European Journal of Applied Physiology

, Volume 118, Issue 11, pp 2281–2293 | Cite as

Effects of endurance training on neuromuscular fatigue in healthy active men. Part I: Strength loss and muscle fatigue

  • J. Mira
  • S. J. Aboodarda
  • M. Floreani
  • R. Jaswal
  • S. J. Moon
  • K. Amery
  • T. Rupp
  • Guillaume Y. MilletEmail author
Original Article



The adaptations induced by endurance training on the neuromuscular function remain under investigation and, for methodological reasons, unclear. This study investigates the effects of cycling training on neuromuscular fatigue and its peripheral contribution measured during and immediately after cycling exercise.


Fourteen healthy men performed a fatigue test before a 9-week cycling program (PRE) and two tests after training: at the same absolute power output as PRE (POSTABS) and based on the post-training maximal aerobic power (POSTREL). Throughout the tests and at exhaustion (EXH), maximal voluntary contraction (MVC) and peripheral fatigue were assessed in the quadriceps muscle by electrical nerve stimulation [single twitch (Pt); high-frequency doublet (Db100) and low-to-high-frequency ratio (Db10:100)].


Time to EXH was longer in POSTABS than PRE (34 ± 5 vs. 27 ± 4 min, P < 0.001), and POSTREL tended to be longer than PRE (30 ± 6 min, P = 0.053). MVC and peripheral fatigue were overall less depressed in POSTABS than PRE at isotime. At EXH, MVC and Db10:100 were similarly reduced in all sessions (–37 to − 42% and − 30 to − 37%, respectively). Db100 tended to be less depressed in POSTABS than PRE (–40 ± 9 vs. − 48 ± 16%, P = 0.050) and in POSTREL than PRE (–39 ± 9%, P = 0.071). Pt decreased similarly in POSTABS and PRE (–52 ± 16 vs. − 54 ± 16%), but POSTREL tended to be less depressed than PRE (–48 ± 14%, P = 0.075).


This study confirms fatigue attenuation at isotime after training. Yet lower or similar fatigue at EXH indicates that, unlike previously suggested, fatigue tolerance may not be upregulated after 9 weeks of cycling training.


Aerobic training Excitation–contraction coupling failure Neuromuscular function Peripheral fatigue 



Constant-load submaximal training


Low-frequency doublet


Low-frequency fatigue


High-frequency doublet


Excitation–contraction coupling




Gas exchange threshold


High-intensity interval training


Heart rate




Maximal voluntary contraction


Neuromuscular fatigue


Fatigue session based on the same absolute power output as before training


Fatigue session based on the same relative intensity as before training


Initial fatigue test


Peak twitch


Respiratory compensation point


Rate of perceived exertion


Sarco(endo)plasmic reticulum Ca2+ ATPase


Transcranial magnetic stimulation


Time to exhaustion



\(\dot {V}\)CO2

CO2 output

\(\dot {V}\)E

Minute ventilation

\(\dot {V}\)E/\(\dot {V}\)CO2

Ventilatory equivalent of V̇CO2

\(\dot {V}\)O2max

Maximal oxygen uptake

\(\dot {V}\)O2peak

Peak \(\dot {V}\)O2


Maximal aerobic power output


Author contribution statement

TR, GYM, SJA, and JM conceived and designed the research. SJA, JM, MF, RJ, SJM, and KA conducted the experiment and analyzed data. JM wrote the manuscript. All authors read and approved the manuscript.


This study was supported by the Université Savoie Mont Blanc as part of the doctoral work of José Mira. Saied Jalal Aboodarda was funded by the Eyes High Postdoctoral Scholars.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.


  1. Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88:287–332. PubMedCrossRefGoogle Scholar
  2. Astorino TA, Schubert MM (2014) Individual responses to completion of short-term and chronic interval training: a retrospective study. PLoS One. PubMedPubMedCentralCrossRefGoogle Scholar
  3. Beaver WL, Wasserman K, Whipp BJ (2012) A new method for detecting anaerobic threshold by gas exchange a new method for detecting threshold by gas exchange anaerobic. J Appl Physiol 60:2020–2027CrossRefGoogle Scholar
  4. Berger NJA, Tolfrey K, Williams AG, Jones AM (2006) Influence of continuous and interval training on oxygen uptake on-kinetics. Med Sci Sports Exerc 38:504–512. PubMedCrossRefGoogle Scholar
  5. Burnley M, Vanhatalo A, Jones AM (2012) Distinct profiles of neuromuscular fatigue during muscle contractions below and above the critical torque in humans. J Appl Physiol 113:215–223. PubMedCrossRefGoogle Scholar
  6. Daussin FN, Zoll J, Dufour SP et al (2008) Effect of interval versus continuous training on cardiorespiratory and mitochondrial functions: relationship to aerobic performance improvements in sedentary subjects. AJP Regul Integr Comp Physiol 295:R264–R272. CrossRefGoogle Scholar
  7. Doyle-Baker D, Temesi J, Medysky ME et al (2017) An innovative ergometer to measure neuromuscular fatigue immediately after cycling. Med Sci Sport Exerc. CrossRefGoogle Scholar
  8. Goodall S, González-Alonso J, Ali L et al (2012) Supraspinal fatigue after normoxic and hypoxic exercise in humans. J Physiol 590:2767–2782. PubMedPubMedCentralCrossRefGoogle Scholar
  9. Gruet M, Temesi J, Rupp T et al (2014) Dynamics of corticospinal changes during and after a high-intensity quadriceps exercise. Exp Physiol 8:1–27. CrossRefGoogle Scholar
  10. Gunnarsson TP, Christensen PM, Thomassen M et al (2013) Effect of intensified training on muscle ion kinetics, fatigue development, and repeated short-term performance in endurance-trained cyclists. AJP Regul Integr Comp Physiol 305:R811–R821. CrossRefGoogle Scholar
  11. Jenkins DG, Quigley B (1992) Endurance training enhances critical power. Med Sci Sport Exerc 24:1283–1289CrossRefGoogle Scholar
  12. Jones AM, Wilkerson DP, DiMenna F et al (2008) Muscle metabolic responses to exercise above and below the “critical power” assessed using 31P-MRS. Am J Physiol Regul Integr Comp Physiol 294:R585–R593. PubMedCrossRefGoogle Scholar
  13. Laursen PB, Jenkins DG (2002) The scientific basis for high-intensity interval training: optimising training programmes and maximising performance in highly trained endurance athletes. Sports Med 32:53–73. PubMedCrossRefGoogle Scholar
  14. Lepers R, Maffiuletti N, Rochette L et al (2002) Neuromuscular fatigue during a long-duration cycling exercise. J Appl Physiol 92:1487–1493. PubMedCrossRefGoogle Scholar
  15. MacInnis MJ, Zacharewicz E, Martin BJ et al (2017) Superior mitochondrial adaptations in human skeletal muscle after interval compared to continuous single-leg cycling matched for total work. J Physiol 595:2955–2968. PubMedCrossRefGoogle Scholar
  16. MacIntosh BR, Rassier DE (2002) What is fatigue? Can J Appl Physiol 27:42–55PubMedCrossRefGoogle Scholar
  17. Majerczak J, Karasinski J, Zoladz JA (2008) Training induced decrease in oxygen cost of cycling is accompanied by down-regulation of serca expression in human vastus lateralis muscle. J Physiol Pharmacol 59:589–602PubMedGoogle Scholar
  18. Marcora SM, Staiano W (2010) The limit to exercise tolerance in humans: mind over muscle? Eur J Appl Physiol 109:763–770. PubMedCrossRefGoogle Scholar
  19. McKenzie S, Phillips SM, Carter SL et al (2000) Endurance exercise training attenuates leucine oxidation and BCOAD activation during exercise in humans. Am J Physiol Endocrinol Metab 278:E580–E587PubMedCrossRefGoogle Scholar
  20. Milanović Z, Sporiš G, Weston M (2015) Effectiveness of high-intensity interval training (HIT) and continuous endurance training for VO2max improvements: a systematic review and meta-analysis of controlled trials. Sport Med 45:1469–1481. CrossRefGoogle Scholar
  21. Millet GY (2011) Can neuromuscular fatigue explain running strategies and performance in ultra-marathons? The flush model. Sport Med 41:489–506CrossRefGoogle Scholar
  22. Mira J, Lapole T, Souron R et al (2017) Cortical voluntary activation testing methodology impacts central fatigue. Eur J Appl Physiol. PubMedCrossRefGoogle Scholar
  23. Murias JM, Edwards JA, Paterson DH (2016) Effects of short-term training and detraining on VO2 kinetics: faster VO2 kinetics response after one training session. Scand J Med Sci Sports 26:620–629PubMedCrossRefGoogle Scholar
  24. Noble B, Borg G, Jacobs I et al (1983) A category-ratio perceived exertion scale: relationship to blood and muscle lactates and heart rate. Med Sci Sport Exerc 15:523–528Google Scholar
  25. O’Leary TJ, Collett J, Howells K, Morris MG (2017) Endurance capacity and neuromuscular fatigue following high vs moderate-intensity endurance training: a randomised trial. Scand J Med Sci Sports. PubMedCrossRefGoogle Scholar
  26. Pilegaard H, Domino K, Noland T et al (2012) Effect of high-intensity exercise training on lactate / H + transport capacity in human skeletal muscle. Am J Physiol Endocrinol Metab 276:255–261CrossRefGoogle Scholar
  27. Seiler S, Jøranson K, Olesen BV, Hetlelid KJ (2013) Adaptations to aerobic interval training: Interactive effects of exercise intensity and total work duration. Scand J Med Sci Sport 23:74–83. CrossRefGoogle Scholar
  28. Sinoway LI (1996) Neural responses to exercise in humans: Implications for congestive heart failure. Clin Exp Pharmacol Physiol 23:693–699PubMedCrossRefGoogle Scholar
  29. Stapelfeldt B, Mornieux G, Oberheim R et al (2007) Development and evaluation of a new bicycle instrument for measurements of pedal forces and power output in cycling. Int J Sports Med 28:326–332. PubMedCrossRefGoogle Scholar
  30. Temesi J, Rupp T, Martin V et al (2014) Central fatigue assessed by transcranial magnetic stimulation in ultratrail running. Med Sci Sports Exerc 46(6):1166–1175PubMedCrossRefGoogle Scholar
  31. Temesi J, Maturana FM, Peyrard A et al (2017) The relationship between oxygen uptake kinetics and neuromuscular fatigue in high-intensity cycling exercise. Eur J Appl Physiol 117(5):969–978PubMedCrossRefGoogle Scholar
  32. Vila-Cha C, Falla D, Correia MV, Farina D (2012) Changes in H reflex and V wave following short-term endurance and strength training. J Appl Physiol 112:54–63. PubMedCrossRefGoogle Scholar
  33. Vila-Chã C, Falla D, Farina D (2010) Motor unit behavior during submaximal contractions following six weeks of either endurance or strength training. J Appl Physiol 109:1455–1466. PubMedCrossRefGoogle Scholar
  34. Vila-Chã C, Falla D, Correia MV, Farina D (2012) Adjustments in motor unit properties during fatiguing contractions after training. Med Sci Sports Exerc 44:616–624. PubMedCrossRefGoogle Scholar
  35. Warburton DER, Haykowsky MJ, Quinney HA et al (2004) Blood volume expansion and cardiorespiratory function: Effects of training modality. Med Sci Sports Exerc 36:991–1000. PubMedCrossRefGoogle Scholar
  36. Whipp BJ, Davis JA, Wasserman K (1989) Ventilatory control of the “isocapnic buffering” region in rapidly-incremental exercise. Respir Physiol 76:357–367. PubMedCrossRefGoogle Scholar
  37. Zghal F, Cottin F, Kenoun I et al (2015) Improved tolerance of peripheral fatigue by the central nervous system after endurance training. Eur J Appl Physiol 115:1401–1415. PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • J. Mira
    • 1
    • 2
  • S. J. Aboodarda
    • 1
  • M. Floreani
    • 1
    • 3
  • R. Jaswal
    • 1
  • S. J. Moon
    • 1
  • K. Amery
    • 1
  • T. Rupp
    • 2
  • Guillaume Y. Millet
    • 1
    Email author
  1. 1.Human Performance Laboratory, Faculty of KinesiologyUniversity of CalgaryCalgaryCanada
  2. 2.Laboratoire Interuniversitaire de Biologie de la MotricitéUniversité Savoie Mont BlancChambéryFrance
  3. 3.Department of Medical and Biological SciencesUniversity of UdineUdineItaly

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