Cited by 41Muscle activation and electromyography studiesCardiovascular and exercise physiologySports Performance and Training

Effects of fatiguing, submaximal high- versus low-torque isometric exercise on motor unit recruitment and firing behavior

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Muddle, Tyler W. D., Colquhoun, Ryan J., Magrini, Mitchel A., Luera, Micheal J., DeFreitas, Jason M., Jenkins, Nathaniel D. M.·2018·Physiological Reports

Abstract

The purpose of this investigation was to evaluate the effects of repeated, high- (HT: 70% MVIC) versus low-torque (LT: 30% MVIC) isometric exercise performed to failure on motor unit (MU) recruitment and firing behavior of the vastus lateralis. Eighteen resistance-trained males (23.1 ± 3.8 years) completed familiarization, followed by separate experimental sessions in which they completed either HT or LT exercise to failure in random order. LT exercise resulted in a greater time to task failure and a more dramatic decline in the muscle's force capacity, but the total work completed was similar for HT and LT exercise. An examination of the firing trains from 4670 MUs recorded during exercise revealed that firing rates generally increased during HT and LT exercise, but were higher during HT than LT exercise. Furthermore, recruitment thresholds (RT) did not significantly change during HT exercise, whereas the RT of the smallest MUs increased and the RT for the moderate to large MUs decreased during LT exercise. Both HT and LT exercise resulted in the recruitment of additional higher threshold MUs in order to maintain torque production. However, throughout exercise, HT required the recruitment of larger MUs than did LT exercise. In a few cases, however, MUs were recruited by individuals during LT exercise that were similar in size and original (pre) RT to those detected during HT exercise. Thus, the ability to achieve full MU recruitment during LT exercise may be dependent on the subject. Consequently, our data emphasize the task and subject dependency of muscle fatigue.

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  • Muddle et al. employed a decomposition technique and found that heavier loads were required to recruit the full spectrum of higher threshold motor units, although these results varied somewhat between individuals.

    “Analysis of the firing trains from more than 4000 motor units in the vastus lateralis muscle showed that heavier loads were required to recruit the full spectrum of higher threshold motor units, although these results varied somewhat between individuals.”

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  1. Adam, A., and C. J. De Luca. 2003 Recruitment order of motor units in human vastus lateralis muscle is maintained during fatiguing contractions. J. Neurophysiol. 90: 2919– 2927. 14615422
  2. Adam, A., and C. J. De Luca. 2005 Firing rates of motor units in human vastus lateralis muscle during fatiguing isometric contractions. J. Appl. Physiol. 99: 268– 280. 16036904
  3. Alkner, B. A., P. A. Tesch, and H. E. Berg. 2000 Quadriceps EMG/force relationship in knee extension and leg press. Med. Sci. Sports Exerc. 32: 459– 463. 10694132
  4. Amann, M., and J. A. Dempsey. 2008 Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance. J. Physiol. 586: 161– 173. 17962334 PMC2375542
  5. Amann, M., M. W. Eldridge, A. T. Lovering, M. K. Stickland, D. F. Pegelow, and J. A. Dempsey. 2006 Arterial oxygenation influences central motor output and exercise performance via effects on peripheral locomotor muscle fatigue in humans. J. Physiol. 575: 937– 952. 16793898 PMC1995675
  6. Amann, M., G. M. Blain, L. T. Proctor, J. J. Sebranek, D. F. Pegelow, and J. A. Dempsey. 2011 Implications of group III and IV muscle afferents for high‐intensity endurance exercise performance in humans. J. Physiol. 589: 5299– 5309. 21878520 PMC3225681
  7. Bigland‐Ritchie, B. R., N. J. Dawson, R. S. Johansson, and O. C. Lippold. 1986 Reflex origin for the slowing of motoneurone firing rates in fatigue of human voluntary contractions. J. Physiol. 379: 451– 459. 3560001 PMC1182907
  8. Bongiovanni, L. G., K. E. Hagbarth, and L. Stjernberg. 1990 Prolonged muscle vibration reducing motor output in maximal voluntary contractions in man. J. Physiol. 423: 15– 26. 2388149 PMC1189743
  9. Burnley, M., A. Vanhatalo, J. Fulford, and A. M. Jones. 2010 Similar metabolic perturbations during all‐out and constant force exhaustive exercise in humans: a 31P magnetic resonance spectroscopy study. Exp. Physiol. 95: 798– 807. 20360422
  10. Burnley, M., A. Vanhatalo, and A. M. Jones. 2012 Distinct profiles of neuromuscular fatigue during muscle contractions below and above the critical torque in humans. J. Appl. Physiol. 113: 215– 223. 22556396
  11. Carpentier, A., J. Duchateau, and K. Hainaut. 2001 Motor unit behaviour and contractile changes during fatigue in the human first dorsal interosseus. J. Physiol. 534: 903– 912. 11483719 PMC2278734
  12. Chidnok, W., F. J. DiMenna, J. Fulford, S. J. Bailey, P. F. Skiba, A. Vanhatalo, et al. 2013 Muscle metabolic responses during high‐intensity intermittent exercise measured by 31 P‐MRS: relationship to the critical power concept. Am. J. Physiol. Regul. Integr. Comp. Physiol. 305: R1085– R1092. 24068048 PMC3840318
  13. Contessa, P., and C. J. De Luca. 2013 Neural control of muscle force: indications from a simulation model. J. Neurophysiol. 109: 1548– 1570. 23236008 PMC3602935
  14. Contessa, P., C. J. De Luca, and J. C. Kline. 2016 The compensatory interaction between motor unit firing behavior and muscle force during fatigue. J. Neurophysiol. 116: 1579– 1585. 27385798 PMC5144693
  15. De Luca, C. J., and P. Contessa. 2012 Hierarchical control of motor units in voluntary contractions. J. Neurophysiol. 107: 178– 195. 21975447 PMC3349682
  16. De Luca, C. J., and Z. Erim. 1994 Common drive of motor units in regulation of muscle force. Trends Neurosci. 17: 299– 305. 7524216
  17. De Luca, C. J., and E. C. Hostage. 2010 Relationship between firing rate and recruitment threshold of motoneurons in voluntary isometric contractions. J. Neurophysiol. 104: 1034‐ 1046. 20554838 PMC2934917
  18. De Luca, C. J., and S. H. Nawab. 2011 Reply to Farina and Enoka: the reconstruct‐and‐test approach is the most appropriate validation for surface EMG signal decomposition to date. J. Neurophysiol. 105: 983– 984. 21304161
  19. De Luca, C. J., A. Adam, R. Wotiz, L. D. Gilmore, and S. H. Nawab. 2006 Decomposition of surface EMG signals. J. Neurophysiol. 96: 1646– 1657. 16899649
  20. Duchateau, J., and K. Hainaut. 1993 Behaviour of short and long latency reflexes in fatigued human muscles. J. Physiol. 471: 787– 799. 8120833 PMC1143989
  21. Enoka, R. M., and J. Duchateau. 2015 Inappropriate interpretation of surface EMG signals and muscle fiber characteristics impedes understanding of the control of neuromuscular function. J. Appl. Physiol. 119: 1516– 1518. 26159758
  22. Enoka, R. M., G. A. Robinson, and A. R. Kossev. 1989 Task and fatigue effects on low‐threshold motor units in human hand muscle. J. Neurophysiol. 62: 1344– 1359. 2600629
  23. Farina, D., A. Holobar, M. Gazzoni, D. Zazula, R. Merletti, and R. M. Enoka. 2009 Adjustments differ among low‐threshold motor units during intermittent, isometric contractions. J. Neurophysiol. 101: 350– 359. 19004996 PMC2637005
  24. Fuglevand, A. J., K. M. Zackowski, K. A. Huey, and R. M. Enoka. 1993 Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. J. Physiol. 460: 549– 572. 8387589 PMC1175228
  25. Gagnon, P., D. Saey, I. Vivodtzev, L. Laviolette, V. Mainguy, J. Milot, et al. 2009 Impact of preinduced quadriceps fatigue on exercise response in chronic obstructive pulmonary disease and healthy subjects. J. Appl. Physiol. 107: 832– 840. 19574500
  26. Garland, S. J., and A. J. McComas. 1990 Reflex inhibition of human soleus muscle during fatigue. J. Physiol. 429: 17– 27. 2277345 PMC1181684
  27. Henneman, E. 1957 Relation between size of neurons and their susceptibility to discharge. Science 126: 1345– 1347. 13495469
  28. Herda, T. J., J. A. Siedlik, M. A. Trevino, M. A. Cooper, and J. P. Weir. 2015 Motor unit control strategies of endurance‐versus resistance‐trained individuals. Muscle Nerve 52: 832– 843. 25664898
  29. Hogan, M. C., R. S. Richardson, and L. J. Haseler. 1999 Human muscle performance and PCr hydrolysis with varied inspired oxygen fractions: a 31 P‐MRS study. J. Appl. Physiol. 86: 1367– 1373. 10194224
  30. Hu, X., W. Z. Rymer, and N. L. Suresh. 2013a Motor unit pool organization examined via spike‐triggered averaging of the surface electromyogram. J. Neurophysiol. 110: 1205– 1220. 23699053 PMC4073930
  31. Hu, X., W. Z. Rymer, and N. L. Suresh. 2013b Reliability of spike triggered averaging of the surface electromyogram for motor unit action potential estimation. Muscle Nerve 48: 557– 570. 23424086
  32. Hu, X., W. Z. Rymer, and N. L. Suresh. 2013c Assessment of validity of a high‐yield surface electromyogram decomposition. J. Neuroeng. Rehabil. 10: 99. 24059856 PMC3849018
  33. Hu, X., W. Z. Rymer, and N. L. Suresh. 2014a Control of motor unit firing during step‐like increases in voluntary force. Front. Hum. Neurosci. 8: 721. 25309395 PMC4160994
  34. Hu, X., W. Z. Rymer, and N. L. Suresh. 2014b Motor unit firing rate patterns during voluntary muscle force generation: a simulation study. J. Neural Eng. 11: 026015. 24658323
  35. Hureau, T. J., G. P. Ducrocq, and G. M. Blain. 2016 Peripheral and central fatigue development during all‐out repeated cycling sprints. Med. Sci. Sports Exerc. 48: 391– 401. 26496420
  36. Jenkins, N. D. M., T. J. Housh, H. C. Bergstrom, K. C. Cochrane, E. C. Hill, C. M. Smith, et al. 2015 Muscle activation during three sets to failure at 80 vs. 30% 1RM resistance exercise. Euro. J. Appl. Physiol. 115: 2335– 2347. 26159316
  37. Kelly, L. A., S. Racinais, and A. G. Cresswell. 2013 Discharge properties of abductor hallucis before, during, and after an isometric fatigue task. J. Neurophysiol. 110: 891– 898. 23678020
  38. Kernell, D., and A. W. Monster. 1982 Motoneurone properties and motor fatigue. Exp. Brain Res. 46: 197– 204. 6284540
  39. Kniffki, K. D., S. Mense, and R. F. Schmidt. 1978 Responses of group IV afferent units from skeletal muscle to stretch, contraction and chemical stimulation. Exp. Brain Res. 31: 511– 522. 658178
  40. Light, A. R., R. W. Hughen, J. Zhang, J. Rainier, Z. Liu, and J. Lee. 2008 Dorsal root ganglion neurons innervating skeletal muscle respond to physiological combinations of protons, ATP, and lactate mediated by ASIC, P2X, and TRPV1. J. Neurophys. 100: 1184– 1201. PMC6195653 18509077
  41. Lind, A. R., and J. S. Petrofsky. 1979 Amplitude of the surface electromyogram during fatiguing isometric contractions. Muscle Nerve 2: 257– 264. 492202
  42. Macefield, G., K. E. Hagbarth, R. Gorman, S. C. Gandevia, and D. Burke. 1991 Decline in spindle support to alpha‐motoneurones during sustained voluntary contractions. J. Physiol. 440: 497– 512. 1839558 PMC1180165
  43. McManus, L., X. Hu, W. Z. Rymer, M. M. Lowery, and N. L. Suresh. 2015 Changes in motor unit behavior following isometric fatigue of the first dorsal interosseous muscle. J. Neurophys. 113: 3186– 3196. PMC4432683 25761952
  44. Mense, S. 1977 Nervous outflow from skeletal muscle following chemical noxious stimulation. J. Physiol. 267: 75– 88. 141496 PMC1283603
  45. Mettler, J. A., and L. Griffin. 2016 Muscular endurance training and motor unit firing patterns during fatigue. Exp. Brain Res. 234: 267– 276. 26449966
  46. Milner‐Brown, H. S., R. B. Stein, and R. Yemm. 1973 The orderly recruitment of human motor units during voluntary isometric contractions. J. Physiol. 230: 359– 370. 4350770 PMC1350367
  47. Mottram, C. J., J. M. Jakobi, J. G. Semmler, and R. M. Enoka. 2005 Motor‐unit activity differs with load type during a fatiguing contraction. J. Neurophys. 93: 1381– 1392. 15483059
  48. Nawab, S. H., S. S. Chang, and C. J. De Luca. 2010 High‐yield decomposition of surface EMG signals. Clin. Neurophysiol. 121: 1602– 1615. 20430694 PMC2932793
  49. Petrofsky, J. S., R. M. Glaser, C. A. Phillips, A. R. Lind, and C. Williams. 1982 Evaluation of the amplitude and frequency components of the surface EMG as an index of muscle fatigue. Ergonomics 25: 213– 223. 7117234
  50. Pope, Z. K., G. M. Hester, F. M. Benik, and J. M. DeFreitas. 2016 Action potential amplitude as a noninvasive indicator of motor unit‐specific hypertrophy. J. Neurophys. 115: 2608– 2614. PMC4922476 26936975
  51. Potvin, J. R., and A. J. Fuglevand. 2017b A motor‐unit based model of muscle fatigue. PLoS Comput. Biol. 13: e1005581. 28574981 PMC5473583
  52. Romer, L. M., H. C. Haverkamp, M. Amann, A. T. Lovering, D. F. Pegelow, and J. A. Dempsey. 2007 Effect of acute severe hypoxia on peripheral fatigue and endurance capacity in healthy humans. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292: R598– R606. 16959862
  53. Rossman, M. J., R. S. Garten, M. Venturelli, M. Amann, and R. S. Richardson. 2014 The role of active muscle mass in determining the magnitude of peripheral fatigue during dynamic exercise. Am. J. Physiol. Regul. Integr. Comp. Physiol. 306: R934– R940. 24740653 PMC4159732
  54. Rotto, D. M., and M. P. Kaufman. 1988 Effect of metabolic products of muscular contraction on discharge of group III and IV afferents. J. Appl. Physiol. 64: 2306– 2313. 3136123
  55. de Ruiter, C. J., M. J. Elzinga, P. W. Verdijk, W. van Mechelen, and A. de Haan. 2005 Changes in force, surface and motor unit EMG during post‐exercise development of low frequency fatigue in vastus lateralis muscle. Eur. J. Appl. Physiol. 94: 659– 669. 15887021
  56. Sidhu, S. K., J. C. Weavil, M. Venturelli, R. S. Garten, M. J. Rossman, R. S. Richardson, et al. 2014 Spinal μ‐opioid receptor‐sensitive lower limb muscle afferents determine corticospinal responsiveness and promote central fatigue in upper limb muscle. J. Physiol. 592: 5011– 5024. 25172953 PMC4259540
  57. Trevino, M. A., T. J. Herda, A. C. Fry, P. M. Gallagher, J. P. Vardiman, E. M. Mosier, et al. 2016 Influence of the contractile properties of muscle on motor unit firing rates during a moderate‐intensity contraction in vivo. J. Neurophysiol. 116: 552– 562. 27146989 PMC4978784
  58. Vanhatalo, A., J. Fulford, F. J. DiMenna, and A. M. Jones. 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. Exp. Physiol. 95: 528– 540. 20028850
  59. Vila‐Chã, C., D. Falla, M. V. Correia, and D. Farina. 2012 Adjustments in motor unit properties during fatiguing contractions after training. Med. Sci. Sports Exerc. 44: 616– 624. 21904248
  60. Woods, J. J., F. Furbush, and B. R. Bigland‐Ritchie. 1987 Evidence for a fatigue‐induced reflex inhibition of motoneuron firing rates. J. Neurophysiol. 58: 125– 137. 3039078
  61. Zaheer, F., S. H. Roy, and C. J. De Luca. 2012 Preferred sensor sites for surface EMG signal decomposition. Physiol. Meas. 33: 195– 206. 22260842 PMC3428954

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Authors
Muddle, T. W. D., Colquhoun, R. J., Magrini, M. A., Luera, M. J., DeFreitas, J. M., & Jenkins, N. D. M.
Affiliations
Oklahoma State University (US)
Corresponding author
Jenkins, Nathaniel D. M.
Venue
Physiological Reports
Publisher
Wiley
Published
2018-04
Volume
6
Issue
8
Pages
e13675
ISSN
2051-817X (ISSN-L)
OpenAlex
W2799734388
Cited by
41
References
1
Citations by year
2026: 2 · 2025: 5 · 2024: 5 · 2023: 8 · 2022: 3 · 2021: 4 · 2020: 5 · 2019: 7 · 2018: 2
FWCI
1.75
Type
journal article
Language
en
Open access
Locations
  • Physiological Reports (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Topics
  • Physical Sciences › Engineering › Biomedical Engineering › Muscle activation and electromyography studies
  • Health Sciences › Medicine › Complementary and alternative medicine › Cardiovascular and exercise physiology
  • Health Sciences › Medicine › Orthopedics and Sports Medicine › Sports Performance and Training
Keywords
motor unit recruitment, isometric exercise, vastus lateralis, motor unit recruitment threshold, firing rate, muscle fatigue, task dependencies, resistance-trained men
MeSH terms
Action Potentials, Adult, Humans, Isometric Contraction, Male, Motor Neurons, Recruitment, Neurophysiological, Exercise, Muscle, Skeletal, Muscle Fatigue, Torque, Young Adult

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