physiology in Luft’s syndrome. Electromyography and Clinical Neurophysiology 14, 17–27.PubMedGoogle Scholar
  13. Drummond M & Drummond WB (1915) (English translation of Mosso A book). Fatigue, pp. 81–102. London: George Allen & Unwin Ltd.Google Scholar
  14. Duchenne L (1872). L’electrisation localisée et de son application a la pathologie et a la thérapeutique par courants induits et par courants galvaniques interrompus et continus. Paris: Bailliere, JB et fils.Google Scholar
  15. Edwards RHT (1983). Biochemical basis of fatigue in exercise: Catastrophy theory of muscular fatigue In: Knuttgen HG, Vogel JA, Poortmans J (eds.), Biochemistry of Exercise, pp. 3–28. Champaign: Human Kinetics.Google Scholar
  16. Edwards RHT, Dawson MJ, Wilkie DR & Gordon RE (1982). Clinical use of nuclear magnetic resonance in the investigation of myopathy. Lancet 1(8274), 725–731.PubMedCrossRefGoogle Scholar
  17. Edwards RHT, Hill DK, Jones DA & Merton PA (1977). Fatigue of long duration in human skeletal muscle after exercise. Journal of Physiology (London) 272, 769–778.Google Scholar
  18. Edwards RG & Lippold OCJ (1956). The relation between force an integrated electrical activity in fatigued muscle. Journal of Physiology (London) 132, 677–681.Google Scholar
  19. Foster M (1883). A Textbook of Physiology. 4th Ed, pp. 96–97. London: Macmillan and Co.Google Scholar
  20. Gibson H & Edwards RHT (1988). No ischaemic recovery of the evoked compound muscle action potential in McArdle’s disease. Clinical Science 75, 40P.Google Scholar
  21. Gibson H & Edwards RHT (1993). Inter-relation of electro-mechanical coupling and chemistry in the study of fatigue by 31P-NMR spectroscopy In: Sargeant AJ, Kerneil D (eds.), Neuromuscular Fatigue, pp. 30-31. Amsterdam: Royal Netherlands Academy of Arts and Sciences.Google Scholar
  22. Gibson H, Carroll N, Clague JE & Edwards RHT (1993a). Exercise performance and fatiguability in patients with the chronic fatigue syndrome. Journal of Neurology, Neurosurgery, and Psychiatry 56, 993–998.PubMedCrossRefGoogle Scholar
  23. Gibson H, Saugen E, Martin PA, Vollestad NK & Edwards RHT (1993b). Individual pathways for eletromechanical-coupling and energy utilization in submaximal exercise. International Union of Physiological Sciences, Glasgow, August 1-6, 216.Google Scholar
  24. Gollnick PD, Karlsson J, Piehl K & Saltin B (1974). Selective glycogen depletion in skeletal muscle fibres in man following sustained contractions. Journal of Physiology (London) 241, 59–67.Google Scholar
  25. Harvey AM & Masland RL (1941). A method for the study of neuromuscular transmission in human subjects. Bulletin of the Hopkins Hospital 68, 81–93.Google Scholar
  26. Henneman E (1957). Relation between size of neurons and their susceptibility to discharge. Science 126, 1345–1347.PubMedCrossRefGoogle Scholar
  27. Hill AV, Long CNH & Lupton H (1924). Muscular exercise lactic acid, and the supply and utilization of oxygen, parts I–III. Proceedings of the Royal Society of London 96, 438–479.CrossRefGoogle Scholar
  28. Hultman E, Bergstrom J & McLennan AN (1967). Breakdown and resynthesis of adenosine triphosphate in connection with muscular work in man. Scandinavian Journal of Clinical Laboratory Investigation 19, 56–66.CrossRefGoogle Scholar
  29. Jolly F (1895). Über myasthenia gravis pseudoparalytica. Berliner Kliniscshe Wochenschrift 32, 1–7.Google Scholar
  30. Jones DA (1981). Muscle fatigue due to changes beyond the neuromuscular junction In: Porter R, Whelan J (eds.), Human Muscle Fatigue: Physiological Mechanisms. Ciba Foundation Symposium 82, pp. 178-212. London: Pitman Medical.Google Scholar
  31. Kaplan EB (1959) (English translation of Duchenne GB book). Physiology of Motion Demonstrated by Means of Electrical Stimulation and Clinical Observation and Applied to the Study of Paralysis and Deformities. Philadelphia: WB Saunders.Google Scholar
  32. Kemp GJ & Radda GK (1994). Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle: an analytical review. Magnetic Resonance Quarterly 10, 43–63.PubMedGoogle Scholar
  33. Kessel L & Hyman HT (1923). The clinical manifestations of disturbances of the involuntary nervous system (autonomie imbalance). American Journal of Medical Sciences 165, 513.CrossRefGoogle Scholar
  34. Lewis T (1918). The Soldier’s Heart and The Effort Syndrome. London: Shaw & Sons.Google Scholar
  35. Lewis T (1942). Pain. New York: The Macmillan Company.Google Scholar
  36. Lindsley DB (1935). Myographic and electromyographic studies of myasthenia gravis. Brain 58, 470–482.CrossRefGoogle Scholar
  37. 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
  38. Lundsgaard E (1930). Über die Einwirkung der Monoiodoessigsäure aud den spaltungs-und Oxydationsstoffweschel. Biochemishe Zeitschrift 220, 8–12.Google Scholar
  39. Marsden CD, Meadows JC & Merton PA (1971). Isolated single motor units in human muscle and their rate of discharge during maximal voluntary effort. Journal of Physiology (London) 217, 12–13P.Google Scholar
  40. Marsden CD, Meadows JC & Merton PA (1983). “Muscular wisdom” that minimizes fatigue during prolonged effort in man: peak rates of motorneuron discharge and slowing of discharge during fatigue In: Desmedt JE (ed.), Motor Control Mechanisms in Health and Disease, pp. 169–211. New York: Raven Press.Google Scholar
  41. McArdle B (1951). Myopathy due to a defect in muscle glycogen breakdown. Clinical Science 10, 13–33.Google Scholar
  42. Merton PA (1954). Voluntary strength and fatigue. Journal of Physiology (London) 123, 553–564.Google Scholar
  43. Merton PA (1956). Problems of muscular fatigue. British Medical Bulletin 12, 219–239.PubMedGoogle Scholar
  44. Miller RG, Giannini D, Milner-Brown HS, Layzer RB, Koretsky AP, Hooper D & Weiner MW (1987). Effects of fatiguing exercise on high-energy phosphates, force, and EMG: evidence for three phases of recovery. Muscle & Nerve 10, 810–821.CrossRefGoogle Scholar
  45. Morgan-Hughes JA, Darveniza P, Kahn SN, Landon DN, Sherratt RM, Land JM & Clark JP (1977). A mitochondrial myopathy characterised by a deficiency in reducible cytochrome b. Brain 100, 617–640.PubMedCrossRefGoogle Scholar
  46. Muller EA (1935). Die Erholung nach statischer Haltearbeit. Arlbeitsphysiologie 8, 72–75.Google Scholar
  47. Needham DM (ed) (1971). Machina Carnis. Cambridge: Cambridge University Press.Google Scholar
  48. Newham DJ, Mills KR, Quigley BM & Edwards RHT (1983). Pain and fatigue after concentric and eccentric muscle contractions. Clinical Science 64, 55–62.PubMedGoogle Scholar
  49. Newsholme EA, Acworth IN & Blomstrand E (1987). Amino acids, brain neurotransmitters and a functional link between muscle and brain that is important in sustained exercise In: Benzi G (ed.), Advances in Myochemistry, pp. 127–133. London: John Libbey, Ltd.Google Scholar
  50. Oppenheimer B, Levine SA, Moneson RA, Rothechild MA, St. Lawrence W & Wilson FN (1918). Appendix of illustrative cases of neurocirculatory asthenia. Military Surgery 42, 409–420.Google Scholar
  51. Rasch PJ & Burke RK (eds.) (1967). The history of kinesiology In: Kinesiology and Applied Anatomy The Science of Human Movement, 3rd Ed., pp. 1–17. Philadelphia: Lea & Febiger.Google Scholar
  52. Rosenthal I (ed.) (1883). General Physiology of Muscles and Nerves. London: Kegan Paul, Trench & Co.Google Scholar
  53. Shorter E (1992). From Paralysis to Fatigue. New York: Free Press.Google Scholar
  54. Siesjo BK (1982). Lactic acidosis in the brain: occurrence, triggering mechanisms and pathophysiological importance In: Porter R, Lawrenson G (eds.), Metabolic Acidosis, Ciba Foundation Symposium 87, pp. 77–88. Edinburgh: Churchill Livingstone.Google Scholar
  55. Stephens JA & Taylor A (1972). Fatigue of maintained voluntary muscle contraction in man. Journal of Physiology (London) 220, 1–18.Google Scholar
  56. Stokes M, Cooper RG & Edwards RHT (1988). Normal muscle strength and fatigability in patients with ‘effort syndromes’. British Medical Journal 297, 1014–1017.PubMedCrossRefGoogle Scholar
  57. Vestergaard-Poulsen P, Thomsen C, Sinkjaer T & Henriksen O (1994). Simultaneous 31P NMR spectroscopy and EMG in exercising and recovering human skeletal muscle: technical aspects. Magnetic Resonance in Medicine 31, 93–102.PubMedCrossRefGoogle Scholar
  58. Vøllestad NK, Sejersted OM, Bahr R & Bigland-Ritchie B (1988). Motor drive and metabolic responses during repeated sub-maximal contractions in man. Journal of Applied Physiology 63, 1–7.CrossRefGoogle Scholar
  59. Waller AD (1891). The sense of effort: an objective study. Brain 14, 179–249.CrossRefGoogle Scholar
  60. Weichardt W (1904). Uber das ermudungtoxin und-antitoxin. Muenchener Medizinsche Wochenschrift 51, 2121–2126.Google Scholar
  61. Wiles CM, Jones DA & Edwards RHT (1981). Fatigue in human metabolic myopathy In: Porter R, Whelan J (eds.), Human Muscle Fatigue: Physiological Mechanisms, Ciba Foundation symposium 82, pp. 264–282. London: Pitman Medical.Google Scholar
  62. Wiles CM, Young A, Jones DA & Edwards RHT (1979). Muscle relaxation rate, fibre-type composition and energy turnover in hyper-and hypo-thyroid patients. Clinical Science 57, 375–384.PubMedGoogle Scholar
  63. Wood P (1941). Da Costa’s syndrome (or effort syndrome). British Medical Journal i, 767–770.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1995

Authors and Affiliations

  • R. H. T. Edwards
    • 1
  • V. Toescu
    • 1
  • H. Gibson
    • 1
  1. 1.Muscle Research Centre, Department of MedicineUniversity of LiverpoolLiverpoolUK

Personalised recommendations