Changes in motor unit behaviour across repeated bouts of eccentric exercise.
fatigue
high‐density electromyography
motoneuron
muscle damage
recovery
Journal
Experimental physiology
ISSN: 1469-445X
Titre abrégé: Exp Physiol
Pays: England
ID NLM: 9002940
Informations de publication
Date de publication:
03 Sep 2024
03 Sep 2024
Historique:
received:
29
05
2024
accepted:
13
08
2024
medline:
3
9
2024
pubmed:
3
9
2024
entrez:
3
9
2024
Statut:
aheadofprint
Résumé
Unaccustomed eccentric exercise (EE) is protective against muscle damage following a subsequent bout of similar exercise. One hypothesis suggests the existence of an alteration in motor unit (MU) behaviour during the second bout, which might contribute to the adaptive response. Accordingly, the present study investigated MU changes during repeated bouts of EE. During two bouts of exercise where maximal lengthening dorsiflexion (10 repetitions × 10 sets) was performed 3 weeks apart, maximal voluntary isometric torque (MVIC) and MU behaviour (quantified using high-density electromyography; HDsEMG) were measured at baseline, during (after set 5), and post-EE. The HDsEMG signals were decomposed into individual MU discharge timings, and a subset were tracked across each time point. MVIC was reduced similarly in both bouts post-EE (Δ27 vs. 23%, P = 0.144), with a comparable amount of total work performed (∼1,300 J; P = 0.905). In total, 1,754 MUs were identified and the decline in MVIC was accompanied by a stepwise increase in discharge rate (∼13%; P < 0.001). A decrease in relative recruitment was found immediately after EE in Bout 1 versus baseline (∼16%; P < 0.01), along with reductions in derecruitment thresholds immediately after EE in Bout 2. The coefficient of variation of inter-spike intervals was lower in Bout 2 (∼15%; P < 0.001). Our data provide new information regarding a change in MU behaviour during the performance of a repeated bout of EE. Importantly, such changes in MU behaviour might contribute, at least in part, to the repeated bout phenomenon.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024 The Author(s). Experimental Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.
Références
Ansdell, P., Brownstein, C. G., Škarabot, J., Hicks, K. M., Simoes, D. C., Thomas, K., Howatson, G., Hunter, S. K., & Goodall, S. (2019). Menstrual cycle‐associated modulations in neuromuscular function and fatigability of the knee extensors in eumenorrheic women. Journal of Applied Physiology, 126(6), 1701–1712.
Ansdell, P., Brownstein, C. G., Škarabot, J., Angius, L., Kidgell, D., Frazer, A., Hicks, K. M., Durbaba, R., Howatson, G., Goodall, S., & Thomas, K. (2020). Task‐specific strength increases after lower‐limb compound resistance training occurred in the absence of corticospinal changes in vastus lateralis. Experimental Physiology, 105(7), 1132–1150.
Balshaw, T. G., Pahar, M., Chesham, R., Macgregor, L. J., & Hunter, A. M. (2017). Reduced firing rates of high threshold motor units in response to eccentric overload. Physiological Reports, 5(2), e13111.
Barbero, M., Merletti, R., & Rainoldi, A. (2012). Atlas of muscle innervation zones: Understanding surface electromyography and its applications. Springer Science & Business Media.
Baudry, S., Klass, M., Pasquet, B., & Duchateau, J. (2007). Age‐related fatigability of the ankle dorsiflexor muscles during concentric and eccentric contractions. European Journal of Applied Physiology, 100(5), 515–525.
Beretta Piccoli, M., Rainoldi, A., Heitz, C., Wüthrich, M., Boccia, G., Tomasoni, E., Spirolazzi, C., Egloff, M., & Barbero, M. (2014). Innervation zone locations in 43 superficial muscles: Toward a standardization of electrode positioning. Muscle & Nerve, 49, 413–421.
Bigland‐Ritchie, B., Fuglevand, A. J., & Thomas, C. K. (1998). Contractile properties of human motor units: Is man a gat? The Neuroscientist, 4(4), 240–249.
Bingham, A., Arjunan, S., Jelfs, B., & Kumar, D. (2017). Normalised mutual information of high‐density surface electromyography during muscle fatigue. Entropy, 19(7), 697.
Bruce, C. D., Ruggiero, L., Dix, G. U., Cotton, P. D., & Mcneil, C. J. (2021). Females and males do not differ for fatigability, muscle damage and magnitude of the repeated bout effect following maximal eccentric contractions. Applied Physiology, Nutrition, and Metabolism, 46(3), 238–246.
Burt, D., Hayman, O., Forsyth, J., Doma, K., & Twist, C. (2020). Monitoring indices of exercise‐induced muscle damage and recovery in male field hockey: Is it time to retire creatine kinase? Science & Sports, 35, 402–404.
Byrne, C., O'keeffe, D., Donnelly, A., & Lyons, G. (2007). Effect of walking speed changes on tibialis anterior EMG during healthy gait for FES envelope design in drop foot correction. Journal of Electromyography and Kinesiology, 17(5), 605–616.
Casolo, A., Farina, D., Falla, D., Bazzucchi, I., Felici, F., & Del Vecchio, A. (2020). Strength Training Increases Conduction Velocity of High‐Threshold Motor Units. Medicine and Science in Sports and Exercise, 52(4), 955–967.
Castronovo, A. M., Negro, F., Conforto, S., & Farina, D. (2015). The proportion of common synaptic input to motor neurons increases with an increase in net excitatory input. Journal of Applied Physiology, 119(11), 1337–1346.
Chen, T. C. (2003). Effects of a second bout of maximal eccentric exercise on muscle damage and electromyographic activity. European Journal of Applied Physiology, 89(2), 115–121.
Chen, T. C., Chen, H. L., Cheng, L. F., Chou, T. Y., & Nosaka, K. (2021). Effect of leg eccentric exercise on muscle damage of the elbow flexors after maximal eccentric exercise. Medicine and Science in Sports and Exercise, 53(7), 1473–1481.
Chen, T. C., Lin, K. Y., Chen, H. L., Lin, M. J., & Nosaka, K. (2011). Comparison in eccentric exercise‐induced muscle damage among four limb muscles. European Journal of Applied Physiology, 111(2), 211–223.
Dartnall, T. J., Nordstrom, M. A., & Semmler, J. G. (2008). Motor unit synchronization is increased in biceps brachii after exercise‐induced damage to elbow flexor muscles. Journal of Neurophysiology, 99(2), 1008–1019.
Dartnall, T. J., Nordstrom, M. A., & Semmler, J. G. (2011). Adaptations in biceps brachii motor unit activity after repeated bouts of eccentric exercise in elbow flexor muscles. Journal of Neurophysiology, 105(3), 1225–1235.
Dartnall, T. J., Rogasch, N. C., Nordstrom, M. A., & Semmler, J. G. (2009). Eccentric muscle damage has variable effects on motor unit recruitment thresholds and discharge patterns in elbow flexor muscles. Journal of Neurophysiology, 102(1), 413–423.
Del Vecchio, A., Casolo, A., Dideriksen, J., Aagaard, P., Felici, F., Falla, D., & Farina, D. (2022). Lack of increased rate of force development after strength training is explained by specific neural, not muscular, motor unit adaptations. Journal of Applied Physiology, 132(1), 84–94.
Del Vecchio, A., Casolo, A., Negro, F., Scorcelletti, M., Bazzucchi, I., Enoka, R., Felici, F., & Farina, D. (2019). The increase in muscle force after 4 weeks of strength training is mediated by adaptations in motor unit recruitment and rate coding. The Journal of Physiology, 597(7), 1873–1887.
Del Vecchio, A., & Farina, D. (2019). Interfacing the neural output of the spinal cord: Robust and reliable longitudinal identification of motor neurons in humans. Journal of Neural Engineering, 17(1), 016003.
Del Vecchio, A., Holobar, A., Falla, D., Felici, F., Enoka, R. M., & Farina, D. (2020). Tutorial: Analysis of motor unit discharge characteristics from high‐density surface EMG signals. Journal of Electromyography and Kinesiology, 53, 102426.
Deyhle, M. R., Gier, A. M., Evans, K. C., Eggett, D. L., Nelson, W. B., Parcell, A. C., & Hyldahl, R. D. (2016). Skeletal muscle inflammation following repeated bouts of lengthening contractions in humans. Frontiers in Physiology, 6, 424.
Doma, K., Schumann, M., Leicht, A. S., Heilbronn, B. E., Damas, F., & Burt, D. (2017). The repeated bout effect of traditional resistance exercises on running performance across 3 bouts. Applied Physiology, Nutrition and Metabolism, 42(9), 978–985.
Duchateau, J., & Enoka, R. M. (2016). Neural control of lengthening contractions. Journal of Experimental Biology, 219(2), 197–204.
Duclay, J., Martin, A., Robbe, A., & Pousson, M. (2008). Spinal reflex plasticity during maximal dynamic contractions after eccentric training. Medicine and Science in Sports and Exercise, 40(4), 722–734.
Enoka, R. M. (1996). Eccentric contractions require unique activation strategies by the nervous system. Journal of Applied Physiology, 81(6), 2339–2346.
Enoka, R. M., Trayanova, N., Laouris, Y., Bevan, L., Reinking, R. M., & Stuart, D. G. (1992). Fatigue‐related changes in motor unit action potentials of adult cats. Muscle & Nerve, 15, 138–150.
Frančič, A., & Holobar, A. (2021). On the reuse of motor unit filters in high density surface electromyograms recorded at different contraction levels. IEEE Access, 9, 115227–115236.
Friden, J., & Lieber, R. L. (2001). Eccentric exercise‐induced injuries to contractile and cytoskeletal muscle fibre components. Acta Physiologica Scandinavica, 171(3), 321–326.
Gandevia, S. C. (2001). Spinal and supraspinal factors in human muscle fatigue. Physiological Reviews, 81(4), 1725–1789.
Garland, S., Enoka, R., Serrano, L., & Robinson, G. (1994). Behavior of motor units in human biceps brachii during a submaximal fatiguing contraction. Journal of Applied Physiology, 76(6), 2411–2419.
Gault, M. L., & Willems, M. E. T. (2013). Isometric strength and steadiness adaptations of the knee extensor muscles to level and downhill treadmill walking in older adults. Biogerontology, 14(2), 197–208.
Giboin, L. S., Tokuno, C., Kramer, A., Henry, M., & Gruber, M. (2020). Motor learning induces time‐dependent plasticity that is observable at the spinal cord level. The Journal of Physiology, 598(10), 1943–1963.
Goodall, S., Thomas, K., Barwood, M., Keane, K., Gonzalez, J. T., St Clair Gibson, A., & Howatson, G. (2017). Neuromuscular changes and the rapid adaptation following a bout of damaging eccentric exercise. Acta Physiologica, 220(4), 486–500.
Guo, Y., Jones, E. J., Inns, T. B., Ely, I. A., Stashuk, D. W., Wilkinson, D. J., Smith, K., Piasecki, J., Phillips, B. E., & Atherton, P. J. (2022). Neuromuscular recruitment strategies of the vastus lateralis according to sex. Acta Physiologica, 235(2), e13803.
Heckman, C., Gorassini, M. A., & Bennett, D. J. (2005). Persistent inward currents in motoneuron dendrites: Implications for motor output. Muscle & Nerve, 31, 135–156.
Hirono, T., Kunugi, S., Yoshimura, A., Holobar, A., & Watanabe, K. (2022). Acute changes in motor unit discharge property after concentric versus eccentric contraction exercise in knee extensor. Journal of Electromyography and Kinesiology, 67, 102704.
Hohmann, H. (2009). Examining the efficacy, safety, and patient acceptability of the etonogestrel implantable contraceptive. Patient Prefer Adherence, 3, 205–11.
Holobar, A., Farina, D., Gazzoni, M., Merletti, R., & Zazula, D. (2009). Estimating motor unit discharge patterns from high‐density surface electromyogram. Clinical Neurophysiology, 120(3), 551–562.
Holobar, A., Minetto, M. A., & Farina, D. (2014). Accurate identification of motor unit discharge patterns from high‐density surface EMG and validation with a novel signal‐based performance metric. Journal of Neural Engineering, 11(1), 016008.
Holobar, A., & Zazula, D. (2007). Multichannel blind source separation using convolution kernel compensation. IEEE Transactions on Signal Processing, 55(9), 4487–4496.
Howatson, G., & Van Someren, K. A. (2007). Evidence of a contralateral repeated bout effect after maximal eccentric contractions. European Journal of Applied Physiology, 101(2), 207–214.
Howell, J., Fuglevand, A., Walsh, M., & Bigland‐Ritchie, B. (1995). Motor unit activity during isometric and concentric‐eccentric contractions of the human first dorsal interosseus muscle. Journal of Neurophysiology, 74(2), 901–904.
Hwang, I.‐S., Lin, Y.‐T., Huang, C.‐C., & Chen, Y.‐C. (2020). Fatigue‐related modulation of low‐frequency common drive to motor units. European Journal of Applied Physiology, 120(6), 1305–1317.
Hyldahl, R. D., Chen, T. C., & Nosaka, K. (2017). Mechanisms and mediators of the skeletal muscle repeated bout effect. Exercise and Sport Sciences Reviews, 45(1), 24–33.
Hyldahl, R. D., Nelson, B., Xin, L., Welling, T., Groscost, L., Hubal, M. J., Chipkin, S., Clarkson, P. M., & Parcell, A. C. (2015). Extracellular matrix remodeling and its contribution to protective adaptation following lengthening contractions in human muscle. The Federation of American Societies for Experimental Biology Journal, 29(7), 2894–2904.
Jakobsson, F., Borg, K., Edström, L., & Grimby, L. (1988). Use of motor units in relation to muscle fiber type and size in man. Muscle & Nerve, 11, 1211–1218.
Janecki, D., Jaskólska, A., Marusiak, J., Andrzejewska, R., & Jaskólski, A. (2014). Twitch mechanical properties after repeated eccentric exercise of the elbow flexors. Applied Physiology, Nutrition, and Metabolism, 39(1), 74–81.
Jenz, S. T., Beauchamp, J. A., Gomes, M. M., Negro, F., Heckman, C., & Pearcey, G. E. (2023). Estimates of persistent inward currents in lower limb motoneurons are larger in females than in males. Journal of Neurophysiology, 129(6), 1322–1333.
Jones, E. J., Guo, Y., Martinez‐Valdes, E., Negro, F., Stashuk, D. W., Atherton, P. J., Phillips, B. E., & Piasecki, M. (2023). Acute adaptation of central and peripheral motor unit features to exercise‐induced fatigue differs with concentric and eccentric loading. Experimental Physiology, 108(6), 827–837.
Komi, P. V., & Rusko, H. (1974). Quantitative evaluation of mechanical and electrical changes during fatigue loading of eccentric and concentric work. Scandinavian Journal of Rehabilitation Medicine Supplement, 3, 121–126.
Kornatz, K. W., Christou, E. A., & Enoka, R. M. (2005). Practice reduces motor unit discharge variability in a hand muscle and improves manual dexterity in old adults. Journal of Applied Physiology, 98(6), 2072–2080.
Lee, R. H., & Heckman, C. J. (2000). Adjustable amplification of synaptic input in the dendrites of spinal motoneurons in vivo. Journal of Neuroscience, 20(17), 6734–6740.
Linnamo, V., Moritani, T., Nicol, C., & Komi, P. (2003). Motor unit activation patterns during isometric, concentric and eccentric actions at different force levels. Journal of Electromyography and Kinesiology, 13(1), 93–101.
Lulic‐Kuryllo, T., & Inglis, J. G. (2022). Sex differences in motor unit behaviour: A review. Journal of Electromyography and Kinesiology, 66, 102689.
Macgregor, L. J., & Hunter, A. M. (2018). High‐threshold motor unit firing reflects force recovery following a bout of damaging eccentric exercise. PLoS ONE, 13(4), e0195051.
Martinez‐Valdes, E., Laine, C. M., Falla, D., Mayer, F., & Farina, D. (2016). High‐density surface electromyography provides reliable estimates of motor unit behavior. Clinical Neurophysiology, 127(6), 2534–2541.
Martinez‐Valdes, E., Negro, F., Farina, D., & Falla, D. (2020). Divergent response of low‐ versus high‐threshold motor units to experimental muscle pain. The Journal of Physiology, 598(11), 2093–2108.
Martinez‐Valdes, E., Negro, F., Laine, C. M., Falla, D., Mayer, F., & Farina, D. (2017). Tracking motor units longitudinally across experimental sessions with high‐density surface electromyography. The Journal of Physiology, 595(5), 1479–1496.
Mchugh, M. P. (2003). Recent advances in the understanding of the repeated bout effect: The protective effect against muscle damage from a single bout of eccentric exercise. Scandinavian Journal of Medicine & Science in Sports, 13(2), 88–97.
Mchugh, M. P., Connolly, D. A., Eston, R. G., & Gleim, G. W. (1999). Exercise‐induced muscle damage and potential mechanisms for the repeated bout effect. Sports Medicine, 27(3), 157–170.
Mchugh, M. P., Connolly, D. A., Eston, R. G., & Gleim, G. W. (2000). Electromyographic analysis of exercise resulting in symptoms of muscle damage. Journal of Sports Sciences, 18(3), 163–172.
Minahan, C., Joyce, S., Bulmer, A. C., Cronin, N., & Sabapathy, S. (2015). The influence of estradiol on muscle damage and leg strength after intense eccentric exercise. European Journal of Applied Physiology, 115(7), 1493–1500.
Minett, G. M., & Duffield, R. (2014). Is recovery driven by central or peripheral factors? A role for the brain in recovery following intermittent‐sprint exercise. Frontiers in Physiology, 5, 24.
Morawetz, D., Blank, C., Koller, A., Arvandi, M., Siebert, U., & Schobersberger, W. (2020). Sex‐related differences after a single bout of maximal eccentric exercise in response to acute effects: A systematic review and meta‐analysis. The Journal of Strength & Conditioning Research, 34, 2697–2707.
Nardone, A., Romano, C., & Schieppati, M. (1989). Selective recruitment of high‐threshold human motor units during voluntary isotonic lengthening of active muscles. The Journal of Physiology, 409(1), 451–471.
Negro, F., & Farina, D. (2012). Factors influencing the estimates of correlation between motor unit activities in humans. PloS ONE, 7(9), e44894.
Nosaka, K., & Clarkson, P. M. (1995). Muscle damage following repeated bouts of high force eccentric exercise. Medicine and Science in Sports and Exercise, 27(9), 1263–1269.
Oya, T., Riek, S., & Cresswell, A. G. (2009). Recruitment and rate coding organisation for soleus motor units across entire range of voluntary isometric plantar flexions. The Journal of Physiology, 587(19), 4737–4748.
Pasquet, B., Carpentier, A., & Duchateau, J. (2006). Specific modulation of motor unit discharge for a similar change in fascicle length during shortening and lengthening contractions in humans. The Journal of Physiology, 577(2), 753–765.
Pasquet, B., Carpentier, A., Duchateau, J., & Hainaut, K. (2000). Muscle fatigue during concentric and eccentric contractions. Muscle & Nerve, 23, 1727–1735.
Peake, J. M., Neubauer, O., Della Gatta, P. A., & Nosaka, K. (2017). Muscle damage and inflammation during recovery from exercise. Journal of Applied Physiology, 122(3), 559–570.
Piitulainen, H., Holobar, A., & Avela, J. (2012). Changes in motor unit characteristics after eccentric elbow flexor exercise. Scandinavian Journal of Medicine & Science in Sports, 22(3), 418–429.
Pincheira, P. A., Hoffman, B. W., Cresswell, A. G., Carroll, T. J., Brown, N. A., & Lichtwark, G. A. (2018). The repeated bout effect can occur without mechanical and neuromuscular changes after a bout of eccentric exercise. Scandinavian Journal of Medicine & Science in Sports, 28, 2123–2134.
Pincheira, P. A., Martinez‐Valdes, E., Guzman‐Venegas, R., Falla, D., Garrido, M. I., Cresswell, A. G., & Lichtwark, G. A. (2021). Regional changes in muscle activity do not underlie the repeated bout effect in the human gastrocnemius muscle. Scandinavian Journal of Medicine & Science in Sports, 31, 799–812.
Plattner, K., Baumeister, J., Lamberts, R. P., & Lambert, M. I. (2011). Dissociation in changes in EMG activation during maximal isometric and submaximal low force dynamic contractions after exercise‐induced muscle damage. Journal of Electromyography and Kinesiology, 21(3), 542–550.
Power, G. A., Rice, C. L., & Vandervoort, A. A. (2012). Residual force enhancement following eccentric induced muscle damage. Journal of Biomechanics, 45(10), 1835–1841.
Prasartwuth, O., Suteebut, R., Chawawisuttikool, J., Yavuz, U. S., & Turker, K. S. (2019). Using first bout effect to study the mechanisms underlying eccentric exercise induced force loss. Journal of Bodywork and Movement Therapies, 23(1), 48–53.
Rodriguez‐Falces, J., Negro, F., & Farina, D. (2017). Correlation between discharge timings of pairs of motor units reveals the presence but not the proportion of common synaptic input to motor neurons. Journal of Neurophysiology, 117(4), 1749–1760.
Semmler, J. G. (2014). Motor unit activity after eccentric exercise and muscle damage in humans. Acta Physiologica, 210(4), 754–767.
Sewright, K. A., Hubal, M. J., Kearns, A., Holbrook, M. T., & Clarkson, P. M. (2008). Sex differences in response to maximal eccentric exercise. Medicine and Science in Sports and Exercise, 40(2), 242–251.
Škarabot, J., Ansdell, P., Temesi, J., Howatson, G., Goodall, S., & Durbaba, R. (2019). Neurophysiological responses and adaptation following repeated bouts of maximal lengthening contractions in young and older adults. Journal of Applied Physiology, 127(5), 1224–1237.
Starbuck, C., & Eston, R. G. (2012). Exercise‐induced muscle damage and the repeated bout effect: Evidence for cross transfer. European Journal of Applied Physiology, 112(3), 1005–1013.
Taylor, A. M., Christou, E. A., & Enoka, R. M. (2003). Multiple features of motor‐unit activity influence force fluctuations during isometric contractions. Journal of Neurophysiology, 90(2), 1350–1361.
Taylor, J. L., Amann, M., Duchateau, J., Meeusen, R., & Rice, C. L. (2016). Neural contributions to muscle fatigue: From the brain to the muscle and back again. Medicine and Science in Sports and Exercise, 48(11), 2294.
Trevino, M., Sterczala, A., Miller, J., Wray, M., Dimmick, H., Ciccone, A., Weir, J., Gallagher, P., Fry, A., & Herda, T. (2019). Sex‐related differences in muscle size explained by amplitudes of higher‐threshold motor unit action potentials and muscle fibre typing. Acta Physiologica, 225(4), e13151.
Urh, F., & Holobar, A. (2020). Automatic identification of individual motor unit firing accuracy from high‐density surface electromyograms. IEEE Transactions on Neural Systems and Rehabilitation Engineering, 28(2), 419–426.
Vangsgaard, S., Taylor, J. L., Hansen, E. A., & Madeleine, P. (2014). Changes in H reflex and neuromechanical properties of the trapezius muscle after 5 weeks of eccentric training: A randomized controlled trial. Journal of Applied Physiology, 116(12), 1623–1631.
Warren, G. L., Hermann, K. M., Ingalls, C. P., Masselli, M. R., & Armstrong, R. (2000). Decreased EMG median frequency during a second bout of eccentric contractions. Medicine and Science in Sports and Exercise, 32(4), 820–829.
Wilkinson, R. D., Mazzo, M. R., & Feeney, D. F. (2022). Rethinking the statistical analysis of neuromechanical data. Exercise and Sport Sciences Reviews, 10, 1249.