Skip to main content
Top
Published in: European Journal of Applied Physiology 2/2014

01-02-2014 | Original Article

Effect of neuromuscular electrical stimulation intensity over the tibial nerve trunk on triceps surae muscle fatigue

Authors: Aude-Clémence M. Doix, Boris Matkowski, Alain Martin, Karin Roeleveld, Serge S. Colson

Published in: European Journal of Applied Physiology | Issue 2/2014

Login to get access

Abstract

Purpose

This study was designed to investigate whether the intensity modulation of a neuromuscular electrical stimulation (NMES) protocol delivered over the nerve trunk of the plantar flexors would lead to differential peripheral and central contributions of muscle fatigue.

Methods

Three fatiguing isometric protocols of the plantar flexors matched for the same amount of isometric torque-time integral (TTI) were randomly performed including a volitional protocol at 20 % of the maximal voluntary contraction (MVC) and two NMES protocols (one at constant intensity, CST; the other at intensity level progressively adjusted to maintain 20 % of MVC, PROG).

Results

No time x protocol interaction was found for any of the variables. The MVC decreased similarly (≈12 %, p < 0.001) after all protocols, so did the potentiated twitch responses (p = 0.001). Although voluntary activation of the plantar flexors did not change, maximal H-reflex to M-wave ratio of the soleus (SOL) and the gastrocnemius medialis (GM) muscles showed an overall increase (SOL: p = 0.037, GM: p = 0.041), while it remained stable for the gastrocnemius lateralis muscle (p = 0.221). A main time effect was observed only for the SOL maximal V-wave to the superimposed M-wave ratio (p = 0.024) and to the superimposed H-reflex (p = 0.008). While similar central and peripheral adaptations were observed after the three fatiguing protocols, the individual contribution of the three different triceps surae muscles was different.

Conclusion

Whether the current intensity was increased or not, the adaptations after a NMES protocol yield to similar muscle fatigue adaptations as voluntary contractions likely through similar pathways matching a similar TTI.
Literature
go back to reference Aagaard P, Simonsen EB, Andersen JL et al (2002) Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J Appl Physiol 92:2309–2318PubMed Aagaard P, Simonsen EB, Andersen JL et al (2002) Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J Appl Physiol 92:2309–2318PubMed
go back to reference Adams GR, Harris RT, Woodard D, Dudley GA (1993) Mapping of electrical muscle stimulation using MRI. J Appl Physiol 74:532–537PubMed Adams GR, Harris RT, Woodard D, Dudley GA (1993) Mapping of electrical muscle stimulation using MRI. J Appl Physiol 74:532–537PubMed
go back to reference Allen GM, Gandevia SC, McKenzie DK (1995) Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 18:593–600PubMedCrossRef Allen GM, Gandevia SC, McKenzie DK (1995) Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 18:593–600PubMedCrossRef
go back to reference Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88:287–332PubMedCrossRef Allen DG, Lamb GD, Westerblad H (2008) Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 88:287–332PubMedCrossRef
go back to reference Baldwin ERL, Klakowicz PM, Collins DF (2006) Wide-pulse-width, high-frequency neuromuscular stimulation: implications for functional electrical stimulation. J Appl Physiol 101:228–240PubMedCrossRef Baldwin ERL, Klakowicz PM, Collins DF (2006) Wide-pulse-width, high-frequency neuromuscular stimulation: implications for functional electrical stimulation. J Appl Physiol 101:228–240PubMedCrossRef
go back to reference Bawa P, Murnaghan C (2009) Motor unit rotation in a variety of human muscles. J Neurophysiol 102:2265–2272PubMedCrossRef Bawa P, Murnaghan C (2009) Motor unit rotation in a variety of human muscles. J Neurophysiol 102:2265–2272PubMedCrossRef
go back to reference Bawa P, Pang MY, Olesen KA, Calancie B (2006) Rotation of motoneurons during prolonged isometric contractions in humans. J Neurophysiol 96:1135–1140PubMedCrossRef Bawa P, Pang MY, Olesen KA, Calancie B (2006) Rotation of motoneurons during prolonged isometric contractions in humans. J Neurophysiol 96:1135–1140PubMedCrossRef
go back to reference Bax L, Staes F, Verhagen A (2005) Does neuromuscular electrical stimulation strengthen the quadriceps femoris? A systematic review of randomised controlled trials. Sports Med 35:191–212PubMedCrossRef Bax L, Staes F, Verhagen A (2005) Does neuromuscular electrical stimulation strengthen the quadriceps femoris? A systematic review of randomised controlled trials. Sports Med 35:191–212PubMedCrossRef
go back to reference 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 110:627–637PubMedCrossRef 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 110:627–637PubMedCrossRef
go back to reference Bergquist AJ, Clair JM, Lagerquist O et al (2011b) Neuromuscular electrical stimulation: implications of the electrically evoked sensory volley. Eur J Appl Physiol 111:2409–2426PubMedCrossRef Bergquist AJ, Clair JM, Lagerquist O et al (2011b) Neuromuscular electrical stimulation: implications of the electrically evoked sensory volley. Eur J Appl Physiol 111:2409–2426PubMedCrossRef
go back to reference Bergquist AJ, Wiest MJ, Collins DF (2012) Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared with a muscle belly: quadriceps femoris. J Appl Physiol 113:78–89PubMedCrossRef Bergquist AJ, Wiest MJ, Collins DF (2012) Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared with a muscle belly: quadriceps femoris. J Appl Physiol 113:78–89PubMedCrossRef
go back to reference Bergström M, Hultman E (1988) Energy cost and fatigue during intermittent electrical stimulation of human skeletal muscle. J Appl Physiol 65:1500–1505PubMed Bergström M, Hultman E (1988) Energy cost and fatigue during intermittent electrical stimulation of human skeletal muscle. J Appl Physiol 65:1500–1505PubMed
go back to reference Binder-Macleod SA, Scott WB (2001) Comparison of fatigue produced by various electrical stimulation trains. Acta Physiol Scand 172:195–203PubMedCrossRef Binder-Macleod SA, Scott WB (2001) Comparison of fatigue produced by various electrical stimulation trains. Acta Physiol Scand 172:195–203PubMedCrossRef
go back to reference Boerio D, Jubeau M, Zory R, Maffiuletti NA (2005) Central and peripheral fatigue after electrostimulation-induced resistance exercise. Med Sci Sports Exerc 37:973–978PubMed Boerio D, Jubeau M, Zory R, Maffiuletti NA (2005) Central and peripheral fatigue after electrostimulation-induced resistance exercise. Med Sci Sports Exerc 37:973–978PubMed
go back to reference Burridge JH, Ladouceur M (2001) Clinical and therapeutic applications of neuromuscular stimulation: a review of current use and speculation into future developments. Neuromodulation 4:147–154PubMedCrossRef Burridge JH, Ladouceur M (2001) Clinical and therapeutic applications of neuromuscular stimulation: a review of current use and speculation into future developments. Neuromodulation 4:147–154PubMedCrossRef
go back to reference Collins DF (2007) Central contributions to contractions evoked by tetanic neuromuscular electrical stimulation. Exerc Sport Sci Rev 35:102–109PubMedCrossRef Collins DF (2007) Central contributions to contractions evoked by tetanic neuromuscular electrical stimulation. Exerc Sport Sci Rev 35:102–109PubMedCrossRef
go back to reference Colson SS, Benchortane M, Tanant V et al (2010) Neuromuscular electrical stimulation training: a safe and effective treatment for facioscapulohumeral muscular dystrophy patients. Arch Phys Med Rehabil 91:697–702PubMedCrossRef Colson SS, Benchortane M, Tanant V et al (2010) Neuromuscular electrical stimulation training: a safe and effective treatment for facioscapulohumeral muscular dystrophy patients. Arch Phys Med Rehabil 91:697–702PubMedCrossRef
go back to reference Dean JC, Yates LM, Collins DF (2007) Turning on the central contribution to contractions evoked by neuromuscular electrical stimulation. J Appl Physiol 103:170–176PubMedCrossRef Dean JC, Yates LM, Collins DF (2007) Turning on the central contribution to contractions evoked by neuromuscular electrical stimulation. J Appl Physiol 103:170–176PubMedCrossRef
go back to reference Enoka RM, Duchateau J (2008) Muscle fatigue: what, why and how it influences muscle function. J Physiol (Lond) 586:11–23CrossRef Enoka RM, Duchateau J (2008) Muscle fatigue: what, why and how it influences muscle function. J Physiol (Lond) 586:11–23CrossRef
go back to reference Fuglevand AJ, Zackowski KM, Huey KA, Enoka RM (1993) Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. J Physiol (Lond) 460:549–572 Fuglevand AJ, Zackowski KM, Huey KA, Enoka RM (1993) Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. J Physiol (Lond) 460:549–572
go back to reference Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789PubMed Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789PubMed
go back to reference Gondin J, Guette M, Ballay Y, Martin A (2005) Electromyostimulation training effects on neural drive and muscle architecture. Med Sci Sports Exerc 37:1291–1299PubMedCrossRef Gondin J, Guette M, Ballay Y, Martin A (2005) Electromyostimulation training effects on neural drive and muscle architecture. Med Sci Sports Exerc 37:1291–1299PubMedCrossRef
go back to reference Gondin J, Duclay J, Martin A (2006) Soleus-and gastrocnemii-evoked V-wave responses increase after neuromuscular electrical stimulation training. J Neurophysiol 95:3328–3335PubMedCrossRef Gondin J, Duclay J, Martin A (2006) Soleus-and gastrocnemii-evoked V-wave responses increase after neuromuscular electrical stimulation training. J Neurophysiol 95:3328–3335PubMedCrossRef
go back to reference Gondin J, Giannesini B, Vilmen C et al (2010) Effects of stimulation frequency and pulse duration on fatigue and metabolic cost during a single bout of neuromuscular electrical stimulation. Muscle Nerve 41:667–678PubMed Gondin J, Giannesini B, Vilmen C et al (2010) Effects of stimulation frequency and pulse duration on fatigue and metabolic cost during a single bout of neuromuscular electrical stimulation. Muscle Nerve 41:667–678PubMed
go back to reference Gorgey AS, Black CD, Elder CP, Dudley GA (2009) Effects of electrical stimulation parameters on fatigue in skeletal muscle. J Orthop Sports Phys Ther 39:684–692PubMedCrossRef Gorgey AS, Black CD, Elder CP, Dudley GA (2009) Effects of electrical stimulation parameters on fatigue in skeletal muscle. J Orthop Sports Phys Ther 39:684–692PubMedCrossRef
go back to reference Gregory CM, Bickel CS (2005) Recruitment patterns in human skeletal muscle during electrical stimulation. Phys Ther 85:358–364PubMed Gregory CM, Bickel CS (2005) Recruitment patterns in human skeletal muscle during electrical stimulation. Phys Ther 85:358–364PubMed
go back to reference Gregory CM, Dixon W, Bickel CS (2007) Impact of varying pulse frequency and duration on muscle torque production and fatigue. Muscle Nerve 35:504–509PubMedCrossRef Gregory CM, Dixon W, Bickel CS (2007) Impact of varying pulse frequency and duration on muscle torque production and fatigue. Muscle Nerve 35:504–509PubMedCrossRef
go back to reference Grosprêtre S, Martin A (2012) H reflex and spinal excitability: methodological considerations. J Neurophysiol 107:1649–1654PubMedCrossRef Grosprêtre S, Martin A (2012) H reflex and spinal excitability: methodological considerations. J Neurophysiol 107:1649–1654PubMedCrossRef
go back to reference Hagbarth KE (1962) Post-tetanic potentiation of myotatic reflexes in man. J Neurol Neurosurg Psychiatr 25:1–10PubMedCrossRef Hagbarth KE (1962) Post-tetanic potentiation of myotatic reflexes in man. J Neurol Neurosurg Psychiatr 25:1–10PubMedCrossRef
go back to reference Hamdy S, Rothwell JC, Aziz Q et al (1998) Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nat Neurosci 1:64–68PubMedCrossRef Hamdy S, Rothwell JC, Aziz Q et al (1998) Long-term reorganization of human motor cortex driven by short-term sensory stimulation. Nat Neurosci 1:64–68PubMedCrossRef
go back to reference Henneman E, Somjen G, Carpenter DO (1965) Excitability and inhabitability of motoneurons of different sizes. J Neurophysiol 28:599–620PubMed Henneman E, Somjen G, Carpenter DO (1965) Excitability and inhabitability of motoneurons of different sizes. J Neurophysiol 28:599–620PubMed
go back to reference Herbert RD, Gandevia SC (1999) Twitch interpolation in human muscles: mechanisms and implications for measurement of voluntary activation. J Neurophysiol 82:2271–2283PubMed Herbert RD, Gandevia SC (1999) Twitch interpolation in human muscles: mechanisms and implications for measurement of voluntary activation. J Neurophysiol 82:2271–2283PubMed
go back to reference Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10:361–374PubMedCrossRef Hermens HJ, Freriks B, Disselhorst-Klug C, Rau G (2000) Development of recommendations for SEMG sensors and sensor placement procedures. J Electromyogr Kinesiol 10:361–374PubMedCrossRef
go back to reference Hirst GD, Redman SJ, Wong K (1981) Post-tetanic potentiation and facilitation of synaptic potentials evoked in cat spinal motoneurones. J Physiol (Lond) 321:97–109 Hirst GD, Redman SJ, Wong K (1981) Post-tetanic potentiation and facilitation of synaptic potentials evoked in cat spinal motoneurones. J Physiol (Lond) 321:97–109
go back to reference Hultman E, Sjöholm H, Jäderholm-Ek I, Krynicki J (1983) Evaluation of methods for electrical stimulation of human skeletal muscle in situ. Pflugers Arch 398:139–141PubMedCrossRef Hultman E, Sjöholm H, Jäderholm-Ek I, Krynicki J (1983) Evaluation of methods for electrical stimulation of human skeletal muscle in situ. Pflugers Arch 398:139–141PubMedCrossRef
go back to reference Kebaetse MB, Binder-Macleod SA (2004) Strategies that improve human skeletal muscle performance during repetitive, non-isometric contractions. Pflugers Arch 448:525–532PubMedCrossRef Kebaetse MB, Binder-Macleod SA (2004) Strategies that improve human skeletal muscle performance during repetitive, non-isometric contractions. Pflugers Arch 448:525–532PubMedCrossRef
go back to reference Kesar T, Chou L-W, Binder-Macleod SA (2008) Effects of stimulation frequency versus pulse duration modulation on muscle fatigue. J Electromyogr Kinesiol 18:662–671PubMedCentralPubMedCrossRef Kesar T, Chou L-W, Binder-Macleod SA (2008) Effects of stimulation frequency versus pulse duration modulation on muscle fatigue. J Electromyogr Kinesiol 18:662–671PubMedCentralPubMedCrossRef
go back to reference Kiernan MC, Lin CS-Y, Burke D (2004) Differences in activity-dependent hyperpolarization in human sensory and motor axons. J Physiol (Lond) 558:341–349CrossRef Kiernan MC, Lin CS-Y, Burke D (2004) Differences in activity-dependent hyperpolarization in human sensory and motor axons. J Physiol (Lond) 558:341–349CrossRef
go back to reference Kitago T, Mazzocchio R, Liuzzi G, Cohen LG (2004) Modulation of H-reflex excitability by tetanic stimulation. Clin Neurophysiol 115:858–861PubMedCrossRef Kitago T, Mazzocchio R, Liuzzi G, Cohen LG (2004) Modulation of H-reflex excitability by tetanic stimulation. Clin Neurophysiol 115:858–861PubMedCrossRef
go back to reference Klakowicz PM, Baldwin ERL, Collins DF (2006) Contribution of M-waves and H-reflexes to contractions evoked by tetanic nerve stimulation in humans. J Neurophysiol 96:1293–1302PubMedCrossRef Klakowicz PM, Baldwin ERL, Collins DF (2006) Contribution of M-waves and H-reflexes to contractions evoked by tetanic nerve stimulation in humans. J Neurophysiol 96:1293–1302PubMedCrossRef
go back to reference Kufel TJ, Pineda LA, Mador MJ (2002) Comparison of potentiated and unpotentiated twitches as an index of muscle fatigue. Muscle Nerve 25:438–444PubMedCrossRef Kufel TJ, Pineda LA, Mador MJ (2002) Comparison of potentiated and unpotentiated twitches as an index of muscle fatigue. Muscle Nerve 25:438–444PubMedCrossRef
go back to reference Lagerquist O, Collins DF (2010) Influence of stimulus pulse width on M-waves, H-reflexes, and torque during tetanic low-intensity neuromuscular stimulation. Muscle Nerve 42:886–893PubMedCrossRef Lagerquist O, Collins DF (2010) Influence of stimulus pulse width on M-waves, H-reflexes, and torque during tetanic low-intensity neuromuscular stimulation. Muscle Nerve 42:886–893PubMedCrossRef
go back to reference Lévénez M, Kotzamanidis C, Carpentier A, Duchateau J (2005) Spinal reflexes and co-activation of ankle muscles during a submaximal fatiguing contraction. J Appl Physiol 99:1182–1188PubMedCrossRef Lévénez M, Kotzamanidis C, Carpentier A, Duchateau J (2005) Spinal reflexes and co-activation of ankle muscles during a submaximal fatiguing contraction. J Appl Physiol 99:1182–1188PubMedCrossRef
go back to reference Maffiuletti NA (2010) Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 110:223–234PubMedCrossRef Maffiuletti NA (2010) Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 110:223–234PubMedCrossRef
go back to reference Matsunaga T, Shimada Y, Sato K (1999) Muscle fatigue from intermittent stimulation with low and high frequency electrical pulses. Arch Phys Med Rehabil 80:48–53PubMedCrossRef Matsunaga T, Shimada Y, Sato K (1999) Muscle fatigue from intermittent stimulation with low and high frequency electrical pulses. Arch Phys Med Rehabil 80:48–53PubMedCrossRef
go back to reference Miles GB, Dai Y, Brownstone RM (2005) Mechanisms underlying the early phase of spike frequency adaptation in mouse spinal motoneurones. J Physiol (Lond) 566:519–532CrossRef Miles GB, Dai Y, Brownstone RM (2005) Mechanisms underlying the early phase of spike frequency adaptation in mouse spinal motoneurones. J Physiol (Lond) 566:519–532CrossRef
go back to reference Millet GY, Martin V, Martin A, Vergès S (2011) Electrical stimulation for testing neuromuscular function: from sport to pathology. Eur J Appl Physiol 111:2489–2500PubMedCrossRef Millet GY, Martin V, Martin A, Vergès S (2011) Electrical stimulation for testing neuromuscular function: from sport to pathology. Eur J Appl Physiol 111:2489–2500PubMedCrossRef
go back to reference Muthalib M, Jubeau M, Millet GY et al (2010) Biceps brachii muscle oxygenation in electrical muscle stimulation. Clin Physiol Funct Imaging 30:360–368PubMed Muthalib M, Jubeau M, Millet GY et al (2010) Biceps brachii muscle oxygenation in electrical muscle stimulation. Clin Physiol Funct Imaging 30:360–368PubMed
go back to reference Papaiordanidou M, Guiraud D, Varray A (2010) Kinetics of neuromuscular changes during low-frequency electrical stimulation. Muscle Nerve 41:54–62PubMedCrossRef Papaiordanidou M, Guiraud D, Varray A (2010) Kinetics of neuromuscular changes during low-frequency electrical stimulation. Muscle Nerve 41:54–62PubMedCrossRef
go back to reference Perez MA, Field-Fote EC, Floeter MK (2003) Patterned sensory stimulation induces plasticity in reciprocal Ia inhibition in humans. J Neurosci 23:2014–2018PubMed Perez MA, Field-Fote EC, Floeter MK (2003) Patterned sensory stimulation induces plasticity in reciprocal Ia inhibition in humans. J Neurosci 23:2014–2018PubMed
go back to reference Pierrot-Deseilligny E, Mazevet D (2000) The monosynaptic reflex: a tool to investigate motor control in humans. Interest and limits. Neurophysiol Clin 30:67–80PubMedCrossRef Pierrot-Deseilligny E, Mazevet D (2000) The monosynaptic reflex: a tool to investigate motor control in humans. Interest and limits. Neurophysiol Clin 30:67–80PubMedCrossRef
go back to reference Russ DW, Elliott MA, Vandenborne K et al (2002a) Metabolic costs of isometric force generation and maintenance of human skeletal muscle. Am J Physiol Endocrinol Metab 282:E448–E457PubMed Russ DW, Elliott MA, Vandenborne K et al (2002a) Metabolic costs of isometric force generation and maintenance of human skeletal muscle. Am J Physiol Endocrinol Metab 282:E448–E457PubMed
go back to reference Russ DW, Vandenborne K, Binder-Macleod SA (2002b) Factors in fatigue during intermittent electrical stimulation of human skeletal muscle. J Appl Physiol 93:469–478PubMed Russ DW, Vandenborne K, Binder-Macleod SA (2002b) Factors in fatigue during intermittent electrical stimulation of human skeletal muscle. J Appl Physiol 93:469–478PubMed
go back to reference Scaglioni G, Martin A (2009) Assessment of plantar flexors activation capacity: nerve versus muscle stimulation by single versus double pulse. Eur J Appl Physiol 106:563–572PubMedCrossRef Scaglioni G, Martin A (2009) Assessment of plantar flexors activation capacity: nerve versus muscle stimulation by single versus double pulse. Eur J Appl Physiol 106:563–572PubMedCrossRef
go back to reference Schieppati M (1987) The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol 28:345–376PubMedCrossRef Schieppati M (1987) The Hoffmann reflex: a means of assessing spinal reflex excitability and its descending control in man. Prog Neurobiol 28:345–376PubMedCrossRef
go back to reference Shield A, Zhou S (2004) Assessing voluntary muscle activation with the twitch interpolation technique. Sports Med 34:253–267PubMedCrossRef Shield A, Zhou S (2004) Assessing voluntary muscle activation with the twitch interpolation technique. Sports Med 34:253–267PubMedCrossRef
go back to reference Strojnik V, Komi PV (1998) Neuromuscular fatigue after maximal stretch-shortening cycle exercise. J Appl Physiol 84:344–350PubMed Strojnik V, Komi PV (1998) Neuromuscular fatigue after maximal stretch-shortening cycle exercise. J Appl Physiol 84:344–350PubMed
go back to reference Taylor JL (2009) Point:Counterpoint: the interpolated twitch does/does not provide a valid measure of the voluntary activation of muscle. J Appl Physiol 107:354–355PubMedCrossRef Taylor JL (2009) Point:Counterpoint: the interpolated twitch does/does not provide a valid measure of the voluntary activation of muscle. J Appl Physiol 107:354–355PubMedCrossRef
go back to reference 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 157:341–347PubMedCrossRef 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 157:341–347PubMedCrossRef
go back to reference Tucker KJ, Tuncer M, Türker KS (2005) A review of the H-reflex and M-wave in the human triceps surae. Hum Mov Sci 24:667–688PubMedCrossRef Tucker KJ, Tuncer M, Türker KS (2005) A review of the H-reflex and M-wave in the human triceps surae. Hum Mov Sci 24:667–688PubMedCrossRef
go back to reference Upton AR, McComas AJ, Sica RE (1971) Potentiation of “late” responses evoked in muscles during effort. J Neurol Neurosurg Psychiatr 34:699–711PubMedCrossRef Upton AR, McComas AJ, Sica RE (1971) Potentiation of “late” responses evoked in muscles during effort. J Neurol Neurosurg Psychiatr 34:699–711PubMedCrossRef
go back to reference Vanderthommen M, Depresseux JC, Dauchat L et al (2000) Spatial distribution of blood flow in electrically stimulated human muscle: a positron emission tomography study. Muscle Nerve 23:482–489PubMedCrossRef Vanderthommen M, Depresseux JC, Dauchat L et al (2000) Spatial distribution of blood flow in electrically stimulated human muscle: a positron emission tomography study. Muscle Nerve 23:482–489PubMedCrossRef
go back to reference 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 94:1012–1024PubMed 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 94:1012–1024PubMed
go back to reference Vilin YY, Ruben PC (2001) Slow inactivation in voltage-gated sodium channels: molecular substrates and contributions to channelopathies. Cell Biochem Biophys 35:171–190PubMedCrossRef Vilin YY, Ruben PC (2001) Slow inactivation in voltage-gated sodium channels: molecular substrates and contributions to channelopathies. Cell Biochem Biophys 35:171–190PubMedCrossRef
go back to reference Westerblad H, Allen DG, Lännergren J (2002) Muscle fatigue: lactic acid or inorganic phosphate the major cause? News Physiol Sci 17:17–21PubMed Westerblad H, Allen DG, Lännergren J (2002) Muscle fatigue: lactic acid or inorganic phosphate the major cause? News Physiol Sci 17:17–21PubMed
go back to reference Zehr EP (2002) Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86:455–468PubMedCrossRef Zehr EP (2002) Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86:455–468PubMedCrossRef
Metadata
Title
Effect of neuromuscular electrical stimulation intensity over the tibial nerve trunk on triceps surae muscle fatigue
Authors
Aude-Clémence M. Doix
Boris Matkowski
Alain Martin
Karin Roeleveld
Serge S. Colson
Publication date
01-02-2014
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Applied Physiology / Issue 2/2014
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-013-2780-y

Other articles of this Issue 2/2014

European Journal of Applied Physiology 2/2014 Go to the issue