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Modulation of motor unit discharge rate and H-reflex amplitude during submaximal fatigue of the human soleus muscle

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Abstract

Declining motor unit discharge rates and H-reflex amplitude have been observed in separate experiments during fatiguing submaximal contractions in humans. The purpose of this experiment was to investigate motor unit discharge rate, H-reflex amplitude, and twitch contractile properties concurrently during a fatiguing submaximal isometric contraction of the ankle plantarflexors. Eleven healthy subjects performed fatiguing contractions of low force (25% maximal voluntary contraction (MVC)) or high force (42–66% MVC). Hoffmann (H)-reflexes, muscle compound action potentials (M-waves), twitch contractile properties, and motor unit discharges were recorded from the soleus muscle. In the low-force fatigue task, motor unit firing rate increased gradually over time, whereas the resting H-reflex was significantly depressed at 15% of endurance time and remained quasiconstant for the rest of the task. This suggests that the processes mediating the resting H-reflex depression are relatively independent of those modulating the motor unit firing rate during a low-force fatigue task. In the high-force fatigue task, a decline in the average motor unit discharge rate was accompanied by a decrease in the resting H-reflex amplitude and a prolongation of the twitch half-relaxation time (HRT) at the completion of the fatigue task. Overall, motor unit firing rate was modulated in parallel with changes in the twitch HRT, consistent with the muscle wisdom hypothesis.

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References

  • Allen GM, Gandevia SC, McKenzie DK (1995) Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 18:593–600

    CAS  PubMed  Google Scholar 

  • Bigland-Ritchie B, Johansson R, Lippold OCJ, Smith S, Woods JJ (1983a) Changes in motoneurone firing rates during sustained maximal voluntary contractions. J Physiol 340:335–346

    CAS  PubMed  Google Scholar 

  • Bigland-Ritchie B, Johansson R, Lippold OCJ, Woods JJ (1983b) Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. J Neurophysiol 50:313–324

    CAS  PubMed  Google Scholar 

  • Bigland-Ritchie B, Cafarelli E, Vøllestad NK (1986a) Fatigue of submaximal static contractions. Acta Physiol Scand Suppl 556:137–148

    CAS  PubMed  Google Scholar 

  • Bigland-Ritchie B, Dawson NJ, Johansson RS, Lippold OCJ (1986b) Reflex origin for the slowing of motoneurone firing rates in fatigue of human voluntary contractions. J Physiol 379:451–459

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Capaday C, Stein RB (1986) Amplitude modulation of the soleus H-reflex in the human during walking and standing. J Neurosci 6:1308–1313

    CAS  PubMed  Google Scholar 

  • Cresswell AG, Löscher WN, Thorstensson A (1995) Influence of grastrocnemius muscle length on triceps surae torque development and electromyographic activity in man. Exp Brain Res 105:283–290

    CAS  PubMed  Google Scholar 

  • Davies CT, Mecrow IK, White MJ (1982) Contractile properties of the human triceps surae with some observations on the effects of temperature and exercise. Eur J Appl Physiol Occup Physiol 49:255–269

    CAS  PubMed  Google Scholar 

  • Duchateau J, Hainaut K (1993) Behaviour of short and long latency reflexes in fatigued human muscles. J Physiol 471:787–799

    CAS  PubMed  Google Scholar 

  • Duchateau J, Balestra C, Carpentier A, Hainaut K (2002) Reflex regulation during sustained and intermittent submaximal contractions in humans. J Physiol 541:959–967

    Article  CAS  PubMed  Google Scholar 

  • Enoka RM, Hutton RS, Eldred E (1980) Changes in excitability of tendon tap and Hoffmann reflexes following voluntary contractions. EEG Clin Neurophysiol 48:664–672

    Article  CAS  Google Scholar 

  • Enoka RM, Robinson GA, Kossev AR (1989) Task and fatigue effects on low-threshold motor units in human hand muscle. J Neurophysiol 62:1344–1359

    CAS  PubMed  Google Scholar 

  • Fuglevand AJ, Keen DA (2003) Re-evaluation of muscle wisdom in the human adductor pollicis using physiological rates of stimulation. J Physiol 549:865–75. DOI 10.1113/jphysiol.2003.038836

    Article  CAS  PubMed  Google Scholar 

  • Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789

    CAS  PubMed  Google Scholar 

  • Garland SJ (1991) Role of small diameter afferents in reflex inhibition during human muscle fatigue. J Physiol 435:547–558

    CAS  PubMed  Google Scholar 

  • Garland SJ, Gossen ER (2002) The muscular wisdom hypothesis in human muscle fatigue. Exerc Sport Sci Rev 30:45–49

    Article  PubMed  Google Scholar 

  • Garland SJ, McComas AJ (1990) Reflex inhibition of human soleus muscle during fatigue. J Physiol 429:17–27

    CAS  PubMed  Google Scholar 

  • Garland SJ, Enoka RM, Serrano LP, Robinson GA (1994) Behavior of motor units in human biceps brachii during a submaximal fatiguing contraction. J Appl Physiol 76:2411–2419

    CAS  PubMed  Google Scholar 

  • Garland SJ, Griffin L, Ivanova T (1997) Motor unit discharge rate is not associated with muscle relaxation time in sustained submaximal contractions in humans. Neurosci Lett 239:25–28. DOI 10.1016/S0304-3940(97)00885-9

    CAS  PubMed  Google Scholar 

  • Griffin L, Garland SJ, Ivanova T, Gossen ER (2001) Muscle vibration sustains motor unit firing rate during submaximal isometric fatigue in humans. J Physiol 535:929–936

    CAS  PubMed  Google Scholar 

  • Hayward L, Wesselmann U, Rymer WZ (1991) Effects of muscle fatigue on mechanically sensitive afferents of slow conduction velocity in the cat triceps surae. J Neurophysiol 65:360–370

    CAS  PubMed  Google Scholar 

  • Hugon M (1973) Methodology of the Hoffmann reflex in man. In: Desmedt JE (ed) New developments in electromyography and clinical neurophysiology. Karger, Basel, pp 277–293

  • Kawakami Y, Amemiya K, Kanehisa H, Ikegawa S, Fukunaga T (2000) Fatigue responses of human triceps surae muscles during repetitive maximal isometric contractions. J Appl Physiol 88:1969–1975

    Google Scholar 

  • Kennedy PM, Cresswell AG (2001) The effect of muscle length on motor-unit recruitment during isometric plantar flexion in humans. Exp Brain Res 137:58–64. DOI 10.1007/s002210000623

    Article  CAS  PubMed  Google Scholar 

  • Kuchinad RA, Garland SJ, Ivanova TD (2001) Reflex inhibition and motor unit discharge rate in fatiguing contractions of human soleus muscle. 31st Annual Meeting, San Diego, Calif., Society for Neuroscience Abstracts 27, part 1, 444

  • Lin CS, Chan JH, Pierrot-Deseilligny E, Burke D (2002) Excitability of human muscle afferents studied using threshold tracking of the H reflex. J Physiol 545:661–669. DOI 10.1113/jphysiol.2002.026526

    Article  CAS  PubMed  Google Scholar 

  • Lindström L, Kadefors R, Petersen I (1977) An electromyographic index for localized muscle fatigue. J Appl Physiol 43:750–754

    CAS  PubMed  Google Scholar 

  • Löscher WN, Cresswell AG, Thorstensson A (1994) Electromyographic responses of the human triceps surae and force tremor during sustained submaximal isometric plantar flexion. Acta Physiol Scand 152:73–82

    PubMed  Google Scholar 

  • Löscher WN, Cresswell AG, Thorstensson A (1996) Excitatory drive to the alpha-motorneuron pool during a fatiguing submaximal contraction in man. J Physiol 491:271–280

    PubMed  Google Scholar 

  • Maffiuletti NA, Martin A, Babault N, Pensini M, Lucas B, Schieppati M (2001) Electrical and mechanical H(max)-to-M(max) ratio in power- and endurance-trained athletes. J Appl Physiol 90:3–9

    CAS  PubMed  Google Scholar 

  • Marsden CD, Meadows JC, Merton PA (1983) “Muscular wisdom” that minimizes fatigue during prolonged effort in man: peak rates of motoneuron discharge and slowing of discharge during fatigue. Adv Neurol 39:169–211

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Nielsen J, Petersen N (1994) Is presynaptic inhibition distributed to corticospinal fibres in man? J Physiol 477:47–58

    PubMed  Google Scholar 

  • Nordstrom MA, Miles TS (1991) Instability of motor unit firing rates during prolonged isometric contractions in human masseter. Brain Res 549:268–274

    Article  CAS  PubMed  Google Scholar 

  • Pierrot-Deseilligny E, Mazevet D (2000) The monosynaptic reflex: a tool to investigate motor control in humans. Interests and limits. Neurophysiol Clin 30:67–80. DOI 10.1016/S0987-7053(00)00062-9

    CAS  PubMed  Google Scholar 

  • Rankin LL, Enoka RM, Volz KA, Stuart DG (1988) Coexistence of twitch potentiation and tetanic force decline in rat hindlimb muscle. J Appl Physiol 65:2687–2695

    CAS  PubMed  Google Scholar 

  • Rudomin P, Schmidt RF (1999) Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 129:1–37. DOI 10.1007/s002210050933

    Article  CAS  PubMed  Google Scholar 

  • Schieppati M (1987) The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol 28:345–376

    CAS  PubMed  Google Scholar 

  • Sejersted OM, Vøllestad NK (1993) Physiology of muscle fatigue and associated pain. In: Vaeroy H, Merksey H (eds) Progress in fibromyalgia and myofascial pain. Elsevier Science Publications, Amsterdam, pp 41–51

  • Taylor JL, Petersen N, Butler JE, Gandevia SC (2000) Ischaemia after exercise does not reduce responses of human motoneurones to cortical or corticospinal tract stimulation. J Physiol 525:793–801

    CAS  PubMed  Google Scholar 

  • Vagg R, Mogyoros I, Kiernan MC, Burke D (1998) Activity-dependent hyperpolarization of human motor axons produced by natural activity. J Physiol 507:919–925

    CAS  PubMed  Google Scholar 

  • Walton DM, Kuchinad RA, Ivanova TD, Garland SJ (2002) Reflex inhibition during muscle fatigue in endurance-trained and sedentary individuals. Eur J Appl Physiol 87:462–468. DOI 10.1007/s00421-002-0670-9

    Article  PubMed  Google Scholar 

  • Westerblad H, Duty S, Allen DG (1993) Intracellular calcium concentration during low-frequency fatigue in isolated single fibers of mouse skeletal muscle. J Appl Physiol 75:382–388

    CAS  PubMed  Google Scholar 

  • Wiles CM, Young A, Jones DA, Edwards RH (1979) Relaxation rate of constituent muscle-fibre types in human quadriceps. Clin Sci 56:47–52

    CAS  PubMed  Google Scholar 

  • Woods J, Furbush F, Bigland-Ritchie B (1987) Evidence for a fatigue-induced reflex inhibition of motoneuron firing rates. J Neurophysiol 58:125–137

    CAS  PubMed  Google Scholar 

  • Zehr EP (2002) Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86:455–468. DOI 10.1007/s00421-002-0577-5

    Google Scholar 

Download references

Acknowledgements

This work was supported by a grant awarded to S.J. Garland from the Natural Sciences and Engineering Research Council of Canada and a PGS-A scholarship awarded to R.A. Kuchinad.

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Kuchinad, R.A., Ivanova, T.D. & Garland, S.J. Modulation of motor unit discharge rate and H-reflex amplitude during submaximal fatigue of the human soleus muscle. Exp Brain Res 158, 345–355 (2004). https://doi.org/10.1007/s00221-004-1907-0

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  • DOI: https://doi.org/10.1007/s00221-004-1907-0

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