Skip to main content

Advertisement

SpringerLink
Log in

Alterations of Neuromuscular Function After Prolonged Running, Cycling and Skiing Exercises

  • Review Article
  • Published:
Sports Medicine Aims and scope Submit manuscript

Abstract

It is well known that impairment of performance resulting from muscle fatigue differs according to the types of contraction involved, the muscular groups tested and the exercise duration/intensity. Depending on these variables, strength loss with fatigue can originate from several sites from the motor cortex through to contractile elements. This has been termed ‘task dependency of muscle fatigue’.

Only recently have studies focused on the origin of muscle fatigue after prolonged exercise lasting 30 minutes to several hours. Central fatigue has been shown to contribute to muscle fatigue during long-distance running by using different methods such as the twitch interpolation technique, the ratio of the electromyogram (EMG) signal during maximal voluntary contraction normalised to the M-wave amplitude or the comparison of the forces achieved with voluntary-and electrically-evoked contractions. Some central activation deficit has also been observed for knee extensor muscles in cycling but central fatigue after activities inducing low muscular damage was attenuated compared with running. While supraspinal fatigue cannot be ruled out, it can be suggested that spinal adaptation, such as inhibition from type III and IV group afferents or disfacilitation from muscle spindles, contributes to the reduced neural drive after prolonged exercise. It has been shown that after a 30km run, individuals with the greatest knee extensor muscle strength loss experienced a significant activation deficit. However, central fatigue alone cannot explain the entire strength loss after prolonged exercise. Alterations of neuromuscular propagation, excitation-contraction coupling failure and modifications of the intrinsic capability of force production may also be involved. Electrically-evoked contractions and associated EMG can help to characterise peripheral fatigue. The purpose of this review is to further examine the central and peripheral mechanisms contributing to strength loss after prolonged running, cycling and skiing exercises.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Table I
Fig. 2
Fig. 3
Fig. 4
Table II
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Edwards RHT. Human muscle function and fatigue. In: Porter R, Whelan J, editors. Human muscle fatigue: physiological mechanisms. London: Pitman, 1981: 1–18

    Google Scholar 

  2. Enoka RM. Neuromechanics of human movement. 3rd rev ed. Champaign (IL): Human Kinetics, 2002

    Google Scholar 

  3. Ostrowski K, Rohde T, Zacho M, et al. Evidence that interleukin-6 is produced in human skeletal muscle during prolonged running. J Physiol 1998; 508: 949–53

    Article  PubMed  CAS  Google Scholar 

  4. Fournier PE, Stalder J, Mermillod B, et al. Effects of a 110 kilometers ultra-marathon race on plasma hormone levels. Int J Sports Med 1997; 18: 252–6

    Article  PubMed  CAS  Google Scholar 

  5. Noakes TD, Lambert EV, Lambert MI, et al. Carbohydrate ingestion and muscle glycogen depletion during marathon and ultramarathon racing. Eur J Appl Physiol 1988; 57: 482–9

    Article  CAS  Google Scholar 

  6. Brainbridge FA. The physiology of muscular exercise. London: Longmans, Green & Co, 1931

    Google Scholar 

  7. Edwards RHT, Gibson H. Perspectives in the study of normal and pathological skeletal muscle. In: Atlan G, Beliveau L, Bouissou P, editors. Muscle fatigue, biochemical and physiological aspects. Paris: Masson, 1991: 3–15

    Google Scholar 

  8. Davis JM, Bailey SP. Possible mechanisms of central nervous system fatigue during exercise. Med Sci Sports Exerc 1997; 29: 45–57

    PubMed  CAS  Google Scholar 

  9. Koller A, Mair J, Schobersberger W, et al. Effects of prolonged strenuous endurance exercise on plasma myosin heavy chain fragments and other muscular proteins. J Sports Med Phys Fitness 1998; 38: 10–7

    PubMed  CAS  Google Scholar 

  10. Kyröläinen H, Pullinen T, Candau R, et al. Effects of marathon running on running economy and kinematics. Eur J Appl Physiol 2000; 82: 297–304

    Article  PubMed  Google Scholar 

  11. Overgaard K, Lindstrom T, Ingemann-Hansen T, et al. Membrane leakage and increased content of Na+-K+ pumps and Ca2+ in human muscle after a 100-km run. J Appl Physiol 2002; 92: 1891–8

    PubMed  CAS  Google Scholar 

  12. Lepers R, Millet GY, Maffiuletti NA. Effects of cycling cadence on contractile and neural properties of knee extensors. Med Sci Sports Exerc 2001; 33: 1882–8

    Article  PubMed  CAS  Google Scholar 

  13. Lepers R, Maffiuletti NA, Rochette L, et al. Neuromuscular fatigue during a long-duration cycling exercise. J Appl Physiol 2002; 92: 1487–93

    PubMed  Google Scholar 

  14. Millet GY, Lepers R, Maffiuletti NA, et al. Alteration of neuromuscular function after an ultra-marathon. J Appl Physiol 2002; 92: 486–92

    PubMed  CAS  Google Scholar 

  15. Millet GY, Martin V, Lattier G, et al. Mechanisms contributing to knee extensors strength loss after prolonged running exercise. J Appl Physiol 2003; 94: 193–8

    PubMed  CAS  Google Scholar 

  16. Takekura H, Fujinami N, Nishizawa T, et al. Eccentric exercise-induced morphological changes in the membrane systems involved in excitation-contraction coupling in rat skeletal muscle. J Physiol 2001; 533: 571–83

    Article  PubMed  CAS  Google Scholar 

  17. Jones DA, Newham DJ, Torgan C. Mechanical influences on long-lasting human muscle fatigue and delayed-onset pain. J Physiol 1989; 412: 415–27

    PubMed  CAS  Google Scholar 

  18. Millet GY, Martin V, Maffiuletti NA, et al. Neuromuscular fatigue after a ski skating marathon. Can J Appl Physiol 2003; 28: 434–45

    Article  PubMed  Google Scholar 

  19. Davies CTM, Thompson MW. Physiological responses to prolonged exercise in ultramarathon athletes. J Appl Physiol 1986; 61: 611–7

    PubMed  CAS  Google Scholar 

  20. Rama R, Ibanez J, Riera M, et al. Hematological, electrolyte, and biochemical alterations after a 100-km run. Can J Appl Physiol 1994; 19: 411–20

    Article  PubMed  CAS  Google Scholar 

  21. Lepers R, Pousson M, Maffiuletti NA, et al. The effects of a prolonged running exercise on strength characterisics. Int J Sports Med 2000; 21: 275–80

    Article  PubMed  CAS  Google Scholar 

  22. Nicol C, Komi PV, Marconnet P. Fatigue effects of marathon running on neuromuscular performance: II. Changes in force, intergrated electromyographic activity and endurance capacity. Scand J Med Sci Sports 1991; 1: 18–24

    Article  Google Scholar 

  23. Nicol C, Komi PV, Marconnet P. Fatigue effects of marathon running on neuromuscular performance: I. Changes in muscle force and stiffness characteristics. Scand J Med Sci Sports 1991; 1: 10–7

    Article  Google Scholar 

  24. Viitasalo JT, Komi PV, Jacobs I, et al. Effects of prolonged cross-country skiing on neuromuscular performance. Exerc Sport Biol 1982; 12: 191–8

    Google Scholar 

  25. Sahlin K, Seger JY. Effects of prolonged exercise on the contractile properties of human quadriceps muscle. Eur J Appl Physiol 1995; 71: 180–6

    Article  CAS  Google Scholar 

  26. Booth FW, McKenna MJ, Ruell PA, et al. Impaired calcium pump function does not slow relaxation in human skeletal muscle after prolonged exercise. J Appl Physiol 1997; 83: 511–21

    PubMed  CAS  Google Scholar 

  27. Bentley DJ, Smith PA, Davie AJ, et al. Muscle activation of the knee extensors following high intensity endurance exercise in cyclists. Eur J Appl Physiol 2000; 81: 297–302

    Article  PubMed  CAS  Google Scholar 

  28. Lepers R, Hausswirth C, Maffiuletti N, et al. Evidence of neuromuscular fatigue after prolonged cycling exercise. Med Sci Sports Exerc 2000; 32: 1880–6

    Article  PubMed  CAS  Google Scholar 

  29. Forsberg A, Tesch P, Karlsson J. Effect of prolonged exercise on muscle strength performance. In: Asmussen E, Jorgensen K, editors. Biomechanics VI-A. Baltimore (MD): University Park Press, 1979: 62–7

    Google Scholar 

  30. Avela J, Kyröläinen H, Komi P, et al. Reduced reflex sensitivity persists several days after long-lasting stretch-shortening cycle exercises. J Appl Physiol 1999; 86: 1292–300

    Article  PubMed  CAS  Google Scholar 

  31. Davies CTM, White MJ. Muscle weakness following dynamic exercise in human. J Appl Physiol 1982; 53: 236–41

    PubMed  CAS  Google Scholar 

  32. Pasquet B, Carpentier A, Duchateau J, et al. Muscle fatigue during concentric and eccentric contractions. Muscle Nerve 2000; 23: 1727–35

    Article  PubMed  CAS  Google Scholar 

  33. Duchateau J, Enoka RM. Neural adaptations with chronic activity patterns in able-bodied humans. Am J Phys Med Rehabil 2002; 81: S1–S11

    Article  Google Scholar 

  34. Merton PA. Voluntary strength and fatigue. J Physiol 1954; 123: 553–64

    PubMed  CAS  Google Scholar 

  35. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 2001; 81: 1725–89

    PubMed  CAS  Google Scholar 

  36. Noakes TD. Physiological models to understand exercise fatigue and the adaptations that predict or enhance athletic performance. Scand J Med Sci Sports 2000; 10: 123–45

    Article  PubMed  CAS  Google Scholar 

  37. Pitsiladis YP, Strachan AT, Davidson I, et al. Hyperprolactinaemia during prolonged exercise in the heat: evidence for a centrally mediated component of fatigue in trained cyclists. Exp Physiol 2002; 87: 215–26

    Article  PubMed  CAS  Google Scholar 

  38. Wilson WM, Maughan RJ. Evidence for a possible role of 5-hydroxytryptamine in the genesis of fatigue in man: administration of paroxetine, a 5-HT re-uptake inhibitor, reduces the capacity to perform prolonged exercise. Exp Physiol 1992; 77: 921–4

    PubMed  CAS  Google Scholar 

  39. Millet GY, Lepers R, Lattier G, et al. Influence of ultra-long term fatigue on oxygen cost of two types of locomotion. Eur J Appl Physiol 2000; 83: 376–80

    Article  PubMed  CAS  Google Scholar 

  40. Millet GY, Millet GP, Lattier G, et al. Alteration of neuromuscular function after a prolonged road cycling race. Int J Sports Med 2003; 24: 190–4

    Article  PubMed  CAS  Google Scholar 

  41. Perrey S, Millet GY, Candau R, et al. Stretch-shortening cycle in roller ski skating: effects of technique. Int J Sports Med 1998; 19: 513–20

    Article  PubMed  CAS  Google Scholar 

  42. Millet GY, Perrey S, Candau R, et al. External loading does not change energy cost and mechanics of roller ski skating. Eur J Appl Physiol 1998; 78: 276–82

    Article  CAS  Google Scholar 

  43. Hicks A, Fenton J, Garner S, et al. M wave potentiation during and after muscle activity. J Appl Physiol 1989; 66: 2606–10

    PubMed  CAS  Google Scholar 

  44. Dimitrova NA, Dimitrov GV. Amplitude-related characteristics of motor unit and M-wave potentials during fatigue: a simulation study using literature data on intracellular potential changes found in vitro. J Electromyogr Kinesiol 2002; 12: 339–249

    Article  PubMed  CAS  Google Scholar 

  45. Hicks A, McComas AJ. Increased sodium pump activity following repetitive stimulation of rat soleus muscles. J Physiol 1989; 414: 337–49

    PubMed  CAS  Google Scholar 

  46. Pastene J, Germain M, Allevard A, et al. Water balance during and after marathon running. Eur J Appl Physiol 1996; 73: 49–55

    Article  CAS  Google Scholar 

  47. Nielsen OB, Clausen T. The Na+/K+-pump protects muscle excitability and contractility during exercise. Exerc Sport Sci Rev 2000; 28: 159–64

    PubMed  CAS  Google Scholar 

  48. Fitts RH. Muscle fatigue: the cellular aspects. Am J Sports Med 1996; 24: S9–S13

    Article  PubMed  CAS  Google Scholar 

  49. Sjogaard G. Potassium and fatigue: the pros and cons. Acta Physiol Scand 1996; 156: 257–64

    Article  PubMed  CAS  Google Scholar 

  50. Green HJ. Mechanisms of muscle fatigue in intense exercise. J Sports Sci 1997; 15: 247–56

    Article  PubMed  CAS  Google Scholar 

  51. Nielsen OB, De Paoli F, Overgaard K. Protective effects of lactic acid on force production in rat skeletal muscle. J Physiol 2001; 536: 161–6

    Article  PubMed  CAS  Google Scholar 

  52. Eversten F, Medbo JI, Jebens E, et al. Hard training for 5 mo increases Na+-K+ pump concentration in skeletal muscle of cross-country skiers. Am J Physiol Regul Integr Comp Physiol 1997; 272: R1417–R24

    Google Scholar 

  53. Pousson M, Pérot C, Goubel F. Stiffness changes and fibre type transitions in rat soleus muscle produced by jumping training. Pflugers Arch 1991; 419: 127–30

    Article  PubMed  CAS  Google Scholar 

  54. Vigreux B, Cnockaert JC, Pertuzon E. Effects of fatigue on the series elastic component on human muscle. Eur J Appl Physiol 1980; 45: 11–7

    Article  CAS  Google Scholar 

  55. Biilow PM, Norregaard J, Mehlsen J, et al. The twitch interpolation technique for study of fatigue of human quadriceps muscle. J Neurosci Methods 1995; 62: 103–9

    Article  Google Scholar 

  56. Chin ER, Allen DG. Effects of reduced muscle glycogen concentration on force, Ca2+ release and contractile protein function in intact mouse skeletal muscle. J Physiol 1997; 498: 17–29

    PubMed  CAS  Google Scholar 

  57. Lattier G, Millet GY, Martin A, et al. Fatigue and recovery after high-intensity exercise — part 1: neuromuscular fatigue. Int J Sports Med. In press

  58. Binder-Macleod SA, Lee SCK, Fritz AD, et al. New-look at force-frequency relationship of human skeletal muscle: effect of fatigue. J Neurophysiol 1998; 79: 1858–68

    PubMed  CAS  Google Scholar 

  59. Hill CA, Thompson MW, Ruell PA, et al. Sarcoplasmic reticulum function and muscle contractile character following fatiguing exercise in humans. J Physiol 2001; 531: 871–8

    Article  PubMed  CAS  Google Scholar 

  60. Kyparos A, Matziari C, Albani M, et al. A decrease in soleus muscle force generation in rats after downhill running. Can J Appl Physiol 2001; 26: 323–35

    Article  PubMed  CAS  Google Scholar 

  61. Strojnik V, Komi PV. Neuromuscular fatigue after maximal stretch-shortening cycle exercise. J Appl Physiol 1998; 84: 344–50

    PubMed  CAS  Google Scholar 

  62. Strojnik V, Komi PV. Fatigue after submaximal intensive stretch-shortening cycle exercise. Med Sci Sports Exerc 2000; 32: 1314–9

    Article  PubMed  CAS  Google Scholar 

  63. Feieresen P, Duchateau J, Hainaut K. Motor unit recruitment order during voluntary and electrically induced contractions in the tibialis anterior. Exp Brain Res 1997; 11: 117–23

    Article  Google Scholar 

  64. Heyters M, Carpentier A, Duchateau J, et al. Twitch analysis as an approach to motor unit activation during electrical stimulation. Can J Appl Physiol 1994; 19: 451–61

    Article  PubMed  CAS  Google Scholar 

  65. Lexell J, Henriksson-Larsen K, Sjostrom M. Distribution of different fibre types in human skeletal muscles: a study of cross-sections on whole muscle vastus lateralis. Acta Physiol Scand 1983; 117: 115–22

    Article  PubMed  CAS  Google Scholar 

  66. Psek JA, Cafarelli E. Behaviour of coactive muscle during fatigue. J Appl Physiol 1993; 74: 170–5

    PubMed  CAS  Google Scholar 

  67. Rothmuller C, Cafarelli E. Effect of vibration on antagonist muscle coactivation during progressive fatigue in humans. J Physiol 1995; 485 (Pt 3): 857–64

    PubMed  CAS  Google Scholar 

  68. Miller M, Downham D, Lexell J. Superimposed single impulse and pulse train electrical stimulation: a quantative assessment during submaximal isometric knee extension in young healthy men. Muscle Nerve 1999; 22: 1038–46

    Article  PubMed  CAS  Google Scholar 

  69. Taylor JL, Allen GM, Gandevia SC. Changes in motor cortical excitability during human muscle fatigue. J Physiol 1996; 490: 519–28

    PubMed  CAS  Google Scholar 

  70. Tergau F, Geese R, Bauer A, et al. Motor cortex fatigue in sports measured by transcranial magnetic double stimulation. Med Sci Sports Exerc 2000; 32: 1942–8

    Article  PubMed  CAS  Google Scholar 

  71. Löscher WN, Nordlund MM. Central fatigue and motor cortical excitability during repeated shortening and lengthening actions. Muscle Nerve 2002; 25: 864–72

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Dr Sandra Hunter for her helpful comments in preparing the manuscript. No sources of funding were used to assist in the preparation of this manuscript. The authors have no conflicts of interest that are directly relevant to the content of this manuscript.

Author information

Authors and Affiliations

  1. Research Group Physiology and Physiopathology of Exercise and Handicap, University of Saint-Etienne, Saint-Etienne, France

    Guillaume Y. Millet

  2. Faculty of Sport Sciences, University of Burgundy, Dijon, France

    Romuald Lepers

Authors
  1. Guillaume Y. Millet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Romuald Lepers
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Guillaume Y. Millet.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Millet, G.Y., Lepers, R. Alterations of Neuromuscular Function After Prolonged Running, Cycling and Skiing Exercises. Sports Med 34, 105–116 (2004). https://doi.org/10.2165/00007256-200434020-00004

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2165/00007256-200434020-00004

Keywords

Search

Navigation