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Impact of stimulation frequency on neuromuscular fatigue

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European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

Purpose

The aim of the present study was to examine the frequency effects (20 Hz and 100 Hz) on neuromuscular fatigue using stimulation parameters favoring an indirect motor unit recruitment through the afferent pathway.

Methods

Nineteen subjects were divided into two groups: 20 Hz (n = 10) and 100 Hz (n = 9). The electrical stimulation session consisted of 25 stimulation trains (20 s ON/20 s OFF, pulse width: 1 ms) applied over the tibial nerve and delivered at an intensity evoking 10% maximal voluntary isometric contraction (MVIC). Before and after these protocols, MVIC was assessed, while neural changes were evaluated by the level of activation (VAL) and muscle changes were evaluated by the twitch associated with the maximal M-wave (Pt). For all stimulation trains, the real and the theoretical values of the torque-time integral (TTIr and TTIth, respectively) were calculated. The TTIr/TTIth ratio of the first train was calculated to evaluate the presence of extra torque.

Results

The main results showed a similar decrease in MVIC torque after both protocols accompanied by neural and muscle changes, as evidenced by the decrease in VAL and Pt. TTIr values across the 20-Hz trains remained constant, whereas they significantly decreased during the 100-Hz stimulation trains. The relative MVIC decrease was negatively correlated with TTIr/TTIth.

Conclusion

Results give evidence of an identical neuromuscular fatigue development between protocols, while lower stimulation frequency permitted preservation of a given torque level during the stimulation trains. The negative correlation between this fatigue development and TTIr/TTIth suggests that extra torque production induces greater voluntary torque losses.

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Abbreviations

ANOVA:

Analysis of variance

EMG:

Electromyographic activity

ET:

Extra torque

M MAX :

Maximal M-wave

MU:

Motor unit

MVIC:

Maximal voluntary isometric contraction

NMES:

Neuromuscular electrical stimulation

Pt:

Peak torque amplitude of the potentiated twitch associated to MMAX

SOL:

Soleus

TTI:

Torque-time integral

TTIr:

Real torque-time integral

TTIth:

Theoretical torque-time integral

VAL:

Voluntary activation level

WPHF:

Wide-pulse high frequency

References

  • Allen DG, Westerblad H (2001) Role of phosphate and calcium stores in muscle fatigue. J Physiol 536:657–665

    Article  CAS  Google Scholar 

  • Bergquist AJ, Clair JM, Collins DF (2011a) Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared with a muscle belly: triceps surae. J Appl Physiol 110:627–637

    Article  CAS  Google Scholar 

  • Bergquist AJ, Clair JM, Lagerquist O et al (2011b) Neuromuscular electrical stimulation: implications of the electrically evoked sensory volley. Eur J Appl Physiol 111:2409–2426

    Article  CAS  Google Scholar 

  • Binder-Macleod SA, Scott WB (2001) Comparison of fatigue produced by various electrical stimulation trains. Acta Physiol Scand 172:195–203

    Article  CAS  Google Scholar 

  • Boerio D, Jubeau M, Zory R, Maffiuletti NA (2005) Central and peripheral fatigue after electrostimulation-induced resistance exercise. Med Sci Sports Exerc 37:973–978

    PubMed  Google Scholar 

  • Bostock H, Bergmans J (1994) Post-tetanic excitability changes and ectopic discharges in a human motor axon. Brain 117:913–928

    Article  Google Scholar 

  • Collins DF (2007) Central contributions to contractions evoked by tetanic neuromuscular electrical stimulation. Exerc Sport Sci Rev 35:102–109

    Article  Google Scholar 

  • Collins DF, Burke D, Gandevia SC (2001) Large involuntary forces consistent with plateau-like behavior of human motoneurons. J Neurosci 21:4059–4065

    Article  CAS  Google Scholar 

  • Collins DF, Burke D, Gandevia SC (2002) Sustained contractions produced by plateau-like behaviour in human motoneurones. J Physiol 538:289–301

    Article  CAS  Google Scholar 

  • Dean J, Yates L, Collins DF (2007) Turning on the central contributions to contractions evoked by neuromuscular electrical stimulation. J Appl Physiol 9:102–109

    Google Scholar 

  • Dean JC, Clair-Auger JM, Lagerquist O, Collins DF (2014) Asynchronous recruitment of low-threshold motor units during repetitive, low-current stimulation of the human tibial nerve. Front Hum Neurosci 8:1–12

    Article  Google Scholar 

  • Fitts RH (2008) The cross-bridge cycle and skeletal muscle fatigue. J Appl Physiol 104:551–558

    Article  CAS  Google Scholar 

  • Gorgey AS, Black CD, Elder CP, Dudley GA (2009) Effects of electrical stimulation parameters on fatigue in skeletal muscle. J Orthop Sport Phys Ther 39:684–692

    Article  Google Scholar 

  • Gregory CM, Bickel CS (2005) Recruitment patterns in human skeletal muscle during electrical stimulation. Phys Ther 85:358–364

    PubMed  Google Scholar 

  • Henneman E, Somjen G, Carpenter DO (1965) Functional significance of cell size in spinal motoneurons. J Neurophysiol 28:560–580

    Article  CAS  Google Scholar 

  • Hortobágyi T, Maffiuletti NA (2011) Neural adaptations to electrical stimulation strength training. Eur J Appl Physiol 111:2439–2449

    Article  Google Scholar 

  • Jubeau M, Gondin J, Martin A et al (2007) Random motor unit activation by electrostimulation. Int J Sports Med 28:901–904

    Article  CAS  Google Scholar 

  • Kent-Braun JA (1999) Central and peripheral contributions to muscle fatigue in humans during sustained maximal effort. Eur J Appl Physiol Occup Physiol 80:57–63

    Article  CAS  Google Scholar 

  • Kesar T, Binder-Macleod S (2006) Effect of frequency and pulse duration on human muscle fatigue during repetitive electrical stimulation. Exp Physiol 91:967–976

    Article  Google Scholar 

  • Kesar T, Chou LW, Binder-Macleod SA (2008) Effects of stimulation frequency versus pulse duration modulation on muscle fatigue. J Electromyogr Kinesiol 18:662–671

    Article  Google Scholar 

  • Kiernan M, Mogyoros I, Burke D (1996) Differences in the recovery of excitability in sensory and motor axons of human median nerve. Brain 119:1099–1105

    Article  Google Scholar 

  • Kiernan MC, Lin CS-Y, Burke D (2004) Differences in activity-dependent hyperpolarization in human sensory and motor axons. J Physiol 558:341–349

    Article  CAS  Google Scholar 

  • Lagerquist O, Walsh LD, Blouin J-S et al (2009) Effect of a peripheral nerve block on torque produced by repetitive electrical stimulation. J Appl Physiol 107:161–167

    Article  Google Scholar 

  • Lattier G, Millet G, Martin A, Martin V (2004) Fatigue and recovery after high-intensity exercise. Part I: neuromuscular fatigue. Int J Sport Med 25:450–456

    Google Scholar 

  • Maffiuletti NA (2010) Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 110:223–234

    Article  Google Scholar 

  • Maffiuletti NA, Pensini M, Martin A (2002) Activation of human plantar flexor muscles increases after electromyostimulation training. J Appl Physiol 92:1383–1392

    Article  Google Scholar 

  • Matkowski B, Lepers R, Martin A (2015) Torque decrease during submaximal evoked contractions of the quadriceps muscle is linked not only to muscle fatigue. J Appl Physiol 118:1136–1144

    Article  Google Scholar 

  • Neyroud D, Dodd D, Gondin J et al (2014) Wide-pulse-high-frequency neuromuscular stimulation of triceps surae induces greater muscle fatigue compared with conventional stimulation. J Appl Physiol 116:1281–1289

    Article  Google Scholar 

  • Papaiordanidou M, Guiraud D, Varray A (2010) Does central fatigue exist under low-frequency stimulation of a low fatigue-resistant muscle? Eur J Appl Physiol 110:815–825

    Article  Google Scholar 

  • Papaiordanidou M, Stevenot JD, Mustacchi V et al (2014) Electrically induced torque decrease reflects more than muscle fatigue. Muscle Nerve 50:604–607

    Article  Google Scholar 

  • Scott WB, Lee SCK, Johnston TE et al (2007) Effect of electrical stimulation pattern on the force responses of paralyzed human quadriceps muscles. Muscle Nerve 35:471–478

    Article  Google Scholar 

  • Strojnik V, Komi PV (1998) Neuromuscular fatigue after maximal stretch-shortening cycle exercise. J Appl Physiol 84:344–350

    Article  CAS  Google Scholar 

  • Theurel J, Lepers R, Pardon L, Maffiuletti NA (2007) Differences in cardiorespiratory and neuromuscular responses between voluntary and stimulated contractions of the quadriceps femoris muscle. Respir Physiol Neurobiol 157:341–347

    Article  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

    Article  CAS  Google Scholar 

  • Vanderthommen M, Duteil S, Wary C et al (2003) A comparison of voluntary and electrically induced contractions by interleaved 1H- and 31P-NMRS in humans. J Appl Physiol 94:1012–1024

    Article  CAS  Google Scholar 

  • Veale JL, Mark RF, Rees S (1973) Differential sensitivity of motor and sensory fibres in human ulnar nerve. J Neurol Neurosurg Psychiatry 36:75–86

    Article  CAS  Google Scholar 

  • Vitry F, Martin A, Deley G, Papaiordanidou M (2019) Effect of reflexive activation of motor units on torque development during electrically-evoked contractions of the triceps surae muscle. J Appl Physiol 126:386–392

    Article  CAS  Google Scholar 

  • Zory R, Boërio D, Jubeau M, Maffiuletti NA (2005) Central and peripheral fatigue of the knee extensor muscles induced by electromyostimulation. Int J Sports Med 26:847–853

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. INSERM UMR1093-CAPS, Université Bourgogne Franche-Comté, UFR des Sciences du Sport, 21000, Dijon, France

    Florian Vitry, Alain Martin & Maria Papaiordanidou

Authors
  1. Florian Vitry
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  2. Alain Martin
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  3. Maria Papaiordanidou
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Contributions

FV, AM and MP conceived and designed research; FV conducted experiments; FV analyzed data; FV, AM and MP interpreted results of experiments; FV prepared figures; FV and MP drafted manuscript; FV, AM and MP edited and revised manuscript; FV, AM and MP approved final version of manuscript.

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Correspondence to Florian Vitry.

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The authors declare that they have no conflict of interest.

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Communicated by Toshio Moritani.

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Vitry, F., Martin, A. & Papaiordanidou, M. Impact of stimulation frequency on neuromuscular fatigue. Eur J Appl Physiol 119, 2609–2616 (2019). https://doi.org/10.1007/s00421-019-04239-x

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