Abstract
Purpose
The aim of the present study was to investigate the role of maturation on the etiology of neuromuscular fatigue induced by repeated maximal voluntary isometric contractions (MVIC).
Methods
Nine prepubertal boys (9.9 ± 1.3 years), eight male adolescents (13.6 ± 1.3 years) and eleven men (23.4 ± 3.0 years) performed a series of repeated isometric MVICs of the knee extensors until the MVIC torque reached 60% of its initial value. Magnetic stimulations were delivered to the femoral nerve every five MVICs to follow the course of voluntary activation level (VA) and the potentiated twitch torque (Qtwpot).
Results
Task failure was reached after 52.9 ± 12.7, 42.6 ± 12.5, and 26.6 ± 6.3 repetitions in boys, adolescents and men, respectively. VA remained unchanged in men whereas it decreased significantly and similarly in boys and adolescents (p < 0.001). In contrast, Qtwpot remained unchanged in boys and decreased significantly less in adolescents than adults (p < 0.05).
Conclusions
Children and adolescents experience less peripheral and more central fatigue than adults. However, adolescents experience more peripheral fatigue than children for a comparable amount of central fatigue. This finding supports the idea that the tolerance of the central nervous system to peripheral fatigue could increase during maturation.
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Abbreviations
- %CoAct:
-
Level of antagonist co-activation
- %REP:
-
Percentage of the number of repetitions
- η 2 :
-
Partial eta-squared
- ANOVA:
-
Analysis of variance
- APHV:
-
Age from peak height velocity
- BF:
-
Biceps femoris
- CI:
-
Confidence interval
- EMG:
-
Electromyography
- KE:
-
Knee extensors
- M max :
-
Maximal M-wave amplitude
- MVIC:
-
Maximal voluntary isometric contractions
- M-wave:
-
Compound action potential
- Qtwpot :
-
Potentiated twitch torque
- Qtws :
-
Superimposed twitch torque
- Qtwunpot :
-
Unpotentiated twitch torque
- RF:
-
Rectus femoris
- RMS:
-
Root Mean Square
- VA:
-
Voluntary activation level
- VL:
-
Vastus lateralis
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 586:161–173. https://doi.org/10.1113/jphysiol.2007.141838
Armatas V, Bassa E, Patikas D et al (2010) Neuromuscular differences between men and prepubescent boys during a peak isometric knee extension intermittent fatigue test. Pediatr Exerc Sci 22:205–217
Bigland-Ritchie B, Woods JJ (1984) Changes in muscle contractile properties and neural control during human muscular fatigue. Muscle Nerve 7:691–699. https://doi.org/10.1002/mus.880070902
Bontemps B, Piponnier E, Chalchat E et al (2019) Children exhibit a more comparable neuromuscular fatigue profile to endurance athletes than untrained adults. Front Physiol 10:119. https://doi.org/10.3389/fphys.2019.00119
Burke D (2002) Effects of activity on axonal excitability: implications for motor control studies. Adv Exp Med Biol 508:33–37
Chen TC, Chen H-L, Liu Y-C, Nosaka K (2014) Eccentric exercise-induced muscle damage of pre-adolescent and adolescent boys in comparison to young men. Eur J Appl Physiol 114:1183–1195. https://doi.org/10.1007/s00421-014-2848-3
Cohen J (1969) Statistical power analysis for Behavioral sciences. Academic Press, Cambridge
Dipla K, Tsirini T, Zafeiridis A et al (2009) Fatigue resistance during high-intensity intermittent exercise from childhood to adulthood in males and females. Eur J Appl Physiol 106:645–653. https://doi.org/10.1007/s00421-009-1058-x
Enoka RM, Stuart DG (1992) Neurobiology of muscle fatigue. J Appl Physiol 72:1631–1648. https://doi.org/10.1152/jappl.1992.72.5.1631
Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789. https://doi.org/10.1152/physrev.2001.81.4.1725
Garrandes F, Colson SS, Pensini M et al (2007) Neuromuscular fatigue profile in endurance-trained and power-trained athletes. Med Sci Sports Exerc 39:149–158. https://doi.org/10.1249/01.mss.0000240322.00782.c9
Gorianovas G, Skurvydas A, Streckis V et al (2013) Repeated bout effect was more expressed in young adult males than in elderly males and boys. BioMed Res Int 2013:218970. https://doi.org/10.1155/2013/218970
Hamada T, Sale DG, MacDougall JD, Tarnopolsky MA (2003) Interaction of fibre type, potentiation and fatigue in human knee extensor muscles. Acta Physiol Scand 178:165–173. https://doi.org/10.1046/j.1365-201X.2003.01121.x
Hatzikotoulas K, Patikas D, Ratel S et al (2014) Central and peripheral fatigability in boys and men during maximal contraction. Med Sci Sports Exerc 46:1326–1333. https://doi.org/10.1249/MSS.0000000000000239
Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10:361–374
Hunter SK, Critchlow A, Shin I-S, Enoka RM (2004) Fatigability of the elbow flexor muscles for a sustained submaximal contraction is similar in men and women matched for strength. J Appl Physiol 96:195–202. https://doi.org/10.1152/japplphysiol.00893.2003
Kent-Braun JA, Ng AV, Doyle JW, Towse TF (2002) Human skeletal muscle responses vary with age and gender during fatigue due to incremental isometric exercise. J Appl Physiol 93:1813–1823. https://doi.org/10.1152/japplphysiol.00091.2002
Lexell J, Sjöström M, Nordlund AS, Taylor CC (1992) Growth and development of human muscle: a quantitative morphological study of whole vastus lateralis from childhood to adult age. Muscle Nerve 15:404–409. https://doi.org/10.1002/mus.880150323
Merton PA (1954) Voluntary strength and fatigue. J Physiol 123:553–564
Millet GY (2011) Can neuromuscular fatigue explain running strategies and performance in ultra-marathons?: the flush model. Sports Med Auckl NZ 41:489–506. https://doi.org/10.2165/11588760-000000000-00000
Mira J, Aboodarda SJ, Floreani M et al (2018) Effects of endurance training on neuromuscular fatigue in healthy active men. Part I: strength loss and muscle fatigue. Eur J Appl Physiol. https://doi.org/10.1007/s00421-018-3950-8
Mirwald RL, Baxter-Jones ADG, Bailey DA, Beunen GP (2002) An assessment of maturity from anthropometric measurements. Med Sci Sports Exerc 34:689–694
Murphy JR, Button DC, Chaouachi A, Behm DG (2014) Prepubescent males are less susceptible to neuromuscular fatigue following resistance exercise. Eur J Appl Physiol 114:825–835. https://doi.org/10.1007/s00421-013-2809-2
Neyroud D, Vallotton A, Millet GY et al (2014) The effect of muscle fatigue on stimulus intensity requirements for central and peripheral fatigue quantification. Eur J Appl Physiol 114:205–215. https://doi.org/10.1007/s00421-013-2760-2
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 39:120–124. https://doi.org/10.1136/bjsm.2003.010330
Paraschos I, Hassani A, Bassa E et al (2007) Fatigue differences between adults and prepubertal males. Int J Sports Med 28:958–963. https://doi.org/10.1055/s-2007-964984
Piponnier E, Martin V, Bontemps B et al (2018) Child-adult differences in neuromuscular fatigue are muscle-dependent. J Appl Physiol 125:1246–1256. https://doi.org/10.1152/japplphysiol.00244.2018
Piponnier E, Martin V, Chalchat E et al (2019) Effect of MTU length on child-adult difference in neuromuscular fatigue. Med Sci Sports Exerc 51(9):1961–1970
Ratel S, Bedu M, Hennegrave A et al (2002) Effects of age and recovery duration on peak power output during repeated cycling sprints. Int J Sports Med 23:397–402. https://doi.org/10.1055/s-2002-33737
Ratel S, Blazevich AJ (2017) Are prepubertal children metabolically comparable to well-trained adult endurance athletes? Sports Med Auckl NZ 47:1477–1485. https://doi.org/10.1007/s40279-016-0671-1
Ratel S, Kluka V, Vicencio SG et al (2015) Insights into the mechanisms of neuromuscular fatigue in boys and men. Med Sci Sports Exerc 47:2319–2328. https://doi.org/10.1249/MSS.0000000000000697
Russ D (2009) Sex differences in muscle fatigue. In: Williams C, Ratel S (eds) Human muscle fatigue. Routledge, London, New-York
Souron R, Nosaka K, Jubeau M (2018) Changes in central and peripheral neuromuscular fatigue indices after concentric versus eccentric contractions of the knee extensors. Eur J Appl Physiol 118:805–816. https://doi.org/10.1007/s00421-018-3816-0
Streckis V, Skurvydas A, Ratkevicius A (2007) Children are more susceptible to central fatigue than adults. Muscle Nerve 36:357–363. https://doi.org/10.1002/mus.20816
Tanner JM, Whitehouse RH (1976) Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child 51:170–179
Thomas K, Goodall S, Stone M et al (2015) Central and peripheral fatigue in male cyclists after 4-, 20-, and 40-km time trials. Med Sci Sports Exerc 47:537–546. https://doi.org/10.1249/MSS.0000000000000448
Tonson A, Ratel S, Le Fur Y et al (2008) Effect of maturation on the relationship between muscle size and force production. Med Sci Sports Exerc 40:918–925. https://doi.org/10.1249/MSS.0b013e3181641bed
Tonson A, Ratel S, Le Fur Y et al (2010) Muscle energetics changes throughout maturation: a quantitative 31P-MRS analysis. J Appl Physiol 109:1769–1778. https://doi.org/10.1152/japplphysiol.01423.2009
Zafeiridis A, Dalamitros A, Dipla K et al (2005) Recovery during high-intensity intermittent anaerobic exercise in boys, teens, and men. Med Sci Sports Exerc 37:505–512
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. https://doi.org/10.1007/s00421-015-3123-y
Acknowledgements
Virginie Kluka was supported by a grant of the French National Agency of Technological Research (ANRT), n 2012/0284.
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The authors report no conflict of interest. A funding from the French National Agency of Technological Research (ANRT: n°2012/0284; Virginie Kluka) was received for this project. This work is known to and agreed by the co-authors identified on the manuscript’s title page. This work required more than six people, because of clinical examination (physician or pediatrician), recruitment of volunteers, experimental procedures, statistical analysis and data analysis.
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Piponnier, E., Martin, V., Bourdier, P. et al. Maturation-related changes in the development and etiology of neuromuscular fatigue. Eur J Appl Physiol 119, 2545–2555 (2019). https://doi.org/10.1007/s00421-019-04233-3
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DOI: https://doi.org/10.1007/s00421-019-04233-3