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Differences in Neuromuscular Responses During Isometric Muscle Actions Before and After Pubescence

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Abstract

Purpose

The purpose of this study was to examine the responses of electromyographic (EMG) and mechanomyographic (MMG) amplitude across the torque spectrum in pre- and post-pubescent males and females.

Methods

Forty pre-pubescent (mean ± 95% confidence interval, age = 9.79 ± 0.35 years, n = 10 males, n = 10 females) and post-pubescent (age = 17.23 ± 0.58 years, n = 10 males, n = 10 females) participants completed this study. Participants completed maximal voluntary isometric contractions (MVICs) of the forearm flexors and extensors, as well as isometric ramp muscle actions. EMG and MMG amplitude were quantified from the biceps brachii, brachialis, and brachioradialis during all muscle actions. EMG and MMG amplitude during the isometric ramp muscle actions were normalized to EMG and MMG amplitude from the MVICs.

Results

The pre-pubertal group tended to have greater relative EMG amplitude across intensity (P < 0.050), while the post-pubertal group had a more pronounced increase in EMG amplitude at higher intensities. Similarly, the pre-pubertal group tended to have greater relative MMG amplitude across intensity (P ≤ 0.004) that plateaued earlier than the post-pubertal group (55% vs. 65%–75% of MVIC). Additionally, the pre-pubertal group had greater coactivation across intensity (P ≤ 0.001).

Conclusion

The greater relative EMG and MMG amplitude in the pre-pubertal group, in conjunction with the earlier plateau in MMG amplitude for the pre-pubertal group and greater coactivation, suggests less efficient muscle activation and motor unit recruitment strategies during pre-pubescence. Taken together, the findings of the present study suggest that growth-mediated changes in neuromuscular function lead to improvements in the efficiency of muscular activation and augmentations in motor unit recruitment strategies.

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Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  1. Arabadzhiev T, Dimitrov V, Dimitrov G. The increase in surface EMG could be a misleading measure of neural adaptation during the early gains in strength. Eur J Appl Physiol. 2014;114:1645–55. https://doi.org/10.1007/s00421-014-2893-y.

    Article  PubMed  Google Scholar 

  2. Barry D, Cole N. Muscle sounds are emitted at the resonant frequencies of skeletal muscle. IEEE Trans Biomed Eng. 1990;37(5):525–31.

    Article  CAS  PubMed  Google Scholar 

  3. Beck T, Housh T, Johnson G, Weir J, Cramer J, Coburn J, Malek M. Mechanomyographic and electromyographic responses during submaximal to maximal eccentric isokinetic muscle actions of the biceps brachii. J Strength Cond Res. 2006;20(1):184–91. https://doi.org/10.1519/R-17605.1.

    Article  PubMed  Google Scholar 

  4. Bergeron M, Mountjoy M, Armstrong N, Chia M, Cote J, Emery C, Faigenbaum A, Hall G, Kriemler S, Leglise M, Malina R, Pensgaard A, Sanchez A, Soligard T, Sundgot-Borgen J, Mechelen W, Weissensteiner J, Engebretsen L. International Olympic Committee consensus statement on youth athletic development. Br J Sports Med. 2015;49(13):843–51. https://doi.org/10.1136/bjsports-2015-094962.

    Article  PubMed  Google Scholar 

  5. Coburn JW, Housh TJ, Cramer JT, Weir JP, Miller JM, Beck TW, Malek MH, Johnson GO. Mechanomyographic and electromyographic responses of the vastus medialis muscle during isometric and concentric muscle actions. J Strength Cond Res. 2005;19(2):412–20. https://doi.org/10.1519/15744.1.

    Article  PubMed  Google Scholar 

  6. De Luca CJ. The use of Surface electromyography in biomechanics. J Appl Biomech. 1997;13(2):135–63. https://doi.org/10.1123/jab.13.2.135.

    Article  Google Scholar 

  7. DeFreitas JM, Beck TW, Stock MS. Effects of strength training on mechanomyographic amplitude. Physiological Meas. 2012;33(8):1353–61. https://doi.org/10.1088/0967-3334/33/8/1353.

    Article  ADS  Google Scholar 

  8. Faigenbaum AD, Kraemer WJ, Blimkie CJR, Jeffreys I, Micheli LJ, Nitka M, Rowland TW. Youth resistance training: Updated position statement paper from the National Strength and Conditioning Association. J Strength Cond Res. 2009;23(5 Suppl):60–79.

    Article  Google Scholar 

  9. Falk B, Usselman C, Dotan R, Brunton L, Klentrou P, Shaw J, Gabriel D. Child-adult differences in muscle strength and activation pattern during isometric elbow flexion and extension. Appl Physiol Nutr Metab. 2009;34(4):609–15. https://doi.org/10.1139/H09-020.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Farina D, Merletti R, Enoka RM. The extraction of neural strategies from the surface EMG. J Appl Physiol. 2004;96(4):1486–95. https://doi.org/10.1152/japplphysiol.01070.2003.

    Article  PubMed  Google Scholar 

  11. Gaudet G, Raison M, Maso FD, Achiche S, Begon M. Intra- and intersession reliability of surface electromyography on muscles actuating the forearm during maximum voluntary contractions. J Appl Biomech. 2016;32(6):558–70. https://doi.org/10.1123/jab.2015-0214.

    Article  PubMed  Google Scholar 

  12. Gillen ZM, Shoemaker ME, McKay BD, Bohannon NA, Gibson SM, Cramer JT. Muscle strength, size, and neuromuscular function before and during adolescence. Eur J Appl Physiol. 2019;119(7):1619–32. https://doi.org/10.1007/s00421-019-04151-4.

    Article  PubMed  Google Scholar 

  13. Gillen ZM, Housh TJ, Schmidt RJ, Herda TJ, De Ayala RJ, Shoemaker ME, Cramer JT. Comparisons of muscle strength, size, and voluntary activation in pre- and post-pubescent males and females. Eur J Appl Physiol. 2021;121(9):2487–97. https://doi.org/10.1007/s00421-021-04717-1.

    Article  PubMed  Google Scholar 

  14. Granados A, Gebremariam A, Lee JM. Relationship between timing of peak height velocity and pubertal dtaging in boys and girls. J Clin Res Pediatr Endocrinol. 2015;7(3):235–7. https://doi.org/10.4274/jcrpe.2007.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Gravetter FJ, Wallnau LB. Statistics for the behavioral sciences. 10th Edition. Boston, MA: Cengage Learning; 2017.

  16. Grosset JF, Mora I, Lambertz D, Pérot C. Voluntary activation of the triceps surae in prepubertal children. J Electromyogr Kinesiol. 2008;18(3):455–65. https://doi.org/10.1016/j.jelekin.2006.11.002.

    Article  PubMed  Google Scholar 

  17. Herda TJ, Weir JP, Ryan ED, Walter AA, Costa PB, Hoge KM, Beck TW, Stout JR, Cramer JT. Reliability of absolute versus log-transformed regression models for examining the torque-related patterns of response for mechanomyographic amplitude. J Neurosci Methods. 2009;179(2):240–6. https://doi.org/10.1016/j.jneumeth.2009.01.028.

    Article  PubMed  Google Scholar 

  18. Herda TJ, Housh TJ, Fry AC, Weir JP, Schilling BK, Ryan ED, Cramer JT. A noninvasive, log-transform method for fiber type discrimination using mechanomyography. J Electromyogr Kinesiol. 2010;20(5):787–94.

    Article  PubMed  Google Scholar 

  19. Herda TJ, Walter AA, Costa PB, Ryan ED, Stout JR, Cramer JT. Differences in the log-transformed electromyographic–force relationships of the plantar flexors between high- and moderate-activated subjects. J Electromyogr Kinesiol. 2011;21(5):841–6.

    Article  PubMed  Google Scholar 

  20. Herda TJ, Trevino MA, Sterczala AJ, Miller JD, Wray ME, Dimmick HL, Gallagher PM, Fry AC. Muscular strength and power are correlated with motor unit action potential amplitudes, but not myosin heavy chain isoforms in sedentary males and females. J Biomech. 2019;86:251–5. https://doi.org/10.1016/j.jbiomech.2019.01.050.

    Article  PubMed  Google Scholar 

  21. Herda TJ, Miller JD, Wray ME, Sterczala AJ, Dimmick HL, Trevino MA. Motor unit firing rates of the first dorsal interosseous differ between male and female children aged 8 to 10 years. Hum Mov Sci. 2019;66:416–24. https://doi.org/10.1016/j.humov.2019.04.011.

    Article  PubMed  Google Scholar 

  22. Hermens HJ. SENIAM 8: European Recommendations for Surface Electromyography. 2nd Edition. Enschede, the Netherlands: Roessingh Research and Development; 1999.

  23. Jenkins N, Housh T, Buckner S, Bergstrom H, Cochrane K, Hill E, Smith C, Schmidt R, Johnson G, Cramer J. Neuromuscular adaptations after 2 and 4 weeks of 80% versus 30% 1 repetition maximum resistance training to failure. J Strength Cond Res. 2016;(30):2174–85. https://doi.org/10.1519/JSC.0000000000001308.

    Article  PubMed  Google Scholar 

  24. Jenkins N, Miramonti A, Hill E, Smith C, Cochrane-Snyman K, Housh T, Cramer J. Mechanomyographic amplitude is sensitive to load-dependent neuromuscular adaptations in response to resistance training. J Strength Conditioning Res. 2019;35(11):3265–9. https://doi.org/10.1519/JSC.0000000000003276.

    Article  Google Scholar 

  25. Khairullah A, Klein LC, Ingle SM, May MT, Whetzel CA, Susman EJ, Paus T. Testosterone trajectories and reference ranges in a large longitudinal sample of male adolescents. PLoS ONE. 2014;9(9):e108838. https://doi.org/10.1371/journal.pone.0108838.

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  26. Klein KO, Martha PM Jr, Blizzard RM, Herbst T, Rogol AD. A longitudinal assessment of hormonal and physical alterations during normal puberty in boys. II. Estrogen levels as determined by an ultrasensitive bioassay. J Clin Endocrinol Metab. 1996;81(9):3203–7. https://doi.org/10.1210/jc.81.9.3203.

    Article  CAS  PubMed  Google Scholar 

  27. Kluka V, Martin V, Vicencio SG, Jegu A-G, Cardenoux C, Morio C, Coudeyre E, Ratel S. Effect of muscle length on voluntary activation level in children and adults. Med Sci Sports Exerc. 2015;47(4):718–24. https://doi.org/10.1249/MSS.0000000000000463.

    Article  PubMed  Google Scholar 

  28. Kluka V, Martin V, Vicencio SG, Giustiniani M, Morel C, Morio C, Coudeyre E, Ratel S. Effect of muscle length on voluntary activation of the plantar flexors in boys and men. Eur J Appl Physiol. 2016;116(5):1043–51. https://doi.org/10.1007/s00421-016-3362-6.

    Article  PubMed  Google Scholar 

  29. Lambertz D, Mora I, Grosset J-F, Pérot C. Evaluation of musculotendinous stiffness in prepubertal children and adults, taking into account muscle activity. J Appl Physiol. 2003;95(1):64–72. https://doi.org/10.1152/japplphysiol.00885.2002.

    Article  PubMed  Google Scholar 

  30. Lloyd R, Cronin J, Faigenbaum A, Haff G, Howard R, Kraemer W, Micheli L, Myer G, Oliver J. National Strength and Conditioning Association position statement on long-term athletic development. J Strength Cond Res. 2016;30(6):1491–509. https://doi.org/10.1519/JSC.0000000000001387.

    Article  PubMed  Google Scholar 

  31. Marshall WA, Tanner JM. Variations in pattern of pubertal changes in girls. Arch Dis Child. 1969;44(235):291–303. https://doi.org/10.1136/adc.44.235.291.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Marshall WA, Tanner JM. Variations in the pattern of pubertal changes in boys. Arch Dis Child. 1970;45(239):13–23. https://doi.org/10.1136/adc.45.239.13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Miller JD, Sterczala AJ, Trevino MA, Wray ME, Dimmick HL, Herda TJ. Motor unit action potential amplitudes and firing rates during repetitive muscle actions of the first dorsal interosseous in children and adults. Eur J Appl Physiol. 2019;119(4):1007–18. https://doi.org/10.1007/s00421-019-04090-0.

    Article  PubMed  Google Scholar 

  34. Mirwald RL, Baxter-Jones ADG, Bailey DA, Beunen GP. An assessment of maturity from anthropometric measurements. Med Sci Sports Exerc. 2002;34(4):689–94. https://doi.org/10.1097/00005768-200204000-00020.

    Article  PubMed  Google Scholar 

  35. Nielsen CT, Skakkebaek NE, Darling JA, Hunter WM, Richardson DW, Jørgensen M, Keiding N. Longitudinal study of testosterone and luteinizing hormone (LH) in relation to spermarche, pubic hair, height and sitting height in normal boys. Acta Endocrinol Suppl. 1986;279:98–106.

    CAS  Google Scholar 

  36. O’Brien TD, Reeves ND, Baltzopoulos V, Jones DA, Maganaris CN. The effects of agonist and antagonist muscle activation on the knee extension moment–angle relationship in adults and children. Eur J Appl Physiol. 2009;106(6):849–56. https://doi.org/10.1007/s00421-009-1088-4.

    Article  CAS  PubMed  Google Scholar 

  37. O’Brien TD, Reeves ND, Baltzopoulos V, Jones DA. In vivo measurements of muscle specific tension in adults and children. Exp Physiol. 2010;95(1):202–10. https://doi.org/10.1113/expphysiol.2009.048967.

    Article  PubMed  Google Scholar 

  38. Orizio C. Muscle sound: bases for the introduction of a mechanomyographic signal in muscle studies. Crit Rev Biomed Eng. 1993;21(3):201–43.

    CAS  PubMed  Google Scholar 

  39. Pişkin İE, Gümüş M, Bayraktaroğlu T, Akalin TC, Yamaner F. Growth and pubertal development in adolescent male wrestlers. J Sports Med Phys Fit. 2018;58(6):852–6.

    Google Scholar 

  40. Pitcher CA, Elliott CM, Williams SA, Licari MK, Kuenzel A, Shipman PJ, Valentine JP, Reid SL. Childhood muscle morphology and strength: Alterations over six months of growth. Muscle Nerve. 2012;46(3):360–6. https://doi.org/10.1002/mus.23326.

    Article  PubMed  Google Scholar 

  41. Pope ZK, Hester GM, Benik FM, DeFreitas JM. Action potential amplitude as a noninvasive indicator of motor unit-specific hypertrophy. J Neurophysiol. 2016;115(5):2608–14. https://doi.org/10.1152/jn.00039.2016.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Round JM, Jones DA, Honour JW, Nevill AM. Hormonal factors in the development of differences in strength between boys and girls during adolescence: a longitudinal study. Ann Hum Biol. 1999;26(1):49–62. https://doi.org/10.1080/030144699282976.

    Article  CAS  PubMed  Google Scholar 

  43. Ryan E, Cramer J, Housh T, Beck T, Herda T, Hartman M, Stout J. Inter-individual variability among the mechanomyographic and electromyographic amplitude and mean power frequency responses during isometric ramp muscle actions. Electromyogr Clin Neurophysiol. 2007;47(3):161.

    CAS  PubMed  Google Scholar 

  44. Seger JY, Thorstensson A. Muscle strength and myoelectric activity in prepubertal and adult males and females. Eur J Appl Physiol Occup Physiol. 1994;69(1):81–7. https://doi.org/10.1007/BF00867932.

    Article  CAS  PubMed  Google Scholar 

  45. Seger JY, Thorstensson A. Muscle strength and electromyogram in boys and girls followed through puberty. Eur J Appl Physiol Occup Physiol. 2000;81(1–2):54–61. https://doi.org/10.1007/PL00013797.

    Article  CAS  Google Scholar 

  46. Stokes MJ, Dalton PA. Acoustic myography: Applications and considerations in measuring muscle performance. Isokinet Exerc Sci. 1993;3(1):4–15. https://doi.org/10.3233/IES-1993-3101.

    Article  Google Scholar 

  47. Vincent WJ, Weir JP. Statistics in Kinesiology. 5th Edition. Champaign, IL: Human Kinetics; 2020.

  48. Warburton DER, Jamnik VK, Bredin SSD, Gledhill N. The Physical Activity Readiness Questionnaire for Everyone (PAR-Q+) and Electronic Physical Activity Readiness Medical Examination (ePARmed-X+). Health Fit J Can. 2011;4:3–23.

    Google Scholar 

  49. Wood LE, Dixon S, Grant C, Armstrong N. Elbow flexion and extension strength relative to body or muscle size in children. Med Sci Sports Exerc. 2004;36(11):1977–84. https://doi.org/10.1249/01.MSS.0000145453.02598.7E.

    Article  PubMed  Google Scholar 

  50. Zacharias L, Rand WM. Adolescent growth in height and its relation to menarche in contemporary American girls. Ann Hum Biol. 1983;10:209–22. https://doi.org/10.1080/03014468300006381.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Efforts for this study were funded, in part, by a National Strength and Conditioning Association Foundation (NSCAF) Graduate Research Doctoral Grant, the University of Nebraska Agriculture Research Division with funds provided by the Hatch Act (Agency: U.S. Department of Agriculture, National Institute of Food and Agriculture; Accession No: 1000080; Project No: NEB-36-078) and a grant from Abbott Nutrition, Columbus, OH. The authors would like to thank Nicholas Bohannon and Sydney Gibson for their help conducting the study, as well as each of the subjects for their participation.

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Authors and Affiliations

  1. Department of Kinesiology, Mississippi State University, 236 McCarthy Gymnasium Mississippi State, 39762, Mississippi State, MS, USA

    Zachary M. Gillen

  2. Department of Nutrition & Health Sciences, University of Nebraska-Lincoln, 68583, Lincoln, NE, USA

    Terry J. Housh & Richard J. Schmidt

  3. Department of Health, Sport, and Exercise Sciences, University of Kansas, 66045, Lawrence, KS, USA

    Trent J. Herda

  4. Department of Educational Psychology, University of Nebraska-Lincoln, 68583, Lincoln, NE, USA

    Rafael J. De Ayala

  5. School of Health and Consumer Sciences, South Dakota State University, Brookings, SD, USA

    Marni E. Shoemaker

  6. College of Health Professions and Sciences, University of Central Florida, Orlando, FL, USA

    Joel T. Cramer

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Gillen, Z.M., Housh, T.J., Schmidt, R.J. et al. Differences in Neuromuscular Responses During Isometric Muscle Actions Before and After Pubescence. J. of SCI. IN SPORT AND EXERCISE 6, 22–34 (2024). https://doi.org/10.1007/s42978-022-00199-5

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