Recovery of central and peripheral neuromuscular fatigue after exercise

Journal of Applied Physiology

Volumn 122, Issue 5, 2017, Pages 1068-1076

  Carroll, T J ^a   Taylor, J L ^b   Gandevia, S C ^b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Central fatigue; Endurance, exercise; Muscle fatigue; Recovery

Indexed keywords

ANIMAL; CENTRAL NERVOUS SYSTEM; EXERCISE; HUMAN; MUSCLE FATIGUE; PERIPHERAL NERVE; PHYSIOLOGY; SKELETAL MUSCLE;

ANIMALS; CENTRAL NERVOUS SYSTEM; EXERCISE; HUMANS; MUSCLE FATIGUE; MUSCLE, SKELETAL; PERIPHERAL NERVES;

EID: 85019252142     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00775.2016     Document Type: Review

References (106)

1. Adam A, De Luca CJ. Firing rates of motor units in human vastus lateralis muscle during fatiguing isometric contractions. J Appl Physiol (1985) 99: 268-280, 2005. doi:10.1152/japplphysiol.01344.2004.
2. Allen DG, Lamb GD, Westerblad H. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88: 287-332, 2008. doi:10.1152/physrev.00015.2007.
3. Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA. Implications of group III and IV muscle afferents for high-intensity endurance exercise performance in humans. J Physiol 589: 5299-5309, 2011. doi:10.1113/jphysiol.2011.213769.
4. Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA. Implications of group III and IV muscle afferents for high-intensity endurance exercise performance in humans. J Physiol 589: 5299-5309, 2011. doi:10.1113/jphysiol.2011.213769.
5. Amann M, Dempsey JA. Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance. J Physiol 586: 161-173, 2008. doi:10.1113/jphysiol.2007.141838.
6. Amann M, Eldridge MW, Lovering AT, Stickland MK, Pegelow DF, Dempsey JA. Arterial oxygenation influences central motor output and exercise performance via effects on peripheral locomotor muscle fatigue in humans. J Physiol 575: 937-952, 2006. doi:10.1113/jphysiol.2006.113936.
7. Amann M, Goodall S, Twomey R, Subudhi AW, Lovering AT, Roach RC. AltitudeOmics: on the consequences of high-altitude acclimatization for the development of fatigue during locomotor exercise in humans. J Appl Physiol (1985) 115: 634-642, 2013. doi:10.1152/japplphysiol.00606.2013.
8. Amann M, Pegelow DF, Jacques AJ, Dempsey JA. Inspiratory muscle work in acute hypoxia influences locomotor muscle fatigue and exercise performance of healthy humans. Am J Physiol Regul Integr Comp Physiol 293: R2036-R2045, 2007. doi:10.1152/ajpregu.00442.2007.
9. Amann M, Proctor LT, Sebranek JJ, Eldridge MW, Pegelow DF, Dempsey JA. Somatosensory feedback from the limbs exerts inhibitory influences on central neural drive during whole body endurance exercise. J Appl Physiol (1985) 105: 1714-1724, 2008. doi:10.1152/japplphysiol.90456.2008.
10. Amann M, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA. Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. J Physiol 587: 271-283, 2009. doi:10.1113/jphysiol.2008.163303.
11. Amann M, Romer LM, Pegelow DF, Jacques AJ, Hess CJ, Dempsey JA. Effects of arterial oxygen content on peripheral locomotor muscle fatigue. J Appl Physiol (1985) 101: 119-127, 2006. doi:10.1152/japplphysiol.01596.2005.
12. Amann M, Romer LM, Subudhi AW, Pegelow DF, Dempsey JA. Severity of arterial hypoxaemia affects the relative contributions of peripheral muscle fatigue to exercise performance in healthy humans. J Physiol 581: 389-403, 2007. doi:10.1113/jphysiol.2007.129700.
13. Amann M, Sidhu SK, Weavil JC, Mangum TS, Venturelli M. Autonomic responses to exercise: group III/IV muscle afferents and fatigue. Auton Neurosci 188: 19-23, 2015. doi:10.1016/j.autneu.2014.10.018.
14. Bigland-Ritchie BR, Dawson NJ, Johansson RS, Lippold OCJ. Reflex origin for the slowing of motoneurone firing rates in fatigue of human voluntary contractions. J Physiol 379: 451-459, 1986. doi:10.1113/jphysiol.1986.sp016263.
15. Blain GM, Mangum TS, Sidhu SK, Weavil JC, Hureau TJ, Jessop JE, Bledsoe AD, Richardson RS, Amann M. Group III/IV muscle afferents limit the intramuscular metabolic perturbation during whole body exercise in humans. J Physiol 594: 5303-5315, 2016. doi:10.1113/JP272283.
16. Booth J, McKenna MJ, Ruell PA, Gwinn TH, Davis GM, Thompson MW, Harmer AR, Hunter SK, Sutton JR. Impaired calcium pump function does not slow relaxation in human skeletal muscle after prolonged exercise. J Appl Physiol (1985) 83: 511-521, 1997.
17. Burnley M, Vanhatalo A, Jones AM. Distinct profiles of neuromuscular fatigue during muscle contractions below and above the critical torque in humans. J Appl Physiol (1985) 113: 215-223, 2012. doi:10.1152/japplphysiol.00022.2012.
18. Butler JE, Taylor JL, Gandevia SC. Responses of human motoneurons to corticospinal stimulation during maximal voluntary contractions and ischemia. J Neurosci 23: 10224-10230, 2003.
19. Carpentier A, Duchateau J, Hainaut K. Motor unit behaviour and contractile changes during fatigue in the human first dorsal interosseus. J Physiol 534: 903-912, 2001. doi:10.1111/j.1469-7793.2001.00903.x.
20. Decorte N, Lafaix PA, Millet GY, Wuyam B, Verges S. Central and peripheral fatigue kinetics during exhaustive constant-load cycling. Scand J Med Sci Sports 22: 381-391, 2012. doi:10.1111/j.1600-0838.2010.01167.x.
21. Dempsey JA, Blain GM, Amann M. Are type III-IV muscle afferents required for a normal steady-state exercise hyperpnoea in humans? J Physiol 592: 463-474, 2014. doi:10.1113/jphysiol.2013.261925.
22. Edwards RH, Hill DK, Jones DA, Merton PA. Fatigue of long duration in human skeletal muscle after exercise. J Physiol 272: 769-778, 1977. doi:10.1113/jphysiol.1977.sp012072.
23. Enoka RM, Baudry S, Rudroff T, Farina D, Klass M, Duchateau J. Unraveling the neurophysiology of muscle fatigue. J Electromyogr Kinesiol 21: 208-219, 2011. doi:10.1016/j.jelekin.2010.10.006.
24. Espiritu MG, Lin CS, Burke D. Motoneuron excitability and the F wave. Muscle Nerve 27: 720-727, 2003. doi:10.1002/mus.10388.
25. Fornal CA, Martín-Cora FJ, Jacobs BL. "Fatigue" of medullary but not mesencephalic raphe serotonergic neurons during locomotion in cats. Brain Res 1072: 55-61, 2006. doi:10.1016/j.brainres.2005.12.007.
26. Froyd C, Beltrami FG, Millet GY, Noakes TD. Central regulation and neuromuscular fatigue during exercise of different durations. Med Sci Sports Exerc 48: 1024-1032, 2016. doi:10.1249/MSS.0000000000000867.
27. Froyd C, Millet GY, Noakes TD. The development of peripheral fatigue and short-term recovery during self-paced high-intensity exercise. J Physiol 591: 1339-1346, 2013. doi:10.1113/jphysiol.2012.245316.
28. Gandevia SC. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81: 1725-1789, 2001.
29. Gandevia SC, Allen GM, Butler JE, Taylor JL. Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex. J Physiol 490: 529-536, 1996. doi:10.1113/jphysiol.1996.sp021164.
30. Garland SJ, Enoka RM, Serrano LP, Robinson GA. Behavior of motor units in human biceps brachii during a submaximal fatiguing contraction. J Appl Physiol (1985) 76: 2411-2419, 1994.
31. Girard O, Mendez-Villanueva A, Bishop D. Repeated-sprint ability - part I: factors contributing to fatigue. Sports Med 41: 673-694, 2011. doi:10.2165/11590550-000000000-00000.
32. Gollnick PD, Körge 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 Physiol Scand 142: 135-136, 1991. doi:10.1111/j.1748-1716.1991.tb09139.x.
33. Goodall S, Charlton K, Hignett C, Prichard J, Barwood M, Howatson G, Thomas K. Augmented supraspinal fatigue following constantload cycling in the heat. Scand J Med Sci Sports 25, Suppl 1: 164-172, 2015. doi:10.1111/sms.12370.
34. Goodall S, Charlton K, Howatson G, Thomas K. Neuromuscular fatigability during repeated-sprint exercise in male athletes. Med Sci Sports Exerc 47: 528-536, 2015. doi:10.1249/MSS.0000000000000443.
35. Goodall S, González-Alonso J, Ali L, Ross EZ, Romer LM. Supraspinal fatigue after normoxic and hypoxic exercise in humans. J Physiol 590: 2767-2782, 2012. doi:10.1113/jphysiol.2012.228890.
36. Goodall S, Ross EZ, Romer LM. Effect of graded hypoxia on supraspinal contributions to fatigue with unilateral knee-extensor contractions. J Appl Physiol (1985) 109: 1842-1851, 2010. doi:10.1152/japplphysiol.00458.2010.
37. Goodall S, Twomey R, Amann M. Acute and chronic hypoxia: implications for cerebral function and exercise tolerance. Fatigue 2: 73-92, 2014. 10.1080/21641846.2014.909963.
38. Goodall S, Twomey R, Amann M, Ross EZ, Lovering AT, Romer LM, Subudhi AW, Roach RC. AltitudeOmics: exercise-induced supraspinal fatigue is attenuated in healthy humans after acclimatization to high altitude. Acta Physiol (Oxf) 210: 875-888, 2014. doi:10.1111/apha.12241.
39. Hultman E, Sjöholm H. Electromyogram, force and relaxation time during and after continuous electrical stimulation of human skeletal muscle in situ. J Physiol 339: 33-40, 1983. doi:10.1113/jphysiol.1983.sp014700.
40. Hunter SK, Butler JE, Todd G, Gandevia SC, Taylor JL. Supraspinal fatigue does not explain the sex difference in muscle fatigue of maximal contractions. J Appl Physiol (1985) 101: 1036-1044, 2006. doi:10.1152/japplphysiol.00103.2006.
41. Hunter SK, Todd G, Butler JE, Gandevia SC, Taylor JL. Recovery from supraspinal fatigue is slowed in old adults after fatiguing maximal isometric contractions. J Appl Physiol (1985) 105: 1199-1209, 2008. doi:10.1152/japplphysiol.01246.2007.
42. Hureau TJ, Olivier N, Millet GY, Meste O, Blain GM. Exercise performance is regulated during repeated sprints to limit the development of peripheral fatigue beyond a critical threshold. Exp Physiol 99: 951-963, 2014. doi:10.1113/expphysiol.2014.077974.
43. Jeffers R, Shave R, Ross E, Stevenson EJ, Goodall S. The effect of a carbohydrate mouth-rinse on neuromuscular fatigue following cycling exercise. Appl Physiol Nutr Metab 40: 557-564, 2015. doi:10.1139/apnm-2014-0393.
44. Jubeau M, Rupp T, Perrey S, Temesi J, Wuyam B, Levy P, Verges S, Millet GY. Changes in voluntary activation assessed by transcranial magnetic stimulation during prolonged cycling exercise. PLoS One 9: e89157, 2014. doi:10.1371/journal.pone.0089157.
45. Katayama K, Amann M, Pegelow DF, Jacques AJ, Dempsey JA. Effect of arterial oxygenation on quadriceps fatigability during isolated muscle exercise. Am J Physiol Regul Integr Comp Physiol 292: R1279-R1286, 2007. doi:10.1152/ajpregu.00554.2006.
46. Keller-Ross ML, Pereira HM, Pruse J, Yoon T, Schlinder-Delap B, Nielson KA, Hunter SK. Stressor-induced increase in muscle fatigability of young men and women is predicted by strength but not voluntary activation. J Appl Physiol (1985) 116: 767-778, 2014. doi:10.1152/japplphysiol.01129.2013.
47. Keller ML, Pruse J, Yoon T, Schlinder-Delap B, Harkins A, Hunter SK. Supraspinal fatigue is similar in men and women for a low-force fatiguing contraction. Med Sci Sports Exerc 43: 1873-1883, 2011. doi:10.1249/MSS.0b013e318216ebd4.
48. Kennedy DS, Fitzpatrick SC, Gandevia SC, Taylor JL. Fatigue-related firing of muscle nociceptors reduces voluntary activation of ipsilateral but not contralateral lower limb muscles. J Appl Physiol (1985) 118: 408-418, 2015. doi:10.1152/japplphysiol.00375.2014.
49. Kennedy DS, McNeil CJ, Gandevia SC, Taylor JL. Effects of fatigue on corticospinal excitability of the human knee extensors. Exp Physiol 101: 1552-1564, 2016. doi:10.1113/EP085753.
50. Kennedy DS, McNeil CJ, Gandevia SC, Taylor JL. Fatigue-related firing of distal muscle nociceptors reduces voluntary activation of proximal muscles of the same limb. J Appl Physiol (1985) 116: 385-394, 2014. doi:10.1152/japplphysiol.01166.2013.
51. Kennedy DS, McNeil CJ, Gandevia SC, Taylor JL. Firing of antagonist small-diameter muscle afferents reduces voluntary activation and torque of elbow flexors. J Physiol 591: 3591-3604, 2013. doi:10.1113/jphysiol.2012.248559.
52. Khan SI, Giesebrecht S, Gandevia SC, Taylor JL. Activity-dependent depression of the recurrent discharge of human motoneurones after maximal voluntary contractions. J Physiol 590: 4957-4969, 2012. doi: 10.1113/jphysiol.2012.235697.
53. Khan SI, Taylor JL, Gandevia SC. Unexpected factors affecting the excitability of human motoneurones in voluntary and stimulated contractions. J Physiol 594: 2707-2717, 2016. doi:10.1113/JP272164.
54. Klass M, Roelands B, Lévénez M, Fontenelle V, Pattyn N, Meeusen R, Duchateau J. Effects of noradrenaline and dopamine on supraspinal fatigue in well-trained men. Med Sci Sports Exerc 44: 2299-2308, 2012. doi:10.1249/MSS.0b013e318265f356.
55. Lattier G, Millet GY, Martin A, Martin V. Fatigue and recovery after high-intensity exercise part I: neuromuscular fatigue. Int J Sports Med 25: 450-456, 2004. doi:10.1055/s-2004-820939.
56. Lepers R, Maffiuletti NA, Rochette L, Brugniaux J, Millet GY. Neuromuscular fatigue during a long-duration cycling exercise. J Appl Physiol (1985) 92: 1487-1493, 2002. doi:10.1152/japplphysiol.00880.2001.
57. Martin PG, Weerakkody N, Gandevia SC, Taylor JL. Group III and IV muscle afferents differentially affect the motor cortex and motoneurones in humans. J Physiol 586: 1277-1289, 2008. doi:10.1113/jphysiol.2007.140426.
58. Martin V, Kerhervé H, Messonnier LA, Banfi JC, Geyssant A, Bonnefoy R, Féasson L, Millet GY. Central and peripheral contributions to neuromuscular fatigue induced by a 24-h treadmill run. J Appl Physiol (1985) 108: 1224-1233, 2010. doi:10.1152/japplphysiol.01202.2009.
59. McNeil CJ, Giesebrecht S, Gandevia SC, Taylor JL. Behaviour of the motoneurone pool in a fatiguing submaximal contraction. J Physiol 589: 3533-3544, 2011. doi:10.1113/jphysiol.2011.207191.
60. McNeil CJ, Giesebrecht S, Gandevia SC, Taylor JL. Behaviour of the motoneurone pool in a fatiguing submaximal contraction. J Physiol 589: 3533-3544, 2011. doi:10.1113/jphysiol.2011.207191.
61. McNeil CJ, Martin PG, Gandevia SC, Taylor JL. The response to paired motor cortical stimuli is abolished at a spinal level during human muscle fatigue. J Physiol 587: 5601-5612, 2009. doi:10.1113/jphysiol.2009.180968.
62. Millet GY, Lepers R. Alterations of neuromuscular function after prolonged running, cycling and skiing exercises. Sports Med 34: 105-116, 2004. doi:10.2165/00007256-200434020-00004.
63. Millet GY, Martin V, Maffiuletti NA, Martin A. Neuromuscular fatigue after a ski skating marathon. Can J Appl Physiol 28: 434-445, 2003. doi:10.1139/h03-032.
64. Millet GY, Muthalib M, Jubeau M, Laursen PB, Nosaka K. Severe hypoxia affects exercise performance independently of afferent feedback and peripheral fatigue. J Appl Physiol (1985) 112: 1335-1344, 2012. doi:10.1152/japplphysiol.00804.2011.
65. Millet GY, Tomazin K, Verges S, Vincent C, Bonnefoy R, Boisson RC, Gergelé L, Féasson L, Martin V. Neuromuscular consequences of an extreme mountain ultra-marathon. PLoS One 6: e17059, 2011. doi: 10.1371/journal.pone.0017059.
66. Minett GM, Duffield R. Is recovery driven by central or peripheral factors? A role for the brain in recovery following intermittent-sprint exercise. Front Physiol 5: 24, 2014. doi:10.3389/fphys.2014.00024.
67. Pageaux B, Marcora SM, Rozand V, Lepers R. Mental fatigue induced by prolonged self-regulation does not exacerbate central fatigue during subsequent whole-body endurance exercise. Front Hum Neurosci 9: 67, 2015. doi:10.3389/fnhum.2015.00067.
68. Périard JD, Christian RJ, Knez WL, Racinais S. Voluntary muscle and motor cortical activation during progressive exercise and passively induced hyperthermia. Exp Physiol 99: 136-148, 2014. doi:10.1113/expphysiol.2013.074583.
69. Périard JD, Girard O, Racinais S. Neuromuscular adjustments of the knee extensors and plantar flexors following match-play tennis in the heat. Br J Sports Med 48, Suppl 1: i45-i51, 2014. doi:10.1136/bjsports-2013-093160.
70. Perrey S, Racinais S, Saimouaa K, Girard O. Neural and muscular adjustments following repeated running sprints. Eur J Appl Physiol 109: 1027-1036, 2010. doi:10.1007/s00421-010-1445-3.
71. Peters EJ, Fuglevand AJ. Cessation of human motor unit discharge during sustained maximal voluntary contraction. Neurosci Lett 274: 66-70, 1999. doi:10.1016/S0304-3940(99)00666-7.
72. Place N, Lepers R, Deley G, Millet GY. Time course of neuromuscular alterations during a prolonged running exercise. Med Sci Sports Exerc 36: 1347-1356, 2004. doi:10.1249/01.MSS.0000135786.22996.77.
73. Prasartwuth O, Taylor JL, Gandevia SC. Maximal force, voluntary activation and muscle soreness after eccentric damage to human elbow flexor muscles. J Physiol 567: 337-348, 2005. doi:10.1113/jphysiol.2005.087767.
74. Racinais S, Girard O, Micallef JP, Perrey S. Failed excitability of spinal motoneurons induced by prolonged running exercise. J Neurophysiol 97: 596-603, 2007. doi:10.1152/jn.00903.2006.
75. Rampinini E, Bosio A, Ferraresi I, Petruolo A, Morelli A, Sassi A. Match-related fatigue in soccer players. Med Sci Sports Exerc 43: 2161-2170, 2011. doi:10.1249/MSS.0b013e31821e9c5c.
76. Rösler KM, Scheidegger O, Magistris MR. Corticospinal output and loss of force during motor fatigue. Exp Brain Res 197: 111-123, 2009. doi:10.1007/s00221-009-1897-z.
77. Ross EZ, Cotter JD, Wilson L, Fan JL, Lucas SJ, Ainslie PN. Cerebrovascular and corticomotor function during progressive passive hyperthermia in humans. J Appl Physiol (1985) 112: 748-758, 2012. doi:10.1152/japplphysiol.00988.2011.
78. Ross EZ, Goodall S, Stevens A, Harris I. Time course of neuromuscular changes during running in well-trained subjects. Med Sci Sports Exerc 42: 1184-1190, 2010.
79. Ross EZ, Gregson W, Williams K, Robertson C, George K. Muscle contractile function and neural control after repetitive endurance cycling. Med Sci Sports Exerc 42: 206-212, 2010. doi:10.1249/MSS.0b013e3181b07a18.
80. Ross EZ, Middleton N, Shave R, George K, Nowicky A. Corticomotor excitability contributes to neuromuscular fatigue following marathon running in man. Exp Physiol 92: 417-426, 2007. doi:10.1113/expphysiol.2006.035972.
81. Rossi A, Rossi S, Ginanneschi F. Activity-dependent changes in intrinsic excitability of human spinal motoneurones produced by natural activity. J Neurophysiol 108: 2473-2480, 2012. doi:10.1152/jn.00477.2012.
82. Rupp T, Mallouf TR, Perrey S, Wuyam B, Millet GY, Verges S. CO2 Clamping, Peripheral and Central Fatigue during Hypoxic Knee Extensions in Men. Med Sci Sports Exerc 47: 2513-2524, 2015. doi:10.1249/MSS.0000000000000724.
83. Sidhu SK, Bentley DJ, Carroll TJ. Locomotor exercise induces long-lasting impairments in the capacity of the human motor cortex to voluntarily activate knee extensor muscles. J Appl Physiol (1985) 106: 556-565, 2009. doi:10.1152/japplphysiol.90911.2008.
84. Sidhu SK, Cresswell AG, Carroll TJ. Corticospinal responses to sustained locomotor exercises: moving beyond single-joint studies of central fatigue. Sports Med 43: 437-449, 2013. doi:10.1007/s40279-013-0020-6.
85. Sidhu SK, Weavil JC, Venturelli M, Garten RS, Rossman MJ, Richardson RS, Gmelch BS, Morgan DE, Amann M. Spinal μ-opioid receptor-sensitive lower limb muscle afferents determine corticospinal responsiveness and promote central fatigue in upper limb muscle. J Physiol 592: 5011-5024, 2014. doi:10.1113/jphysiol.2014.275438.
86. Skof B, Strojnik V. Neuro-muscular fatigue and recovery dynamics following anaerobic interval workload. Int J Sports Med 27: 220-225, 2006. doi:10.1055/s-2005-865632.
87. Smith JL, Butler JE, Martin PG, McBain RA, Taylor JL. Increased ventilation does not impair maximal voluntary contractions of the elbow flexors. J Appl Physiol (1985) 104: 1674-1682, 2008. doi:10.1152/japplphysiol.01358.2007.
88. Smith JL, Martin PG, Gandevia SC, Taylor JL. Sustained contraction at very low forces produces prominent supraspinal fatigue in human elbow flexor muscles. J Appl Physiol (1985) 103: 560-568, 2007. doi:10.1152/japplphysiol.00220.2007.
89. Søgaard K, Gandevia SC, Todd G, Petersen NT, Taylor JL. The effect of sustained low-intensity contractions on supraspinal fatigue in human elbow flexor muscles. J Physiol 573: 511-523, 2006. doi:10.1113/jphysiol.2005.103598.
90. Stewart RD, Duhamel TA, Foley KP, Ouyang J, Smith IC, Green HJ. Protection of muscle membrane excitability during prolonged cycle exercise with glucose supplementation. J Appl Physiol (1985) 103: 331-339, 2007. doi:10.1152/japplphysiol.01170.2006.
91. Taylor JL, Allen GM, Butler JE, Gandevia SC. Supraspinal fatigue during intermittent maximal voluntary contractions of the human elbow flexors. J Appl Physiol (1985) 89: 305-313, 2000.
92. Taylor JL, Amann M, Duchateau J, Meeusen R, Rice CL. Neural contributions to muscle fatigue: from the brain to the muscle and back again. Med Sci Sports Exerc 48: 2294-2306, 2016. doi:10.1249/MSS.0000000000000923.
93. Taylor JL, Gandevia SC. A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol (1985) 104: 542-550, 2008. doi:10.1152/japplphysiol.01053.2007.
94. Temesi J, Arnal PJ, Davranche K, Bonnefoy R, Levy P, Verges S, Millet GY. Does central fatigue explain reduced cycling after complete sleep deprivation? Med Sci Sports Exerc 45: 2243-2253, 2013. doi:10.1249/MSS.0b013e31829ce379.
95. Temesi J, Rupp T, Martin V, Arnal PJ, Féasson L, Verges S, Millet GY. Central fatigue assessed by transcranial magnetic stimulation in ultratrail running. Med Sci Sports Exerc 46: 1166-1175, 2014. doi:10.1249/MSS.0000000000000207.
96. Thomas K, Elmeua M, Howatson G, Goodall S. Intensity-dependent contribution of neuromuscular fatigue after constant-load cycling. Med Sci Sports Exerc 48: 1751-1760, 2016. doi:10.1249/MSS.0000000000000950.
97. Thomas K, Goodall S, Stone M, Howatson G, St Clair Gibson A, Ansley L. Central and peripheral fatigue in male cyclists after 4-, 20-, and 40-km time trials. Med Sci Sports Exerc 47: 537-546, 2015. doi:10.1249/MSS.0000000000000448.
98. Todd G, Butler JE, Taylor JL, Gandevia SC. Hyperthermia: a failure of the motor cortex and the muscle. J Physiol 563: 621-631, 2005. doi:10.1113/jphysiol.2004.077115.
99. Todd G, Taylor JL, Gandevia SC. Measurement of voluntary activation based on transcranial magnetic stimulation over the motor cortex. J Appl Physiol (1985) 121: 678-686, 2016. doi:10.1152/japplphysiol.00293.2016.
100. Todd G, Taylor JL, Gandevia SC. Measurement of voluntary activation of fresh and fatigued human muscles using transcranial magnetic stimulation. J Physiol 551: 661-671, 2003. doi:10.1113/jphysiol.2003.044099.
101. Tomazin K, Morin JB, Strojnik V, Podpecan A, Millet GY. Fatigue after short (100-m), medium (200-m) and long (400-m) treadmill sprints. Eur J Appl Physiol 112: 1027-1036, 2012. doi:10.1007/s00421-011-2058-1.
102. Tupling R, Green H, Grant S, Burnett M, Ranney D. Postcontractile force depression in humans is associated with an impairment in SR Ca(2+) pump function. Am J Physiol Regul Integr Comp Physiol 278: R87-R94, 2000.
103. Westerblad H, Lännergren J. Slowing of relaxation during fatigue in single mouse muscle fibres. J Physiol 434: 323-336, 1991. doi:10.1113/jphysiol.1991.sp018472.
104. Yoon T, Schlinder-Delap B, Keller ML, Hunter SK. Supraspinal fatigue impedes recovery from a low-intensity sustained contraction in old adults. J Appl Physiol (1985) 112: 849-858, 2012. doi:10.1152/japplphysiol.00799.2011.
105. Yoon T, Schlinder Delap B, Griffith EE, Hunter SK. Mechanisms of fatigue differ after low- and high-force fatiguing contractions in men and women. Muscle Nerve 36: 515-524, 2007. doi:10.1002/mus.20844.
106. Zghal F, Cottin F, Kenoun I, Rebaï H, Moalla W, Dogui M, Tabka Z, Martin V. Improved tolerance of peripheral fatigue by the central nervous system after endurance training. Eur J Appl Physiol 115: 1401-1415, 2015. doi:10.1007/s00421-015-3123-y.