Relationship between neuromuscular fatigue, muscle activation and the work done above the critical power during severe-intensity exercise

Guillaume P Ducrocq, Grégory M Blain, Guillaume P Ducrocq, Grégory M Blain

Abstract

New findings: What is the central question of this study? Does the work done above critical power (W') or muscle activation determine the degree of peripheral fatigue induced by cycling time trials performed in the severe-intensity domain? What is the main finding and its importance? Peripheral fatigue increased when power output and muscle activation increased, whereas W' did not change between the time trials. Therefore, no relationship was found between W' and exercise-induced peripheral fatigue such as previously postulated in the literature. In contrast, we found a significant association between EMG amplitude during exercise and exercise-induced reduction in the potentiated quadriceps twitch, suggesting that muscle activation plays a key role in determining peripheral fatigue during severe-intensity exercise.

Abstract: In order to determine the relationship between peripheral fatigue, muscle activation and the total work done above critical power (W'), 10 men and four women performed, on separated days, self-paced cycling time trials of 3, 6, 10 and 15 min. Exercise-induced quadriceps fatigue was quantified using pre- to postexercise (15 s to 15 min recovery) changes in maximal voluntary contraction (MVC) peak force, voluntary activation and potentiated twitch force (QT). Voluntary activation was measured using the interpolated twitch technique, and QT was evoked by electrical stimulations of the femoral nerve. Quadriceps muscle activation was determined using the root mean square of surface EMG of vastus lateralis (VLRMS ), vastus medialis (VMRMS ) and rectus femoris (RFRMS ). Critical power and W' were calculated from the power-duration relationship from the four time trials. Mean power output and mean VLRMS , VMRMS and RFRMS were greater during shorter compared with longer exercise periods (P < 0.05), whereas no significant between-trial change in W' was found. The magnitude of exercise-induced reductions in QT increased with the increase in power output (P < 0.001) and was associated with mean VLRMS, VMRMS and RFRMS (P < 0.001, r2 > 0.369) but not W' (P > 0.150, r2 < 0.044). Reduction in voluntary activation tended (P = 0.067) to be more pronounced with the lengthening in time trial duration, whereas no significant between-trial changes in MVC peak force were found. Our data suggest that peripheral fatigue is not related to the amount of work done above the critical power but rather to the level of muscle activation during exercise in the severe-intensity domain.

Keywords: critical power; exercise performance; muscle activation; neuromuscular fatigue; recovery from fatigue.

© 2022 The Authors. Experimental Physiology © 2022 The Physiological Society.

References

REFERENCES

    1. Allen, D. G., Lamb, G. D., & Westerblad, H. (2008). Skeletal muscle fatigue: Cellular mechanisms. Physiological Reviews, 88, 287-332.
    1. Amann, M., Blain, G. M., Proctor, L. T., Sebranek, J. J., Pegelow, D. F., & Dempsey, J. A. (2011). Implications of group III and IV muscle afferents for high-intensity endurance exercise performance in humans. The Journal of Physiology, 589, 5299-5309.
    1. Amann, M., Proctor, L. T., Sebranek, J. J., Pegelow, D. F., & Dempsey, J. A. (2009). Opioid-mediated muscle afferents inhibit central motor drive and limit peripheral muscle fatigue development in humans. The Journal of Physiology, 587, 271-283.
    1. Ansdell, P., Brownstein, C. G., Škarabot, J., Hicks, K. M., Howatson, G., Thomas, K., Hunter, S. K., & Goodall, S. (2019). Sex differences in fatigability and recovery relative to the intensity-duration relationship. The Journal of Physiology, 597, 5577-5595.
    1. Baker, A. J., Kostov, K. G., Miller, R. G., & Weiner, M. W. (1993). Slow force recovery after long-duration exercise: Metabolic and activation factors in muscle fatigue. Journal of Applied Physiology, 74, 2294-2300.
    1. Black, M. I., Durant, J., Jones, A. M., & Vanhatalo, A. (2014). Critical power derived from a 3-min all-out test predicts 16.1-km road time-trial performance. European Journal of Sport Science, 14, 217-223.
    1. Black, M. I., Jones, A. M., Bailey, S. J., & Vanhatalo, A. (2015). Self-pacing increases critical power and improves performance during severe-intensity exercise. Applied Physiology, Nutrition and Metabolism, 40, 662-670.
    1. Black, M. I., Jones, A. M., Blackwell, J. R., Bailey, S. J., Wylie, L. J., McDonagh, S. T. J., Thompson, C., Kelly, J., Sumners, P., Mileva, K. N., Bowtell, J. L., & Vanhatalo, A. (2017). Muscle metabolic and neuromuscular determinants of fatigue during cycling in different exercise intensity domains. Journal of Applied Physiology, 122, 446-459.
    1. Blain, G. M., Mangum, T. S., Sidhu, S. K., Weavil, J. C., Hureau, T. J., Jessop, J. E., Bledsoe, A. D., Richardson, R. S., & Amann, M. (2016). Group III/IV muscle afferents limit the intramuscular metabolic perturbation during whole body exercise in humans. The Journal of Physiology, 594, 5303-5315.
    1. Bogdanis, G. C., Nevill, M. E., Boobis, L. H., Lakomy, H. K., & Nevill, A. M. (1995). Recovery of power output and muscle metabolites following 30 s of maximal sprint cycling in man. The Journal of Physiology, 482(Pt 2), 467-480.
    1. Bogdanis, G. C., Nevill, M. E., Lakomy, H. K., & Boobis, L. H. (1998). Power output and muscle metabolism during and following recovery from 10 and 20 s of maximal sprint exercise in humans. Acta Physiologica Scandinavica, 163, 261-272.
    1. Borg, E., & Kaijser, L. (2006). A comparison between three rating scales for perceived exertion and two different work tests. Scandinavian Journal of Medicine & Science in Sports, 16, 57-69.
    1. Bottinelli, R., Canepari, M., Reggiani, C., & Stienen, G. J. (1994). Myofibrillar ATPase activity during isometric contraction and isomyosin composition in rat single skinned muscle fibres. The Journal of Physiology, 481(Pt 3), 663-675.
    1. Broxterman, R. M., Craig, J. C., Smith, J. R., Wilcox, S. L., Jia, C., Warren, S., & Barstow, T. J. (2015). Influence of blood flow occlusion on the development of peripheral and central fatigue during small muscle mass handgrip exercise. The Journal of Physiology, 593, 4043-4054.
    1. Broxterman, R. M., Craig, J. C., Weavil, J. C., & Hureau, T. J. (2020). The relationship between W′ and peripheral fatigue considered. Experimental Physiology, 105, 211-212.
    1. Bruton, J. D., Place, N., Yamada, T., Silva, J. P., Andrade, F. H., Dahlstedt, A. J., Zhang, S.-J., Katz, A., Larsson, N.-G., & Westerblad, H. (2008). Reactive oxygen species and fatigue-induced prolonged low-frequency force depression in skeletal muscle fibres of rats, mice and SOD2 overexpressing mice. The Journal of Physiology, 586, 175-184.
    1. Burnley, M., & Jones, A. M. (2016). Power-duration relationship: Physiology, fatigue, and the limits of human performance. European Journal of Sport Science, 18, 1-12.
    1. Burnley, M., Vanhatalo, A., Fulford, J., & Jones, A. M. (2010). Similar metabolic perturbations during all-out and constant force exhaustive exercise in humans: A 31P magnetic resonance spectroscopy study. Experimental Physiology, 95, 798-807.
    1. Burnley, M., Vanhatalo, A., & Jones, A. M. (2012). Distinct profiles of neuromuscular fatigue during muscle contractions below and above the critical torque in humans. Journal of Applied Physiology, 113, 215-223.
    1. Carroll, T. J., Taylor, J. L., & Gandevia, S. C. (2017). Recovery of central and peripheral neuromuscular fatigue after exercise. Journal of Applied Physiology, 122, 1068-1076.
    1. Cheng, A. J., Bruton, J. D., Lanner, J. T., & Westerblad, H. (2015). Antioxidant treatments do not improve force recovery after fatiguing stimulation of mouse skeletal muscle fibres. The Journal of Physiology, 593, 457-472.
    1. Chidnok, W., Dimenna, F. J., Bailey, S. J., Vanhatalo, A., Morton, R. H., Wilkerson, D. P., & Jones, A. M. (2012). Exercise tolerance in intermittent cycling: Application of the critical power concept. Medicine and Science in Sports and Exercise, 44, 966-976.
    1. Chidnok, W., Dimenna, F. J., Bailey, S. J., Wilkerson, D. P., Vanhatalo, A., & Jones, A. M. (2013). Effects of pacing strategy on work done above critical power during high-intensity exercise. Medicine and Science in Sports and Exercise, 45, 1377-1385.
    1. Cohen, J. (1977). Statistical power analysis for the behavioral sciences. Academic Press.
    1. Costill, D. L., Fink, W. J., & Pollock, M. L. (1976). Muscle fiber composition and enzyme activities of elite distance runners. Medicine and Science in Sports, 8, 96-100.
    1. Decorte, N., Lafaix, P. A., Millet, G. Y., Wuyam, B., & Verges, S. (2012). Central and peripheral fatigue kinetics during exhaustive constant-load cycling. Scandinavian Journal of Medicine & Science in Sports, 22, 381-391.
    1. Duchateau, J., & Enoka, R. M. (2011). Human motor unit recordings: Origins and insight into the integrated motor system. Brain Research, 1409, 42-61.
    1. Ducrocq, G. P., Hureau, T. J., Bøgseth, T., Meste, O., & Blain, G. M. (2021). Recovery from fatigue after cycling time trials in elite endurance athletes. Medicine and Science in Sports and Exercise, 53, 904-917.
    1. Edwards, R. H. T., Hill, D. K., Jones, D. A., & Merton, P. A. (1977). Fatigue of long duration in human skeletal muscle after exercise. The Journal of Physiology, 272, 769-778.
    1. Essén, B., Jansson, E., Henriksson, J., Taylor, A. W., & Saltin, B. (1975). Metabolic characteristics of fibre types in human skeletal muscle. Acta Physiologica Scandinavica, 95, 153-165.
    1. Felippe, L. C., Ferreira, G. A., Learsi, S. K., Boari, D., Bertuzzi, R. C. M., & Lima-Silva, A. E. (2018). Caffeine increases both total work performed above critical power and peripheral fatigue during a 4-km cycling time trial. Journal of Applied Physiology, 106, 211.
    1. Gagnon, P., Bussières, J. S., Ribeiro, F., Gagnon, S. L., Saey, D., Gagné, N., Provencher, S., & Maltais, F. (2012). Influences of spinal anesthesia on exercise tolerance in patients with chronic obstructive pulmonary disease. American Journal of Respiratory and Critical Care Medicine, 186, 606-615.
    1. Gandevia, S. C. (2001). Spinal and supraspinal factors in human muscle fatigue. Physiological Reviews, 81, 1725-1789.
    1. Henneman, E. (1957). Relation between size of neurons and their susceptibility to discharge. Science, 126, 1345-1347.
    1. Hill, D. W., Poole, D. C., & Smith, J. C. (2002). The relationship between power and the time to achieve VO2max. Medicine and Science in Sports and Exercise, 34, 709-714.
    1. Hogan, M. C., Richardson, R. S., & Haseler, L. J. (1999). Human muscle performance and PCr hydrolysis with varied inspired oxygen fractions: A 31P-MRS study. Journal of Applied Physiology, 86, 1367-1373.
    1. Howald, H., Hoppeler, H., Claassen, H., Mathieu, O., & Straub, R. (1985). Influences of endurance training on the ultrastructural composition of the different muscle fiber types in humans. Pflugers Archiv: European Journal of Physiology, 403, 369-376.
    1. Hureau, T. J., Weavil, J. C., Thurston, T. S., Wan, H.-Y., Gifford, J. R., Jessop, J. E., Buys, M. J., Richardson, R. S., & Amann, M. (2019). Pharmacological attenuation of group III/IV muscle afferents improves endurance performance when oxygen delivery to locomotor muscles is preserved. Journal of Applied Physiology, 127, 1257-1266.
    1. Jenkins, D. G., & Quigley, B. M. (1991). The y-intercept of the critical power function as a measure of anaerobic work capacity. Ergonomics, 34, 13-22.
    1. Jones, A. M., Wilkerson, D. P., DiMenna, F., Fulford, J., & Poole, D. C. (2008). Muscle metabolic responses to exercise above and below the “critical power” assessed using 31P-MRS. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 294, R585-R593.
    1. Karatzaferi, C., de Haan, A., Ferguson, R. A., van Mechelen, W., & Sargeant, A. J. (2001). Phosphocreatine and ATP content in human single muscle fibres before and after maximum dynamic exercise. Pflugers Archiv: European Journal of Physiology, 442, 467-474.
    1. Kennedy, D. S., Fitzpatrick, S. C., Gandevia, S. C., & Taylor, J. L. (2015). Fatigue-related firing of muscle nociceptors reduces voluntary activation of ipsilateral but not contralateral lower limb muscles. Journal of Applied Physiology, 118, 408-418.
    1. Kennedy, D. S., McNeil, C. J., Gandevia, S. C., & Taylor, J. L. (2014). Fatigue-related firing of distal muscle nociceptors reduces voluntary activation of proximal muscles of the same limb. Journal of Applied Physiology, 116, 385-394.
    1. Laursen, P. B., Francis, G. T., Abbiss, C. R., Newton, M. J., & Nosaka, K. (2007). Reliability of time-to-exhaustion versus time-trial running tests in runners. Medicine and Science in Sports and Exercise, 39, 1374-1379.
    1. Martin, V., Millet, G. Y., Martin, A., Deley, G., & Lattier, G. (2004). Assessment of low-frequency fatigue with two methods of electrical stimulation. Journal of Applied Physiology, 97, 1923-1929.
    1. Mattioni Maturana, F., Fontana, F. Y., Pogliaghi, S., Passfield, L., & Murias, J. M. (2018). Critical power: How different protocols and models affect its determination. Journal of Science and Medicine in Sport, 21, 742-747.
    1. Mendez-Villanueva, A., Edge, J., Suriano, R., Hamer, P., & Bishop, D. J. (2012). The recovery of repeated-sprint exercise is associated with PCr resynthesis, while muscle pH and EMG amplitude remain depressed. PLoS One, 7, e51977.
    1. Merton, P. A. (1954). Voluntary strength and fatigue. The Journal of Physiology, 123, 553-564.
    1. Miller, R. G., Giannini, D., Milner-Brown, H. S., Layzer, R. B., Koretsky, A. P., Hooper, D., & Weiner, M. W. (1987). Effects of fatiguing exercise on high-energy phosphates, force, and EMG: Evidence for three phases of recovery. Muscle & Nerve, 10, 810-821.
    1. Monod, H., & Scherrer, J. (1965). The work capacity of a synergic muscular group. Ergonomics, 8, 329-338.
    1. Moritani, T., Nagata, A., deVries, H. A., & Muro, M. (1981). Critical power as a measure of physical work capacity and anaerobic threshold. Ergonomics, 24, 339-350.
    1. Newham, D. J., & Cady, E. B. (1990). A 31P study of fatigue and metabolism in human skeletal muscle with voluntary, intermittent contractions at different forces. NMR in Biomedicine, 3, 211-219.
    1. Neyroud, D., Vallotton, A., Millet, G. Y., Kayser, B., & Place, N. (2014). The effect of muscle fatigue on stimulus intensity requirements for central and peripheral fatigue quantification. European Journal of Applied Physiology, 114, 205-215.
    1. O'Leary, T. J., Morris, M. G., Collett, J., & Howells, K. (2016). Central and peripheral fatigue following non-exhaustive and exhaustive exercise of disparate metabolic demands. Scandinavian Journal of Medicine & Science in Sports, 26, 1287-1300.
    1. Pethick, J., Winter, S. L., & Burnley, M. (2016). Loss of knee extensor torque complexity during fatiguing isometric muscle contractions occurs exclusively above the critical torque. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 310, R1144-R1153.
    1. Poole, D. C., Ward, S. A., Gardner, G. W., & Whipp, B. J. (1988). Metabolic and respiratory profile of the upper limit for prolonged exercise in man. Ergonomics, 31, 1265-1279.
    1. Schäfer, L. U., Hayes, M., & Dekerle, J. (2019a). The magnitude of neuromuscular fatigue is not intensity dependent when cycling above critical power but relates to aerobic and anaerobic capacities. Experimental Physiology, 104, 209-219.
    1. Schäfer, L. U., Hayes, M., & Dekerle, J. (2019b). Creatine supplementation improves performance above critical power but does not influence the magnitude of neuromuscular fatigue at task failure. Experimental Physiology, 104, 1881-1891.
    1. Sidhu, S. K., Weavil, J. C., Mangum, T. S., Jessop, J. E., Richardson, R. S., Morgan, D. E., & Amann, M. (2017). Group III/IV locomotor muscle afferents alter motor cortical and corticospinal excitability and promote central fatigue during cycling exercise. Clinical Neurophysiology, 128, 44-55.
    1. Sidhu, S. K., Weavil, J. C., Venturelli, M., Garten, R. S., Rossman, M. J., Richardson, R. S., Gmelch, B. S., Morgan, D. E., & Amann, M. (2014). Spinal μ-opioid receptor-sensitive lower limb muscle afferents determine corticospinal responsiveness and promote central fatigue in upper limb muscle. The Journal of Physiology, 592, 5011-5024.
    1. Tabachnick, B. G., & Fidell, L. S. (2007). Using multivariate statistics (5th ed.). Allyn & Bacon/Pearson Education.
    1. Thomas, K., Elmeua, M., Howatson, G., & Goodall, S. (2016). Intensity-dependent contribution of neuromuscular fatigue after constant-load cycling. Medicine and Science in Sports and Exercise, 48, 1751-1760.
    1. Thomas, K., Goodall, S., Stone, M. R., Howatson, G., St Clair Gibson, A., & Ansley, L. (2015). Central and peripheral fatigue in male cyclists after 4-, 20-, and 40-km time trials. Medicine and Science in Sports and Exercise, 47, 537-546.
    1. Vanhatalo, A., Fulford, J., Dimenna, F. J., & Jones, A. M. (2010). Influence of hyperoxia on muscle metabolic responses and the power-duration relationship during severe-intensity exercise in humans: A 31P magnetic resonance spectroscopy study. Experimental Physiology, 95, 528-540.
    1. Watanabe, D., & Wada, M. (2016). Predominant cause of prolonged low-frequency force depression changes during recovery after in situ fatiguing stimulation of rat fast-twitch muscle. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 311, R919-R929.
    1. Wüthrich, T. U., Eberle, E. C., & Spengler, C. M. (2014). Locomotor and diaphragm muscle fatigue in endurance athletes performing time-trials of different durations. European Journal of Applied Physiology, 114, 1619-1633.
    1. Zarzissi, S., Bouzid, M. A., Zghal, F., Rebai, H., & Hureau, T. J. (2020a). Aging reduces the maximal level of peripheral fatigue tolerable and impairs exercise capacity. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 319, R617-R625.
    1. Zarzissi, S., Zghal, F., Bouzid, M. A., Hureau, T. J., Sahli, S., Ben Hassen, H., & Rebai, H. (2020b). Centrally-mediated regulation of peripheral fatigue during knee extensor exercise and consequences on the force-duration relationship in older men. European Journal of Sport Science, 20, 641-649.

Source: PubMed

スポンサーと協力者

医学的状態

薬物療法

3
購読する