Abstract
Purpose
The purposes of this study were to evaluate the effect of endurance training on central fatigue development and recovery.
Methods
A control group was compared to a training group, which followed an 8-week endurance-training program, consisting in low-force concentric and isometric contractions. Before (PRE) and after (POST) the training period, neuromuscular function of the knee extensor (KE) muscles was evaluated before, immediately after and during 33 min after an exhausting submaximal isometric task at 15 % of the maximal voluntary contraction (MVC) force. After training, the trained group performed another test at iso-time, i.e., with the task maintained until the duration completed before training was matched (POST2). The evaluation of neuromuscular function consisted in the determination of the voluntary activation level during MVCs, from peripheral nerve electrical (VAPNS) and transcranial magnetic stimulations (VATMS). The amplitude of the potentiated twitch (Pt), the evoked [motor evoked potentials, cortical silent period (CSP)] and voluntary EMG activities were also recorded on the KE muscles.
Results
Before training, the isometric task induced significant reductions of VAPNS, VATMS and Pt, and an increased CSP. The training period induced a threefold increase of exercise duration, delayed central fatigue appearance, as illustrated by the absence of modification of VAPNS, VATMS and CSP after POST2. At POST, central fatigue magnitude and recovery were not modified but Pt reduction was greater.
Conclusion
These results suggest that central fatigue partially adapts to endurance training. This adaptation principally translates into improved tolerance of peripheral fatigue by the central nervous system.
Similar content being viewed by others
Abbreviations
- Ag:
-
Silver
- AgCl:
-
Silver chloride
- ANOVA:
-
Analysis of variance
- BF:
-
Biceps femoris
- CSP:
-
Cortical silent period
- EMG:
-
Electromyography
- KE muscles:
-
Knee extensor muscles
- Mmax :
-
Maximal muscle compound action potential
- M-wave:
-
Muscle compound action potential
- MEP:
-
Motor evoked potential
- MEP·M −1max :
-
Normalized motor evoked potential
- MVC:
-
Maximal voluntary contraction
- PNS:
-
Peripheral nerve stimulation
- PRE:
-
Before training
- PRE EX:
-
Measurement before exercise
- POST:
-
After training
- POST2:
-
After training; denotes the exercise with a duration equal to the exercise conducted at PRE
- POST EX:
-
Measurement after exercise
- Pt:
-
Amplitude of the potentiated twitch
- RF:
-
Rectus femoris
- RM:
-
Maximal repetition
- RMS:
-
Root mean square
- RMS·M −1max :
-
Normalized voluntary EMG activity
- RPE:
-
Rating of perceived exertion
- TMS:
-
Transcranial magnetic stimulation
- VAPNS :
-
Voluntary activation level measured from peripheral nerve stimulation
- VATMS :
-
Voluntary activation level measured from transcranial magnetic stimulation
- VL:
-
Vastus lateralis
- VM:
-
Vastus medialis
References
Amann M, Dempsey JA (2008) Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance. J Physiol 586(1):161–173. doi:10.1113/jphysiol.2007.141838
Amann M, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA (2009) Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. J Physiol 587(Pt 1):271–283. doi:10.1113/jphysiol.2008.163303
Amann M, Blain GM, Proctor LT, Sebranek JJ, Pegelow DF, Dempsey JA (2011) Implications of group III and IV muscle afferents for high-intensity endurance exercise performance in humans. J Physiol 589(Pt 21):5299–5309. doi:10.1113/jphysiol.2011.213769
Bigland-Ritchie B, Johansson R, Lippold OC, Woods JJ (1983) Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. J Neurophysiol 50(1):313–324
Blangsted AK, Sjogaard G, Madeleine P, Olsen HB, Sogaard K (2005) Voluntary low-force contraction elicits prolonged low-frequency fatigue and changes in surface electromyography and mechanomyography. J Electromyogr Kinesiol 15(2):138–148. doi:10.1016/j.jelekin.2004.10.004
Borg G (1998) Perceived exertion and pain rating scales. Human Kinetics, Champaign
Bosquet L, Montpetit J, Arvisais D, Mujika I (2007) Effects of tapering on performance: a meta-analysis. Med Sci Sports Exerc 39(8):1358–1365. doi:10.1249/mss.0b013e31806010e0
Burke D (2002) Effects of activity on axonal excitability: implications for motor control studies. Adv Exp Med Biol 508:33–37
Damron LA, Dearth DJ, Hoffman RL, Clark BC (2008) Quantification of the corticospinal silent period evoked via transcranial magnetic stimulation. J Neurosci Methods 173(1):121–128. doi:10.1016/j.jneumeth.2008.06.001
Enoka RM, Stuart DG (1992) Neurobiology of muscle fatigue. J Appl Physiol 72(5):1631–1648
Goodall S, Gonzalez-Alonso J, Ali L, Ross EZ, Romer LM (2012) Supraspinal fatigue after normoxic and hypoxic exercise in humans. J Physiol 590(Pt 11):2767–2782. doi:10.1113/jphysiol.2012.228890
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 231:384–399. doi:10.1016/j.neuroscience.2012.10.058
Hermens HJ, Freriks B, Merletti R, Hagg G, Stegeman D, Blok J, Rau G, Disselhorst-Klug C (1999) SENIAM 8: European recommendations for surface electromyography. Roessingh Research and Development, Enschede
Holloszy JO, Coyle EF (1984) Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J Appl Physiol Respir Environ Exerc Physiol 56(4):831–838
Jones DA (1996) High-and low-frequency fatigue revisited. Acta Physiol Scand 156(3):265–270
Jubeau M, Zory R, Gondin J, Martin A, Maffiuletti NA (2007) Effect of electrostimulation training-detraining on neuromuscular fatigue mechanisms. Neurosci Lett 424(1):41–46. doi:10.1016/j.neulet.2007.07.018
Kalmar JM, Cafarelli E (2004) Central fatigue and transcranial magnetic stimulation: effect of caffeine and the confound of peripheral transmission failure. J Neurosci Methods 138(1–2):15–26. doi:10.1016/j.jneumeth.2004.03.006
Kaufman MP, Hayes SG, Adreani CM, Pickar JG (2002) Discharge properties of group III and IV muscle afferents. Adv Exp Med Biol 508:25–32
Lattier G, Millet GY, Martin A, Martin V (2004) Fatigue and recovery after high-intensity exercise. Part II: recovery interventions. Int J Sports Med 25(7):509–515. doi:10.1055/s-2004-820946
Lee M, Gandevia SC, Carroll TJ (2009) Unilateral strength training increases voluntary activation of the opposite untrained limb. Clin Neurophysiol 120(4):802–808. doi:10.1016/j.clinph.2009.01.002
Li JL, Wang XN, Fraser SF, Carey MF, Wrigley TV, McKenna MJ (2002) Effects of fatigue and training on sarcoplasmic reticulum Ca(2 +) regulation in human skeletal muscle. J Appl Physiol 92(3):912–922. doi:10.1152/japplphysiol.00643.2000
Martin V, Millet GY, Martin A, Deley G, Lattier G (2004) Assessment of low-frequency fatigue with two methods of electrical stimulation. J Appl Physiol 97(5):1923–1929. doi:10.1152/japplphysiol.00376.2004
Martin V, Kerherve H, Messonnier LA, Banfi JC, Geyssant A, Bonnefoy R, Feasson L, Millet GY (2010) Central and peripheral contributions to neuromuscular fatigue induced by a 24-h treadmill run. J Appl Physiol 108(5):1224–1233. doi:10.1152/japplphysiol.01202.2009
Mathis J, de Quervain D, Hess CW (1998) Dependence of the transcranially induced silent period on the ‘instruction set’ and the individual reaction time. Electroencephalogr Clin Neurophysiol 109(5):426–435
Merletti R (1999) Standards for reporting EMG data. J Electromyogr Kinesiol 9(1):3–4
Merletti R, Botter A, Troiano A, Merlo E, Minetto MA (2009) Technology and instrumentation for detection and conditioning of the surface electromyographic signal: state of the art. Clin Biomech 24(2):122–134. doi:10.1016/j.clinbiomech.2008.08.006
Merton PA (1954) Voluntary strength and fatigue. J Physiol 123(3):553–564
Michaut A, Babault N, Pousson M (2004) Specific effects of eccentric training on muscular fatigability. Int J Sports Med 25(4):278–283
Millet GY (2011) Can neuromuscular fatigue explain running strategies and performance in ultra-marathons?: the flush model. Sports Med 41(6):489–506. doi:10.2165/11588760-000000000-00000
Millet GY, Martin V, Lattier G, Ballay Y (2003) Mechanisms contributing to knee extensor strength loss after prolonged running exercise. J Appl Physiol 94(1):193–198. doi:10.1152/japplphysiol.00600.2002
Noakes TD, St Clair Gibson A, Lambert EV (2005) From catastrophe to complexity: a novel model of integrative central neural regulation of effort and fatigue during exercise in humans: summary and conclusions. Br J Sports Med 39(2):120–124
Rupp T, Jubeau M, Wuyam B, Perrey S, Levy P, Millet GY, Verges S (2012) Time-dependent effect of acute hypoxia on corticospinal excitability in healthy humans. J Neurophysiol 108(5):1270–1277. doi:10.1152/jn.01162.2011
Sidhu SK, Bentley DJ, Carroll TJ (2009a) Cortical voluntary activation of the human knee extensors can be reliably estimated using transcranial magnetic stimulation. Muscle Nerve 39(2):186–196. doi:10.1002/mus.21064
Sidhu SK, Bentley DJ, Carroll TJ (2009b) 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. doi:10.1152/japplphysiol.90911.2008
Sinoway LI (1996) Neural responses to exercise in humans: implications for congestive heart failure. Clin Exp Pharmacol Physiol 23(8):693–699
Sinoway LI, Rea RF, Smith M, Mark AL (1989) Physical training induces desensitisation of muscle metaboreflex. Circ 80 (Suppl. II):290
Skurvydas A, Dudoniene V, Kalvenas A, Zuoza A (2002) Skeletal muscle fatigue in long-distance runners, sprinters and untrained men after repeated drop jumps performed at maximal intensity. Scand J Med Sci Sports 12(1):34–39
Sogaard K, Gandevia SC, Todd G, Petersen NT, Taylor JL (2006) The effect of sustained low-intensity contractions on supraspinal fatigue in human elbow flexor muscles. J Physiol 573(Pt 2):511–523. doi:10.1113/jphysiol.2005.103598
Taylor JL, Gandevia SC (2008) A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions. J Appl Physiol 104(2):542–550. doi:10.1152/japplphysiol.01053.2007
Todd G, Taylor JL, Gandevia SC (2003) Measurement of voluntary activation of fresh and fatigued human muscles using transcranial magnetic stimulation. J Physiol 551(Pt 2):661–671
Todd G, Taylor JL, Gandevia SC (2004) Reproducible measurement of voluntary activation of human elbow flexors with motor cortical stimulation. J Appl Physiol 97(1):236–242
Triscott S, Gordon J, Kuppuswamy A, King N, Davey N, Ellaway P (2008) Differential effects of endurance and resistance training on central fatigue. J Sports Sci 26(9):941–951. doi:10.1080/02640410701885439
Ugawa Y, Terao Y, Hanajima R, Sakai K, Kanazawa I (1995) Facilitatory effect of tonic voluntary contraction on responses to motor cortex stimulation. Electroencephalogr Clin Neurophysiol 97:451–454
Vila-Cha C, Falla D, Correia MV, Farina D (2012) Adjustments in motor unit properties during fatiguing contractions after training. Med Sci Sports Exerc 44(4):616–624
Acknowledgments
The authors would like to thank Prof. Guillaume Y. Millet for his valuable comments during the preparation of the manuscript. No sources of funding were used to conduct this study or prepare this manuscript.
Conflict of interest
The authors have no conflicts of interest that are directly relevant to this article.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Toshio Moritani.
Rights and permissions
About this article
Cite this article
Zghal, F., Cottin, F., Kenoun, I. et al. Improved tolerance of peripheral fatigue by the central nervous system after endurance training. Eur J Appl Physiol 115, 1401–1415 (2015). https://doi.org/10.1007/s00421-015-3123-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-015-3123-y