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01-12-2019 | Electromyographic | Original Article

Maturation-related changes in the development and etiology of neuromuscular fatigue

Authors: Enzo Piponnier, Vincent Martin, Pierre Bourdier, Brice Biancarelli, Virginie Kluka, Sebastian Garcia-Vicencio, Anne-Gaëlle Jegu, Charlotte Cardenoux, Cédric Morio, Emmanuel Coudeyre, Sébastien Ratel

Published in: European Journal of Applied Physiology | Issue 11-12/2019

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 (Qtw_pot).

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, Qtw_pot 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.

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 CrossRefPubMed

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 22:205–217CrossRef

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

Burke D (2002) Effects of activity on axonal excitability: implications for motor control studies. Adv Exp Med Biol 508:33–37CrossRef

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRefPubMed

Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10:361–374CrossRef

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

Merton PA (1954) Voluntary strength and fatigue. J Physiol 123:553–564CrossRef

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 CrossRef

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 CrossRefPubMed

Mirwald RL, Baxter-Jones ADG, Bailey DA, Beunen GP (2002) An assessment of maturity from anthropometric measurements. Med Sci Sports Exerc 34:689–694PubMed

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 CrossRefPubMed

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 CrossRef

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):1961–1970CrossRef

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 CrossRefPubMed

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 CrossRef

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMed

Tanner JM, Whitehouse RH (1976) Clinical longitudinal standards for height, weight, height velocity, weight velocity, and stages of puberty. Arch Dis Child 51:170–179CrossRef

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 CrossRefPubMed

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 CrossRefPubMed

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 CrossRefPubMedPubMedCentral

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 37:505–512CrossRef

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 CrossRefPubMed

Title: Maturation-related changes in the development and etiology of neuromuscular fatigue
Authors: Enzo Piponnier
Vincent Martin
Pierre Bourdier
Brice Biancarelli
Virginie Kluka
Sebastian Garcia-Vicencio
Anne-Gaëlle Jegu
Charlotte Cardenoux
Cédric Morio
Emmanuel Coudeyre
Sébastien Ratel
Publication date: 01-12-2019
Publisher: Springer Berlin Heidelberg
Keywords: Electromyographic
Fatigue
Published in: European Journal of Applied Physiology / Issue 11-12/2019
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI: https://doi.org/10.1007/s00421-019-04233-3

At a glance: The STEP trials

Springer Medicine

Maturation-related changes in the development and etiology of neuromuscular fatigue

Abstract

Purpose

Methods

Results

Conclusions

At a glance: The STEP trials

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

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