Top

Published in:

01-11-2018 | Original Article

Effects of endurance cycling training on neuromuscular fatigue in healthy active men. Part II: Corticospinal excitability and voluntary activation

Authors: S. J. Aboodarda, J. Mira, M. Floreani, R. Jaswal, S. J. Moon, K. Amery, T. Rupp, G. Y. Millet

Published in: European Journal of Applied Physiology | Issue 11/2018

Abstract

This study investigated the effects of 9-week endurance cycling training on central fatigability and corticomotor excitability of the locomotor muscles. Fourteen healthy participants undertook three incremental fatiguing cycling tests to volitional exhaustion (EXH): (i) before training (PRE), (ii) after training at the same absolute power output as PRE (POST_ABS) and (iii) after training at the same percentage of V̇O_2max as PRE (POST_REL). At baseline (i.e. before cycling), every 5 min during cycling and immediately at EXH, a neuromuscular evaluation including a series of 5-s knee extensions at 100, 75 and 50% of maximal voluntary knee extension (MVC) was performed. During each contraction, transcranial magnetic and peripheral nerve stimuli were elicited to obtain motor evoked potential (MEP), silent period (SP) and compound muscle action potential (Mmax) and to calculate voluntary activation (VA). The MEP·Mmax⁻¹ ratio recorded from vastus lateralis at 100 and 50% MVC did not show any difference between conditions. At 75% MVC, MEP exhibited significantly lower values in POST_ABS and POST_REL compared to PRE at baseline (P = 0.022 and P = 0.011, respectively) as well as at 25% of time to EXH of PRE (P = 0.022) for POST_REL. No adaptations, either at baseline or during cycling, were observed for VA and SPs. In conclusion, endurance training may result in some adaptations in the corticomotor responses when measured at rest or with low level of fatigue, yet these adaptations do not translate into attenuation of central fatigue at a similar cycling workload or at exhaustion.

Behrens M, Weippert M, Wassermann F, Bader R, Bruhn S, Mau-Moeller A (2015) Neuromuscular function and fatigue resistance of the plantar flexors following short-term cycling endurance training. Front Physiol 6:145. https://doi.org/10.3389/fphys.2015.00145 PubMedPubMedCentralCrossRef

Carroll TJ, Riek S, Carson RG (2002) The sites of neural adaptation induced by resistance training in humans. J Physiol 15(544):641–652CrossRef

Carroll TJ, Barton J, Hsu M, Lee M (2009) The effect of strength training on the force of twitches evoked by corticospinal stimulation in humans. Acta Physiol 197(2):161–173. https://doi.org/10.1111/j.1748-1716.2009.01992.x CrossRef

Daussin FN, Zoll J, Dufour SP, Ponsot E, Lonsdorfer-Wolf E, Doutreleau S, Mettauer B, Piquard F, Geny B, Richard R (2008) Effect of interval versus continuous training on cardiorespiratory and mitochondrial functions: relationship to aerobic performance improvements in sedentary subjects. Am J Physiol Regul Integr Comp Physiol 295(1):R264–R272. https://doi.org/10.1152/ajpregu.00875.2007 PubMedCrossRef

Doyle-Baker D, Temesi J, Medysky ME, Holash RJ, Millet GY (2018) An innovative ergometer to measure neuromuscular fatigue immediately after cycling. Med Sci Sports Exerc 50(2):375–387. https://doi.org/10.1249/MSS.0000000000001427 PubMedCrossRef

Edge J, Bishop D, Goodman C (2006) The effects of training intensity on muscle buffer capacity in females. Eur J Appl Physiol 96:97–105. https://doi.org/10.1007/s00421-005-0068-6 PubMedCrossRef

Falvo MJ, Sirevaag EJ, Rohrbaugh JW, Earhart GM (2010) Resistance training induces supraspinal adaptations: evidence from movement-related cortical potentials. Eur J Appl Physiol 109(5):923–933. https://doi.org/10.1007/s00421-010-1432-8 PubMedPubMedCentralCrossRef

Gandevia SC, Allen GM, Butler JE, Taylor JL (1996) Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex. J Physiol 15(490):529–536CrossRef

Gandevia SC, Petersen N, Butler JE, Taylor JL (1999) Impaired response of human motoneurones to corticospinal stimulation after voluntary exercise. J Physiol 15:749–759CrossRef

Goodall S, González-Alonso J, Ali L, Ross EZ, Romer LM (2012) Supraspinal fatigue after normoxic and hypoxic exercise in humans. J Physiol 590(11):2767–2782. https://doi.org/10.1113/jphysiol.2012.228890 CrossRef

Gruet M, Temesi J, Rupp T, Levy P, Millet GY, Verges S (2013) Stimulation of the motor cortex and corticospinal tract to assess human muscle fatigue. Neuroscience 12(231):384–399. https://doi.org/10.1016/j.neuroscience.2012.10.058 CrossRef

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. https://doi.org/10.1152/ajpregu.00467.2012 CrossRef

Hunter SK, Todd G, Butler JE, Gandevia SC, Taylor JL (2008) Recovery from supraspinal fatigue is slowed in old adults after fatiguing maximal isometric contractions. J Appl Physiol 105(4):1199–1209. https://doi.org/10.1152/japplphysiol.01246.2007 PubMedCrossRef

Jensen JL, Marstrand PC, Nielsen JB (2005) Motor skill training and strength training are associated with different plastic changes in the central nervous system. J Appl Physiol 99(4):1558–1568PubMedCrossRef

Jones AM, Carter H (2000) The effect of endurance training on parameters of aerobic fitness. Sports Med 29(6):373–386PubMedCrossRef

Jubeau M, Rupp T, Perrey S, Temesi J, Wuyam B, Levy P, Verges S, Millet GY (2014) Changes in voluntary activation assessed by transcranial magnetic stimulation during prolonged cycling exercise. PLoS One 21 9(2):e89157. https://doi.org/10.1371/journal.pone.0089157 PubMedPubMedCentralCrossRef

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. https://doi.org/10.2165/00007256-200232010-00003 PubMedCrossRef

Le Pera D, Graven-Nielsen T, Valeriani M, Oliviero A, Di Lazzaro V, Tonali PA, Arendt-Nielsen L (2001) Inhibition of motor system excitability at cortical and spinal level by tonic muscle pain. Clin Neurophysiol 112(9):1633–1641PubMedCrossRef

Mira J, Lapole T, Souron R, Messonnier L, Millet GY, Rupp T (2017) Cortical voluntary activation testing methodology impacts central fatigue. Eur J Appl Physiol 117(9):1845–1857. https://doi.org/10.1007/s00421-017-3678-x PubMedCrossRef

Murias JM, Kowalchuk JM, Paterson DH (2010a) Speeding of V̇O₂ kinetics with endurance training in old and young men is associated with improved matching of local O₂ delivery to muscle O₂ utilization. J Appl Physiol 108(4):913–922. https://doi.org/10.1152/japplphysiol.01355.2009 PubMedPubMedCentralCrossRef

Murias JM, Kowalchuk JM, Paterson DH (2010b) Time course and mechanisms of adaptations in cardiorespiratory fitness with endurance training in older and young men. J Appl Physiol 108(3):621–627. https://doi.org/10.1152/japplphysiol.01152.2009 PubMedCrossRef

Murias JM, Kowalchuk JM, Ritchie D, Hepple RT, Doherty TJ, Paterson DH (2011) Adaptations in capillarization and citrate synthase activity in response to endurance training in older and young men. J Gerontol A Biol Sci Med Sci 66(9):957–964. https://doi.org/10.1093/gerona/glr096 PubMedCrossRef

Nybo L, Secher NH (2004) Cerebral perturbations provoked by prolonged exercise. Prog Neurobiol 72:223–261PubMedCrossRef

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 27(12):1648–1661. https://doi.org/10.1111/sms.12854 CrossRef

Perot C, Goubel F, Mora I (1991) Quantification of T- and H-responses before and after a period of endurance training. Eur J Appl Physiol 63:368–375CrossRef

Rossi S, Hallett M, Rossini PM, Pascual-Leone A (2011) Screening questionnaire before TMS: an update. Clin Neurophysiol 122(8):1686. https://doi.org/10.1016/j.clinph.2010.12.037 PubMedCrossRef

Schnitzler A, Benecke R (1994) The silent period after transcranial magnetic stimulation is of exclusive cortical origin: evidence from isolated cortical ischemic lesions in man. Neurosci Lett 180(1):41–45PubMedCrossRef

Sidhu SK, Bentley DJ, Carroll TJ (2009) Locomotor exercise induces long-lasting impairments in the capacity of the human motor cortex to voluntarily activate knee extensor muscles. J Appl Physiol 106(2):556–565. https://doi.org/10.1152/japplphysiol.90911.2008 PubMedCrossRef

Sidhu SK, Weavil JC, Mangum TS, Jessop JE, Richardson RS, Morgan DE, Amann M (2017) Group III/IV locomotor muscle afferents alter motor cortical and corticospinal excitability and promote central fatigue during cycling exercise. Clin Neurophysiol 128(1):44–55. https://doi.org/10.1016/j.clinph.2016.10.008 PubMedCrossRef

Sinoway L (1996) Neural responses to exercise in humans: implications for congestive heart failure. Clin Exp Pharmacol Physiol 23(8):693–699PubMedCrossRef

Strojnik V, Komi PV (1998) Neuromuscular fatigue after maximal stretch-shortening cycle exercise. J Appl Physiol 84(1):344–350PubMedCrossRef

Svensson P, Miles TS, McKay D, Ridding MC (2003) Suppression of motor evoked potentials in a hand muscle following prolonged painful stimulation. Eur J Pain 7(1):55–62PubMedCrossRef

Taylor JL, Petersen NT, Butler JE, Gandevia SC (2002) Interaction of transcranial magnetic stimulation and electrical transmastoid stimulation in human subjects. J Physiol 15:949–958CrossRef

Taylor JL, Todd G, Gandevia SC (2006) Evidence for a supraspinal contribution to human muscle fatigue. Clin Exp Pharmacol Physiol 33(4):400–405PubMedCrossRef

Taylor JL, Amann M, Duchateau J, Meeusen R, Rice CL (2016) Neural contributions to muscle fatigue: from the brain to the muscle and back again. Med Sci Sports Exerc 48(11):2294–2306PubMedPubMedCentralCrossRef

Temesi J, Rupp T, Martin V, Arnal PJ, Féasson L, Verges S, Millet GY (2014) Central fatigue assessed by transcranial magnetic stimulation in ultratrail running. Med Sci Sports Exerc 46(6):1166–1175. https://doi.org/10.1249/MSS.0000000000000207 PubMedCrossRef

Todd G, Taylor JL, Gandevia SC (2003) Measurement of voluntary activation of fresh and fatigued human muscles using transcranial magnetic stimulation. J Physiol 551:661–671PubMedPubMedCentralCrossRef

Todd G, Taylor JL, Gandevia SC (2004) Reproducible measurement of voluntary activation of human elbow flexors with motor cortical stimulation. J Appl Physiol 97:236–242PubMedCrossRef

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. https://doi.org/10.1249/01.MSS.0000128163.88298 PubMedCrossRef

Weavil JC, Sidhu SK, Mangum TS, Richardson RS, Amann M (2016) Fatigue diminishes motoneuronal excitability during cycling exercise. J Neurophysiol 116(4):1743–1751. https://doi.org/10.1152/jn.00300.2016 PubMedPubMedCentralCrossRef

Zghal F, Cottin F, Kenoun I, Rebaï H, Moalla W, Dogui M, Tabka Z, Martin V (2015) Improved tolerance of peripheral fatigue by the central nervous system after endurance training. Eur J Appl Physiol 115(7):1401–1415. https://doi.org/10.1007/s00421-015-3123-y PubMedCrossRef

Title: Effects of endurance cycling training on neuromuscular fatigue in healthy active men. Part II: Corticospinal excitability and voluntary activation
Authors: S. J. Aboodarda
J. Mira
M. Floreani
R. Jaswal
S. J. Moon
K. Amery
T. Rupp
G. Y. Millet
Publication date: 01-11-2018
Publisher: Springer Berlin Heidelberg
Published in: European Journal of Applied Physiology / Issue 11/2018
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-018-3951-7

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Effects of endurance cycling training on neuromuscular fatigue in healthy active men. Part II: Corticospinal excitability and voluntary activation

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 11/2018

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

Mental fatigue does not alter performance or neuromuscular fatigue development during self-paced exercise in recreationally trained cyclists

Differences in elbow extensor muscle characteristics between resistance-trained men and women

Effect of 1-week betalain-rich beetroot concentrate supplementation on cycling performance and select physiological parameters

Swimming versus running: effects on exhaled breath condensate pro-oxidants and pH

Age-related attenuation of conduit artery blood flow response to passive heating differs between the arm and leg