Sports Medicine

, Volume 41, Issue 6, pp 489–506 | Cite as

Can Neuromuscular Fatigue Explain Running Strategies and Performance in Ultra-Marathons?

The Flush Model
  • Guillaume Y. MilletEmail author
Review Article


While the industrialized world adopts a largely sedentary lifestyle, ultra-marathon running races have become increasingly popular in the last few years in many countries. The ability to run long distances is also considered to have played a role in human evolution. This makes the issue of ultra-long distance physiology important. In the ability to run multiples of 10km (up to 1000km in one stage), fatigue resistance is critical. Fatigue is generally defined as strength loss (i.e. a decrease in maximal voluntary contraction [MVC]), which is known to be dependent on the type of exercise. Critical task variables include the intensity and duration of the activity, both of which are very specific to ultra-endurance sports. They also include the muscle groups involved and the type of muscle contraction, two variables that depend on the sport under consideration. The first part of this article focuses on the central and peripheral causes of the alterations to neuromuscular function that occur in ultra-marathon running. Neuromuscular function evaluation requires measurements of MVCs and maximal electrical/magnetic stimulations; these provide an insight into the factors in the CNS and the muscles implicated in fatigue. However, such measurements do not necessarily predict how muscle function may influence ultra-endurance running and whether this has an effect on speed regulation during a real competition (i.e. when pacing strategies are involved). In other words, the nature of the relationship between fatigue as measured using maximal contractions/stimulation and submaximal performance limitation/regulation is questionable. To investigate this issue, we are suggesting a holistic model in the second part of this article. This model can be applied to all endurance activities, but is specifically adapted to ultra-endurance running: the flush model. This model has the following four components: (i) the ball-cock (or buoy), which can be compared with the rate of perceived exertion, and can increase or decrease based on (ii) the filling rate and (iii) the water evacuated through the waste pipe, and (iv) a security reserve that allows the subject to prevent physiological damage. We are suggesting that central regulation is not only based on afferent signals arising from the muscles and peripheral organs, but is also dependent on peripheral fatigue and spinal/supraspinal inhibition (or disfacilitation) since these alterations imply a higher central drive for a given power output. This holistic model also explains how environmental conditions, sleep deprivation/mental fatigue, pain-killers or psychostimulants, cognitive or nutritional strategies may affect ultra-running performance.


Sleep Deprivation Filling Rate Central Fatigue Pace Strategy 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.



The author would like to thank Professor Ken Nosaka for his valuable comments on the manuscript and Wanda Lipski for English language correction.

No sources of funding were used to conduct this study or prepare this manuscript. The author has no conflicts of interest that are directly relevant to this article.


  1. 1.
    Enoka RM, Stuart DG. Neurobiology of muscle fatigue. J Appl Physiol 1992 May; 72 (5): 1631–48PubMedGoogle Scholar
  2. 2.
    Hoffman MD, Ong JC, Wang G. Historical analysis of participation in 161-km ultramarathons in North America. Int J History Sport 2010; 27 (11): 1877–91CrossRefGoogle Scholar
  3. 3.
    Knez WL, Coombes JS, Jenkins DG. Ultra-endurance exercise and oxidative damage: implications for cardiovascularhealth. Sports Med 2006; 36 (5): 429–41PubMedCrossRefGoogle Scholar
  4. 4.
    Zaryski C, Smith DJ. Training principles and issues for ultra-endurance athletes. Cur Sports Med Rep 2005; 4 (3): 165–70Google Scholar
  5. 5.
    Noakes TD. The limits of endurance exercise. Basic Res Cardiol 2006 Sep; 101 (5): 408–17PubMedCrossRefGoogle Scholar
  6. 6.
    Bramble DM, Lieberman DE. Endurance running and the evolution of Homo. Nature 2004 Nov 18; 432 (7015): 345–52PubMedCrossRefGoogle Scholar
  7. 7.
    Pearson H. Physiology: freaks of nature? Nature 2006 Dec 21; 444 (7122): 1000–1PubMedCrossRefGoogle Scholar
  8. 8.
    Abbiss CR, Laursen PB. Models to explain fatigue during prolonged endurance cycling. Sports Med 2005; 35 (10): 865–98PubMedCrossRefGoogle Scholar
  9. 9.
    Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 2001; 81 (4): 1725–89PubMedGoogle Scholar
  10. 10.
    Meeusen R, Watson P, Hasegawa H, et al. Central fatigue: the serotonin hypothesis and beyond. Sports Med 2006; 36 (10): 881–909PubMedCrossRefGoogle Scholar
  11. 11.
    Forestier N, Nougier V. The effects of muscular fatigue on the coordination of a multijoint movement in human. Neurosci Lett 1998 Aug 21; 252 (3): 187–90PubMedCrossRefGoogle Scholar
  12. 12.
    Brisswalter J, Collardeau M, Rene A. Effects of acute physical exercise characteristics on cognitive performance. Sports Med 2002; 32 (9): 555–66PubMedCrossRefGoogle Scholar
  13. 13.
    Bainbridge FA. The physiology of muscular exercise. New York: Longmans, Green and Co., 1931Google Scholar
  14. 14.
    Millet GY, Lepers R. Alterations of neuromuscular function after prolonged running, cycling and skiing exercises. Sports Med 2004; 34 (2): 105–16PubMedCrossRefGoogle Scholar
  15. 15.
    Millet GY, Aubert D, Favier FB, et al. Effect of acute hypoxia on central fatigue during repeated isometric legcontractions. Scand J Med Sci Sports 2009 Oct; 19 (5): 695–702PubMedCrossRefGoogle Scholar
  16. 16.
    Nybo L, Nielsen B. Hyperthermia and central fatigue during prolonged exercise in humans. J Appl Physiol 91 (3): 1055–60Google Scholar
  17. 17.
    Marcora SM, Staiano W, Manning V. Mental fatigue impairs physical performance in humans. J Appl Physiol 2009 Mar; 106 (3): 857–64PubMedCrossRefGoogle Scholar
  18. 18.
    Gauche E, Lepers R, Rabita G, et al. Vitamin and mineral supplementation and neuromuscular recovery after a running race. Med Sci Sports Exerc 2006 Dec; 38 (12): 2110–7PubMedCrossRefGoogle Scholar
  19. 19.
    Petersen K, Hansen CB, Aagaard P, et al. Muscle mechanical characteristics in fatigue and recovery from amarathon race in highly trained runners. Eur J Appl Physiol 2007 Oct; 101 (3): 385–96PubMedCrossRefGoogle Scholar
  20. 20.
    Racinais S, Girard O, Micallef JP, et al. Failed excitability of spinal motoneurons induced by prolonged runningexercise. J Neurophysiol 2007 Jan; 97 (1): 596–603PubMedCrossRefGoogle Scholar
  21. 21.
    Ross EZ, Middleton N, Shave R, et al. Corticomotor excitability contributes to neuromuscular fatigue followingmarathon running in man. Exp Physiol 2007 Mar; 92 (2): 417–26PubMedCrossRefGoogle Scholar
  22. 22.
    Saldanha A, Nordlund Ekblom MM, Thorstensson A. Central fatigue affects plantar flexor strength after prolongedrunning. Scand J Med Sci Sports 2008 Jun; 18 (3): 383–8PubMedCrossRefGoogle Scholar
  23. 23.
    Millet GY, Tomazin K, Verges S, et al. Neuromuscular consequences of an extreme mountain ultra-marathon. PLoS ONE 2011; 6 (2): e17059CrossRefGoogle Scholar
  24. 24.
    Lepers R, Pousson M, Maffiuletti NA, et al. The effects of a prolonged running exercise on strength characterisics. Int J Sports Med 1999; 21: 275–80CrossRefGoogle Scholar
  25. 25.
    Millet GY, Lepers R, Maffiuletti NA, et al. Alterations of neuromuscular function after an ultra marathon. J Appl Physiol 2002 Feb; 92 (2): 486–92PubMedGoogle Scholar
  26. 26.
    Martin V, Kerhervé H, Messonnier LA, et al. Central and peripheral contributions to neuromuscular fatigue inducedby a 24-h treadmill run. J Appl Physiol 2010; 108: 1224–33PubMedCrossRefGoogle Scholar
  27. 27.
    Millet GY, Martin V, Lattier G, et al. Mechanisms contributing to knee extensor strength loss after prolongedrunning exercise. J Appl Physiol 2003 Jan; 94 (1): 193–8PubMedGoogle Scholar
  28. 28.
    Davies CTM, Thompson MW. Physiological responses to prolonged exercise in ultramarathon athletes. J Appl Physiol 1986; 61 (2): 611–7PubMedGoogle Scholar
  29. 29.
    Nicol C, Komi PV, Marconnet P. Fatigue effects of marathon running on neuromuscular performance. II: changesin force, intergrated electromyographic activity and endurancecapacity Scand J Med Sci Sports 1991; 1: 18–24Google Scholar
  30. 30.
    Nicol C, Komi PV, Marconnet P. Fatigue effects of marathon running on neuromuscular performance. I: changesin muscle force and stiffness characteristics Scand J MedSci Sports 1991; 1: 10–7Google Scholar
  31. 31.
    Millet GY, Lepers R, Lattier G, et al. Influence of ultralong- term fatigue on the oxygen cost of two types of locomotion. Eur J Appl Physiol 2000 Nov; 83 (4-5): 376–80PubMedCrossRefGoogle Scholar
  32. 32.
    Place N, Lepers R, Deley G, et al. Time course of neuromuscular alterations during a prolonged running exercise. Med Sci Sports Exerc 2004 Aug; 36 (8): 1347–56PubMedCrossRefGoogle Scholar
  33. 33.
    Rasmussen P, Nielsen J, Overgaard M, et al. Reduced muscle activation during exercise related to brain oxygenationand metabolism in humans. J Physiol 2010 Jun 1; 588 (Pt11): 1985–95PubMedCrossRefGoogle Scholar
  34. 34.
    Taylor JL, Gandevia SC. A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 2008 Feb; 104 (2): 542–50PubMedCrossRefGoogle Scholar
  35. 35.
    Ohta M, Hirai N, Ono Y, et al. Clinical biochemical evaluation of central fatigue with 24-hour continuous exercise. Rinsho Byori 2005 Sep; 53 (9): 802–9PubMedGoogle Scholar
  36. 36.
    Davis JM, Bailey SP. Possible mechanisms of central nervous system fatigue during exercise. Med Sci Sports Exerc 1997; 29 (1): 45–57PubMedCrossRefGoogle Scholar
  37. 37.
    Nybo L, Rasmussen P. Inadequate cerebral oxygen delivery and central fatigue during strenuous exercise. Exerciseand sport sciences reviews 2007 Jul; 35 (3): 110–8CrossRefGoogle Scholar
  38. 38.
    Lepers R, Maffiuletti NA, Rochette L, et al. Neuromuscular fatigue during a long-duration cycling exercise. J Appl Physiol 2002 Apr; 92 (4): 1487–93PubMedGoogle Scholar
  39. 39.
    Millet GY, Millet GP, Lattier G, et al. Alteration of neuromuscular function after a prolonged road cycling race. Int J Sports Med 2003 Apr; 24 (3): 190–4PubMedCrossRefGoogle Scholar
  40. 40.
    Millet GY, Martin V, Maffiuletti NA, et al. Neuromuscular fatigue after a ski skating marathon. Can J Appl Physiol 2003 Jun; 28 (3): 434–45PubMedCrossRefGoogle Scholar
  41. 41.
    Zehr PE. Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 2002 Apr; 86 (6): 455–68PubMedCrossRefGoogle Scholar
  42. 42.
    Jeukendrup AE, Vet-Joop K, Sturk A, et al. Relationship between gastro-intestinal complaints and endotoxaemia,cytokine release and the acute-phase reaction during andafter a long-distance triathlon in highly trained men. Clin Sci (Lond) 2000 Jan; 98 (1): 47–55CrossRefGoogle Scholar
  43. 43.
    Kim HJ, Lee YH, Kim CK. Biomarkers of muscle and cartilage damage and inflammation during a 200 km run. Eur J Appl Physiol 2007 Mar; 99 (4): 443–7PubMedCrossRefGoogle Scholar
  44. 44.
    Ostrowski K, Hermann C, Bangash A, et al. A trauma-like elevation of plasma cytokines in humans in responseto treadmill running. J Physiol 1998 Dec 15; 513 (Pt3): 889–94PubMedCrossRefGoogle Scholar
  45. 45.
    Ostrowski K, Rohde T, Zacho M, et al. Evidence that interleukin-6 is produced in human skeletal muscle duringprolonged running. J Physiol 1998 May 1; 508 (Pt3): 949–53PubMedCrossRefGoogle Scholar
  46. 46.
    Papassotiriou I, Alexiou VG, Tsironi M, et al. Severe aseptic inflammation caused by long distance running(246 km) does not increase procalcitonin. Eur J Clin Invest 2008 Apr; 38 (4): 276–9PubMedCrossRefGoogle Scholar
  47. 47.
    Taylor JL, Todd G, Gandevia SC. Evidence for a supraspinal contribution to human muscle fatigue. Clin Exp Pharmacol Physiol 2006 Apr; 33 (4): 400–5PubMedCrossRefGoogle Scholar
  48. 48.
    Todd G, Taylor JL, Gandevia SC. Measurement of voluntary activation of fresh and fatigued human musclesusing transcranial magnetic stimulation. J Physiol 551 (Pt2): 661–71Google Scholar
  49. 49.
    Goodall S, Romer LM, Ross EZ. Voluntary activation of human knee extensors measured using transcranial magneticstimulation. Exp Physiol 2009 Sep; 94 (9): 995–1004PubMedCrossRefGoogle Scholar
  50. 50.
    Sidhu SK, Bentley DJ, Carroll TJ. Locomotor exercise induces long-lasting impairments in the capacity of the humanmotor cortex to voluntarily activate knee extensormuscles. J Appl Physiol 2009 Feb; 106 (2): 556–65PubMedCrossRefGoogle Scholar
  51. 51.
    Dimitrova NA, Dimitrov GV. Amplitude-related characteristics of motor unit and M-wave potentials duringfatigue: a simulation study using literature data on intracellularpotential changes found in vitro. J Electrom Kinesiol 2002; 12: 339–249CrossRefGoogle Scholar
  52. 52.
    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 (1): 10–7PubMedGoogle Scholar
  53. 53.
    Mastaloudis A, Traber MG, Carstensen K, et al. Antioxidants did not prevent muscle damage in response to anultramarathon run. Med Sci Sports Exerc 2006 Jan; 38 (1): 72–80PubMedCrossRefGoogle Scholar
  54. 54.
    Skenderi KP, Kavouras SA, Anastasiou CA, et al. Exertional rhabdomyolysis during a 246-km continuous runningrace. Med Sci Sports Exerc 2006 Jun; 38 (6): 1054–7PubMedCrossRefGoogle Scholar
  55. 55.
    Nosaka K, Sakamoto K, Newton M, et al. How long does the protective effect on eccentric exercise-induced muscledamage last? Med Sci Sports Exerc 2001 Sep; 33 (9): 1490–5PubMedCrossRefGoogle Scholar
  56. 56.
    Martin V, Millet GY, Lattier G, et al. Effects of recovery modes after knee extensor muscles eccentric contractions. Med Sci Sports Exerc 2004 Nov; 36 (11): 1907–15PubMedCrossRefGoogle Scholar
  57. 57.
    Millet GY, Banfi JC, Kerhervé H, et al. Physiological and biological factors associated with a 24 h treadmill ultramarathonperformance. Scand J Med Sci Sports 2011; 21 (1): 54–61PubMedCrossRefGoogle Scholar
  58. 58.
    Millet GY, Morin JB, Degache F, et al. Running from Paris to Beijing: biomechanical and physiological consequences. Eur J Appl Physiol 2009 Dec; 107 (6): 731–8PubMedCrossRefGoogle Scholar
  59. 59.
    Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 2008 Jan; 88 (1): 287–332PubMedCrossRefGoogle Scholar
  60. 60.
    Martin V, Millet GY, Martin A, et al. Assessment of lowfrequency fatigue with two methods of electrical stimulation. J Appl Physiol 2004 Nov; 97 (5): 1923–9PubMedCrossRefGoogle Scholar
  61. 61.
    Hill CA, Thompson MW, Ruell PA, et al. Sarcoplasmic reticulum function and muscle contractile character followingfatiguing exercise in humans. J Physiol 2001; 531: 871–8PubMedCrossRefGoogle Scholar
  62. 62.
    Martin V, Millet GY, Lattier G, et al. Why does knee extensor muscles torque decrease after eccentric-type exercise? J Sports Med Phys Fitness 2005 Jun; 45 (2): 143–51PubMedGoogle Scholar
  63. 63.
    Utter AC, Kang J, Nieman DC, et al. Ratings of perceived exertion throughout an ultramarathon during carbohydrateingestion. Percept Mot Skills 2003; 97: 175–84PubMedGoogle Scholar
  64. 64.
    Kao WF, Shyu CL, Yang XW, et al. Athletic performance and serial weight changes during 12- and 24-hour ultramarathons. Clin J Sport Med 2008 Mar; 18 (2): 155–8PubMedCrossRefGoogle Scholar
  65. 65.
    Knechtle B, Wirth A, Knechtle P, et al. Personal best marathon performance is associated with performancein a 24-h run and not anthropometry or training Vol.. Br J Sports Med 2009 Nov; 43 (11): 836–9PubMedCrossRefGoogle Scholar
  66. 66.
    Wu HJ, Chen KT, Shee BW, et al. Effects of 24 h ultramarathon on biochemical and hematological parameters. World J Gastroenterol 2004 Sep 15; 10 (18): 2711–4PubMedGoogle Scholar
  67. 67.
    Lambert MI, Dugas JP, Kirkman MC, et al. Changes in running speed in a 100 km ultramarathon race. J Sports Sci Med 2004; 3: 167–73Google Scholar
  68. 68.
    Ely MR, Martin DE, Cheuvront SN, et al. Effect of ambient temperature on marathon pacing is dependent onrunner ability. Med Sci Sports Exerc 2008; 40 (9): 1675–80PubMedCrossRefGoogle Scholar
  69. 69.
    March DS, Vanderburgh PM, Titlebaum PJ, et al. Age, sex, and finish time as determinants of pacing in themarathon. J Strength Cond Res 2011; 25 (2): 386–91PubMedCrossRefGoogle Scholar
  70. 70.
    Esteve-Lanao J, Lucia A, deKoning JJ, et al. How do humans control physiological strain during strenuous enduranceexercise? PloS One 2008; 3 (8): e2943CrossRefGoogle Scholar
  71. 71.
    Marcora SM, Bosio A, de Morree HM. Locomotor muscle fatigue increases cardiorespiratory responses and reduces performance during intense cycling exercise independentlyfrom metabolic stress. Am J Physiol Regul Integr Comp Physiol 2008 Mar; 294 (3): R874–83PubMedCrossRefGoogle Scholar
  72. 72.
    Marcora SM, Staiano W. The limit to exercise tolerance in humans: mind over muscle? Eur J Appl Physiol 2010 Mar 11; 763–70CrossRefGoogle Scholar
  73. 73.
    Marcora SM, Staiano W. Reply to: What limits exercise during high-intensity aerobic exercise? Eur J Appl Physiol 2010 Jul 2; 110: 663–4CrossRefGoogle Scholar
  74. 74.
    Ament W, Verkerke GJ. Exercise and fatigue. Sports Med 2009; 39 (5): 389–422PubMedCrossRefGoogle Scholar
  75. 75.
    Hampson DB, St Clair Gibson, Lambert MI, et al. The influence of sensory cues on the perception of exertionduring exercise and central regulation of exercise performance. Sports Med 2001; 31 (13): 935–52PubMedCrossRefGoogle Scholar
  76. 76.
    Noakes TD, St Clair Gibson, Lambert EV. From catastrophe to complexity: a novel model of integrative centralneural regulation of effort and fatigue during exercise inhumans. Br J Sports Med 2004 Aug; 38 (4): 511–4PubMedCrossRefGoogle Scholar
  77. 77.
    St Clair Gibson, Noakes TD. Evidence for complex system integration and dynamic neural regulation of skeletalmuscle recruitment during exercise in humans. BrJ Sports Med 2004 Dec; 38 (6): 797–806CrossRefGoogle Scholar
  78. 78.
    St-Clair Gibson A, Lambert MI, Noakes TD. Neural control of force output during maximal and submaximalexercise. Sports Med 2001; 31 (9): 637–50PubMedCrossRefGoogle Scholar
  79. 79.
    Kayser B. Exercise starts and ends in the brain. Eur J Appl Physiol 2003; 90: 411–9PubMedCrossRefGoogle Scholar
  80. 80.
    Swart J, Lamberts RP, Lambert MI, et al. Exercising with reserve: evidence that the central nervous system regulates prolonged exercise performance. Br J Sports Med 2009 Oct; 43 (10): 782–8PubMedCrossRefGoogle Scholar
  81. 81.
    Tucker R. The anticipatory regulation of performance: the physiological basis for pacing strategies and the developmentof a perception-based model for exercise performance. Br J Sports Med 2009 Jun; 43 (6): 392–400PubMedCrossRefGoogle Scholar
  82. 82.
    Ulmer HV. Concept of an extracellular regulation of muscular metabolic rate during heavy exercise in humansby psychophysiological feedback. Experientia 1996 May15; 52 (5): 416–20PubMedCrossRefGoogle Scholar
  83. 83.
    Amann M, Proctor LT, Sebranek JJ, et al. Opioid-mediated muscle afferents inhibit central motor drive and limitperipheral muscle fatigue development in humans. JPhysiol 2009 Jan 15; 587 (Pt1): 271–83CrossRefGoogle Scholar
  84. 84.
    Marcora S. Perception of effort during exercise is independent of afferent feedback from skeletal muscles,heart, and lungs. J Appl Physiol 2009 Jun; 106 (6): 2060–2PubMedCrossRefGoogle Scholar
  85. 85.
    Amann M, Secher NH. Point: Afferent feedback from fatigued locomotor muscles is an important determinant ofendurance exercise performance. J Appl Physiol 2010 Feb; 108 (2): 452–4PubMedCrossRefGoogle Scholar
  86. 86.
    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 May; 92 (5): 1891–8PubMedGoogle Scholar
  87. 87.
    Martin PG, Gandevia SC, Taylor JL. Muscle fatigue changes cutaneous suppression of propriospinal drive tohuman upper limb muscles. J Physiol 2007 Apr 1; 580 (Pt1): 211–23PubMedCrossRefGoogle Scholar
  88. 88.
    Kayser B, Sliwinski P, Yan S, et al. Respiratory effort sensation during exercise with induced expiratory-flowlimitation in healthy humans. J Appl Physiol 1997 Sep; 83 (3): 936–47PubMedGoogle Scholar
  89. 89.
    Hoffman MD, Lee J, Zhao H, et al. Pain perception after running a 100-mile ultramarathon. Arch Phys Med Rehabil 2007 Aug; 88 (8): 1042–8PubMedCrossRefGoogle Scholar
  90. 90.
    Gandevia SC, Allen GM, Butler JE, et al. Supraspinal factors in human muscle fatigue: evidence for suboptimaloutput from the motor cortex. J Physiol 1996 Jan 15; 490 (Pt2): 529–36PubMedGoogle Scholar
  91. 91.
    Amann M, Romer LM, Subudhi AW, et al. Severity of arterial hypoxaemia affects the relative contributionsof peripheral muscle fatigue to exercise performance inhealthy humans. J Physiol 2007 May 15; 581 (Pt1): 389–403PubMedCrossRefGoogle Scholar
  92. 92.
    Nybo L. CNS fatigue and prolonged exercise: effect of glucose supplementation. Med Sci Sports Exerc 2003 Apr; 35 (4): 589–94PubMedCrossRefGoogle Scholar
  93. 93.
    Tucker R, Marle T, Lambert EV, et al. The rate of heat storage mediates an anticipatory reduction in exercise intensityduring cycling at a fixed rating of perceived exertion. J Physiol 2006; 574 (Pt3): 905–15PubMedCrossRefGoogle Scholar
  94. 94.
    Smirmaul BD. Sense of effort and other unpleasant sensations during exercise: clarifying concepts and mechanisms. Br J Sports Med. In pressGoogle Scholar
  95. 95.
    Fontes EB, Smirmaul BP, Nakamura FY, et al. The Relationship between rating of perceived exertion andmuscle activity during exhaustive constant-load cycling. Int J Sports Med Oct; 31 (10) 683–8Google Scholar
  96. 96.
    Gagnon P, Saey D, Vivodtzev I, et al. Impact of preinduced quadriceps fatigue on exercise response in chronic obstructivepulmonary disease and healthy subjects. J Appl Physiol 2009 Sep; 107 (3): 832–40PubMedCrossRefGoogle Scholar
  97. 97.
    Millet GY. Central fatigue is not the source but can explain performance decrement due to afferent feedback. J Appl Physiol 2010 Feb; 108 (2): 464PubMedGoogle Scholar
  98. 98.
    Fulco CS, Lewis SF, Frykman PN, et al. Muscle fatigue and exhaustion during dynamic leg exercise in normoxiaand hypobaric hypoxia. J Appl Physiol 1996 Nov; 81 (5): 1891–900PubMedGoogle Scholar
  99. 99.
    Myles WS. Sleep deprivation, physical fatigue, and the perception of exercise intensity. Med Sci Sports Exerc 1985 Oct; 17 (5): 580–4PubMedGoogle Scholar
  100. 100.
    Martin BJ. Effect of sleep deprivation on tolerance of prolonged exercise. Eur J Appl Physiol Occup Physiol 1981; 47 (4): 345–54PubMedCrossRefGoogle Scholar
  101. 101.
    Oliver SJ, Costa RJ, Laing SJ, et al. One night of sleep deprivation decreases treadmill endurance performance. Eur J Appl Physiol 2009 Sep; 107 (2): 155–61PubMedCrossRefGoogle Scholar
  102. 102.
    Bond V, Balkissoon B, Franks BD, et al. Effects of sleep deprivation on performance during submaximal andmaximal exercise. J Sports Med Phys Fitness 1986 Jun; 26 (2): 169–74PubMedGoogle Scholar
  103. 103.
    Baden DA, McLean TL, Tucker R, et al. Effect of anticipation during unknown or unexpected exercise duration on rating of perceived exertion, affect, and physiologicalfunction. Br J Sports Med 2005 Oct; 39 (10): 742–6; discussionPubMedCrossRefGoogle Scholar
  104. 104.
    Waterhouse J, Hudson P, Edwards B. Effects of music tempo upon submaximal cycling performance. ScandJ Med Sci Sports 2010 Aug; 20 (4): 662–9CrossRefGoogle Scholar
  105. 105.
    Raglin JS. The psychology of the marathoner: of one mind and many. Sports Med 2007; 37 (4-5): 404–7PubMedCrossRefGoogle Scholar
  106. 106.
    Morgan WP, Pollock ML. Psychologic characterization of the elite distance runner. Ann N Y Acad Sci 1977; 301: 382–403PubMedCrossRefGoogle Scholar
  107. 107.
    Chambers ES, Bridge MW, Jones DA. Carbohydrate sensing in the human mouth: effects on exercise performance andbrain activity. J Physiol 2009 Apr 15; 587 (Pt8): 1779–94PubMedCrossRefGoogle Scholar
  108. 108.
    Williamson JW, McColl R, Mathews D, et al. Hypnotic manipulation of effort sense during dynamic exercise:cardiovascular responses and brain activation. J ApplPhysiol 2001 Apr; 90 (4): 1392–9PubMedGoogle Scholar
  109. 109.
    Sgaard K, Gandevia SC, Todd G, et al. The effect of sustained low-intensity contractions on supraspinal fatiguein human elbow flexor muscles. J Physiol 2006 Jun 1; 573 (Pt2): 511–23CrossRefGoogle Scholar
  110. 110.
    Baldwin J, Snow RJ, Gibala MJ, et al. Glycogen availability does not affect the TCA cycle or TAN pools duringprolonged, fatiguing exercise. J Appl Physiol 2003 Jun; 94 (6): 2181–7PubMedGoogle Scholar
  111. 111.
    Faulkner J, Parfitt G, Eston R. The rating of perceived exertion during competitive running scales with time. Psychophysiology 2008 Nov; 45 (6): 977–85PubMedCrossRefGoogle Scholar
  112. 112.
    Noakes TD. Linear relationship between the perception of effort and the duration of constant load exercise that remains. J Appl Physiol 2004 Apr; 96 (4): 1571–2PubMedCrossRefGoogle Scholar
  113. 113.
    Sgherza AL, Axen K, Fain R, et al. Effect of naloxone on perceived exertion and exercise capacity during maximalcycle ergometry. J Appl Physiol 2002 Dec; 93 (6): 2023–8PubMedGoogle Scholar
  114. 114.
    Scrimgeour AG, Noakes TD, Adams B, et al. The influence of weekly training distance on fractional utilization ofmaximumaerobic capacity in marathon and ultramarathon runners. Eur J Appl Physiol Occup Physiol 1986; 55 (2): 202–9PubMedCrossRefGoogle Scholar
  115. 115.
    Meeusen R. Fatigue: from muscle to brain or vice versa? J Appl Physiol 2010 Feb; 108 (2): 459–60PubMedGoogle Scholar
  116. 116.
    Mauger AR, Jones AM, Williams CA. Influence of acetaminophen on performance during time trial cycling. J Appl Physiol 2010 Jan; 108 (1): 98–104PubMedCrossRefGoogle Scholar
  117. 117.
    Noakes TD, Lambert MI, Hauman R. Which lap is the slowest? An analysis of 32 world mile record performances. Br J Sports Med 2009 Oct; 43 (10): 760–4PubMedCrossRefGoogle Scholar
  118. 118.
    Weir JP, Beck TW, Cramer JT, et al. Is fatigue all in your head? A critical review of the central governor model. BrJ Sports Med 2006 Jul; 40 (7): 573–86CrossRefGoogle Scholar
  119. 119.
    Marino FE, Gard M, Drinkwater E. The limits to exercise performance and the future of fatigue research. Br J Sports Med 2011; 45: 65–7PubMedCrossRefGoogle Scholar
  120. 120.
    Mosso A. La fatica. Milan: Treves, 1891Google Scholar
  121. 121.
    McKenna MJ, Hargreaves M. Resolving fatigue mechanisms determining exercise performance: integrative physiologyat its finest! J Appl Physiol 2008 Jan; 104 (1): 286–7PubMedCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Universitéde LyonSaint-EtienneFrance
  2. 2.Inserm U1042GrenobleFrance

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