Skip to main content
Top
Published in: European Journal of Applied Physiology 10/2011

Open Access 01-10-2011 | Mini Review

Neural adaptations to electrical stimulation strength training

Authors: Tibor Hortobágyi, Nicola A. Maffiuletti

Published in: European Journal of Applied Physiology | Issue 10/2011

Login to get access

Abstract

This review provides evidence for the hypothesis that electrostimulation strength training (EST) increases the force of a maximal voluntary contraction (MVC) through neural adaptations in healthy skeletal muscle. Although electrical stimulation and voluntary effort activate muscle differently, there is substantial evidence to suggest that EST modifies the excitability of specific neural paths and such adaptations contribute to the increases in MVC force. Similar to strength training with voluntary contractions, EST increases MVC force after only a few sessions with some changes in muscle biochemistry but without overt muscle hypertrophy. There is some mixed evidence for spinal neural adaptations in the form of an increase in the amplitude of the interpolated twitch and in the amplitude of the volitional wave, with less evidence for changes in spinal excitability. Cross-sectional and exercise studies also suggest that the barrage of sensory and nociceptive inputs acts at the cortical level and can modify the motor cortical output and interhemispheric paths. The data suggest that neural adaptations mediate initial increases in MVC force after short-term EST.
Literature
go back to reference Aagaard P, Simonsen EB, Andersen JL, Magnusson P, Dyhre-Poulsen P (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, Magnusson P, Dyhre-Poulsen P (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 Arya T, Bajwa S, Edgley SA (1991) Crossed reflex actions from group II muscle afferents in the lumbar spinal cord of the anaesthetized cat. J Physiol 444:117–131PubMed Arya T, Bajwa S, Edgley SA (1991) Crossed reflex actions from group II muscle afferents in the lumbar spinal cord of the anaesthetized cat. J Physiol 444:117–131PubMed
go back to reference Baldwin ER, Klakowicz PM, Collins DF (2006) Wide-pulse-width, high-frequency neuromuscular stimulation: implications for functional electrical stimulation. J Appl Physiol 101:228–240PubMed Baldwin ER, Klakowicz PM, Collins DF (2006) Wide-pulse-width, high-frequency neuromuscular stimulation: implications for functional electrical stimulation. J Appl Physiol 101:228–240PubMed
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 35:191–212PubMed Bax L, Staes F, Verhagen A (2005) Does neuromuscular electrical stimulation strengthen the quadriceps femoris? A systematic review of randomised controlled trials. Sports Med 35:191–212PubMed
go back to reference Bergquist AJ, Clair JM, Lagerquist O, Mang CS, Okuma Y, Collins DF (2011) Neuromuscular electrical stimulation: implications of the electrically-evoked sensory volley. Eur J Appl Physiol (in press) Bergquist AJ, Clair JM, Lagerquist O, Mang CS, Okuma Y, Collins DF (2011) Neuromuscular electrical stimulation: implications of the electrically-evoked sensory volley. Eur J Appl Physiol (in press)
go back to reference Bezerra P, Zhou S, Crowley Z, Brooks L, Hooper A (2009) Effects of unilateral electromyostimulation superimposed on voluntary training on strength and cross-sectional area. Muscle Nerve 40:430–437PubMed Bezerra P, Zhou S, Crowley Z, Brooks L, Hooper A (2009) Effects of unilateral electromyostimulation superimposed on voluntary training on strength and cross-sectional area. Muscle Nerve 40:430–437PubMed
go back to reference Blickenstorfer A, Kleiser R, Keller T, Keisker B, Meyer M, Riener R, Kollias S (2009) Cortical and subcortical correlates of functional electrical stimulation of wrist extensor and flexor muscles revealed by fMRI. Hum Brain Mapp 30:963–975PubMed Blickenstorfer A, Kleiser R, Keller T, Keisker B, Meyer M, Riener R, Kollias S (2009) Cortical and subcortical correlates of functional electrical stimulation of wrist extensor and flexor muscles revealed by fMRI. Hum Brain Mapp 30:963–975PubMed
go back to reference Brocherie F, Babault N, Cometti G, Maffiuletti N, Chatard JC (2005) Electrostimulation training effects on the physical performance of ice hockey players. Med Sci Sports Exerc 37:455–460PubMed Brocherie F, Babault N, Cometti G, Maffiuletti N, Chatard JC (2005) Electrostimulation training effects on the physical performance of ice hockey players. Med Sci Sports Exerc 37:455–460PubMed
go back to reference Cabric M, Appell HJ (1987) Effect of electrical stimulation of high and low frequency on maximum isometric force and some morphological characteristics in men. Int J Sports Med 8:256–260PubMed Cabric M, Appell HJ (1987) Effect of electrical stimulation of high and low frequency on maximum isometric force and some morphological characteristics in men. Int J Sports Med 8:256–260PubMed
go back to reference Cabric M, Appell HJ, Resic A (1987) Effects of electrical stimulation of different frequencies on the myonuclei and fiber size in human muscle. Int J Sports Med 8:323–326PubMed Cabric M, Appell HJ, Resic A (1987) Effects of electrical stimulation of different frequencies on the myonuclei and fiber size in human muscle. Int J Sports Med 8:323–326PubMed
go back to reference Carroll TJ, Riek S, Carson RG (2001) Neural adaptations to resistance training: implications for movement control. Sports Med 31:829–840PubMed Carroll TJ, Riek S, Carson RG (2001) Neural adaptations to resistance training: implications for movement control. Sports Med 31:829–840PubMed
go back to reference Carroll TJ, Riek S, Carson RG (2002) The sites of neural adaptation induced by resistance training in humans. J Physiol 544:641–652PubMed Carroll TJ, Riek S, Carson RG (2002) The sites of neural adaptation induced by resistance training in humans. J Physiol 544:641–652PubMed
go back to reference Carroll TJ, Selvanayagam VS, Riek S, Semmler JG (2011) Neural adaptations to strength training: moving beyond TMS and reflex studies. Acta Physiol (Oxf) 202(2):119–140 Carroll TJ, Selvanayagam VS, Riek S, Semmler JG (2011) Neural adaptations to strength training: moving beyond TMS and reflex studies. Acta Physiol (Oxf) 202(2):119–140
go back to reference Cavallari P, Fournier E, Katz R, Malmgren K, Pierrot-Deseilligny E, Shindo M (1985) Cutaneous facilitation of transmission in Ib reflex pathways in the human upper limb. Exp Brain Res 60:197–199PubMed Cavallari P, Fournier E, Katz R, Malmgren K, Pierrot-Deseilligny E, Shindo M (1985) Cutaneous facilitation of transmission in Ib reflex pathways in the human upper limb. Exp Brain Res 60:197–199PubMed
go back to reference Chen XY, Chen Y, Wang Y, Thompson A, Carp JS, Segal RL, Wolpaw JR (2010) Reflex conditioning: a new strategy for improving motor function after spinal cord injury. Ann NY Acad Sci 1198 Suppl 1: E12–21 Chen XY, Chen Y, Wang Y, Thompson A, Carp JS, Segal RL, Wolpaw JR (2010) Reflex conditioning: a new strategy for improving motor function after spinal cord injury. Ann NY Acad Sci 1198 Suppl 1: E12–21
go back to reference Christie A, Kamen G (2010) Short-term training adaptations in maximal motor unit firing rates and afterhyperpolarization duration. Muscle Nerve 41:651–660PubMed Christie A, Kamen G (2010) Short-term training adaptations in maximal motor unit firing rates and afterhyperpolarization duration. Muscle Nerve 41:651–660PubMed
go back to reference Collins DF (2007) Central contributions to contractions evoked by tetanic neuromuscular electrical stimulation. Exerc Sport Sci Rev 35:102–109PubMed Collins DF (2007) Central contributions to contractions evoked by tetanic neuromuscular electrical stimulation. Exerc Sport Sci Rev 35:102–109PubMed
go back to reference Collins DF, Burke D, Gandevia SC (2002) Sustained contractions produced by plateau-like behaviour in human motoneurones. J Physiol 538:289–301PubMed Collins DF, Burke D, Gandevia SC (2002) Sustained contractions produced by plateau-like behaviour in human motoneurones. J Physiol 538:289–301PubMed
go back to reference Colson SS, Martin A, Van Hoecke J (2009) Effects of electromyostimulation versus voluntary isometric training on elbow flexor muscle strength. J Electromyogr Kinesiol 19:311–319 Colson SS, Martin A, Van Hoecke J (2009) Effects of electromyostimulation versus voluntary isometric training on elbow flexor muscle strength. J Electromyogr Kinesiol 19:311–319
go back to reference Costa A, Dalloul H, Hegyesi H, Apor P, Csende Z, Racz L, Vaczi M, Tihanyi J (2007) Impact of repeated bouts of eccentric exercise on myogenic gene expression. Eur J Appl Physiol 101:427–436PubMed Costa A, Dalloul H, Hegyesi H, Apor P, Csende Z, Racz L, Vaczi M, Tihanyi J (2007) Impact of repeated bouts of eccentric exercise on myogenic gene expression. Eur J Appl Physiol 101:427–436PubMed
go back to reference de Haan A, Gerrits KHL, de Ruiter CJ (2009) Counterpoint: the interpolated twitch does not provide a valid measure of the voluntary activation of muscle. J Appl Physiol 107:355–357PubMed de Haan A, Gerrits KHL, de Ruiter CJ (2009) Counterpoint: the interpolated twitch does not provide a valid measure of the voluntary activation of muscle. J Appl Physiol 107:355–357PubMed
go back to reference Del Balso C, Cafarelli E (2007) Adaptations in the activation of human skeletal muscle induced by short-term isometric resistance training. J Appl Physiol 103:402–411PubMed Del Balso C, Cafarelli E (2007) Adaptations in the activation of human skeletal muscle induced by short-term isometric resistance training. J Appl Physiol 103:402–411PubMed
go back to reference Dragert K, Zehr EP (2011) Bilateral neuromuscular plasticity from unilateral training of the ankle dorsiflexors. Exp Brain Res 208:217–227PubMed Dragert K, Zehr EP (2011) Bilateral neuromuscular plasticity from unilateral training of the ankle dorsiflexors. Exp Brain Res 208:217–227PubMed
go back to reference Duchateau J, Hainaut K (1988) Training effects of sub-maximal electrostimulation in a human muscle. Med Sci Sports Exerc 20:99–104PubMed Duchateau J, Hainaut K (1988) Training effects of sub-maximal electrostimulation in a human muscle. Med Sci Sports Exerc 20:99–104PubMed
go back to reference Duclay J, Martin A, Robbe A, Pousson M (2008) Spinal reflex plasticity during maximal dynamic contractions after eccentric training. Med Sci Sports Exerc 40:722–734PubMed Duclay J, Martin A, Robbe A, Pousson M (2008) Spinal reflex plasticity during maximal dynamic contractions after eccentric training. Med Sci Sports Exerc 40:722–734PubMed
go back to reference Enoka RM (1988) Muscle strength and its development. New perspectives. Sports Med 6:146–168PubMed Enoka RM (1988) Muscle strength and its development. New perspectives. Sports Med 6:146–168PubMed
go back to reference Enoka RM (2006) Neuromuscular electrical stimulation: what is activated? In: Rainoldi A, Minetto MA, Merletti R (eds) Biomedical engineering in exercise and sports. Edizioni Minerva Medica, Torino, pp 181–186 Enoka RM (2006) Neuromuscular electrical stimulation: what is activated? In: Rainoldi A, Minetto MA, Merletti R (eds) Biomedical engineering in exercise and sports. Edizioni Minerva Medica, Torino, pp 181–186
go back to reference Eriksson E, Haggmark T, Kiessling KH, Karlsson J (1981) Effect of electrical stimulation on human skeletal muscle. Int J Sports Med 2:18–22PubMed Eriksson E, Haggmark T, Kiessling KH, Karlsson J (1981) Effect of electrical stimulation on human skeletal muscle. Int J Sports Med 2:18–22PubMed
go back to reference Everaert DG, Thompson AK, Chong SL, Stein RB (2010) Does functional electrical stimulation for foot drop strengthen corticospinal connections? Neurorehabil Neural Repair 24:168–177PubMed Everaert DG, Thompson AK, Chong SL, Stein RB (2010) Does functional electrical stimulation for foot drop strengthen corticospinal connections? Neurorehabil Neural Repair 24:168–177PubMed
go back to reference Farina D, Holobar A, Merletti R, Enoka RM (2010) Decoding the neural drive to muscles from the surface electromyogram. Clin Neurophysiol 121:1616–1623PubMed Farina D, Holobar A, Merletti R, Enoka RM (2010) Decoding the neural drive to muscles from the surface electromyogram. Clin Neurophysiol 121:1616–1623PubMed
go back to reference Farthing JP (2009) Cross-education of strength depends on limb dominance: implications for theory and application. Exerc Sport Sci Rev 37:179–187PubMed Farthing JP (2009) Cross-education of strength depends on limb dominance: implications for theory and application. Exerc Sport Sci Rev 37:179–187PubMed
go back to reference Farthing JP, Krentz JR, Magnus CRA, Barss TS, Lanovaz JL, Cummine J, Esopenko C, Sarty GE, Borowsky R (2011) Changes in fMRI cortical activation with cross-education to an immobilized limb. Med Sci Sports Exerc (in press) Farthing JP, Krentz JR, Magnus CRA, Barss TS, Lanovaz JL, Cummine J, Esopenko C, Sarty GE, Borowsky R (2011) Changes in fMRI cortical activation with cross-education to an immobilized limb. Med Sci Sports Exerc (in press)
go back to reference Fimland MS, Helgerud J, Solstad GM, Iversen VM, Leivseth G, Hoff J (2009) Neural adaptations underlying cross-education after unilateral strength training. Eur J Appl Physiol 107:723–730PubMed Fimland MS, Helgerud J, Solstad GM, Iversen VM, Leivseth G, Hoff J (2009) Neural adaptations underlying cross-education after unilateral strength training. Eur J Appl Physiol 107:723–730PubMed
go back to reference Fitzgerald GK, Delitto A (2006) Neuromuscular electrical stimualtion for muscle strength training. In: Rainoldi A, Minetto MA, Merletti R (eds) Biomedical engineering in exercise and sports. Edizioni Minerva Medica, Torino, pp 199–207 Fitzgerald GK, Delitto A (2006) Neuromuscular electrical stimualtion for muscle strength training. In: Rainoldi A, Minetto MA, Merletti R (eds) Biomedical engineering in exercise and sports. Edizioni Minerva Medica, Torino, pp 199–207
go back to reference Francis S, Lin X, Aboushoushah S, White TP, Phillips M, Bowtell R, Constantinescu CS (2009) fMRI analysis of active, passive and electrically stimulated ankle dorsiflexion. Neuroimage 44:469–479PubMed Francis S, Lin X, Aboushoushah S, White TP, Phillips M, Bowtell R, Constantinescu CS (2009) fMRI analysis of active, passive and electrically stimulated ankle dorsiflexion. Neuroimage 44:469–479PubMed
go back to reference Gabriel DA, Kamen G, Frost G (2006) Neural adaptations to resistive exercise: mechanisms and recommendations for training practices. Sports Med 36:133–149PubMed Gabriel DA, Kamen G, Frost G (2006) Neural adaptations to resistive exercise: mechanisms and recommendations for training practices. Sports Med 36:133–149PubMed
go back to reference Glinsky J, Harvey L, van Es P, Chee S, Gandevia SC (2009) The addition of electrical stimulation to progressive resistance training does not enhance the wrist strength of people with tetraplegia: a randomized controlled trial. Clin Rehabil 23:696–704PubMed Glinsky J, Harvey L, van Es P, Chee S, Gandevia SC (2009) The addition of electrical stimulation to progressive resistance training does not enhance the wrist strength of people with tetraplegia: a randomized controlled trial. Clin Rehabil 23:696–704PubMed
go back to reference Golaszewski SM, Bergmann J, Christova M, Nardone R, Kronbichler M, Rafolt D, Gallasch E, Staffen W, Ladurner G, Beisteiner R (2010) Increased motor cortical excitability after whole-hand electrical stimulation: a TMS study. Clin Neurophysiol 121:248–254PubMed Golaszewski SM, Bergmann J, Christova M, Nardone R, Kronbichler M, Rafolt D, Gallasch E, Staffen W, Ladurner G, Beisteiner R (2010) Increased motor cortical excitability after whole-hand electrical stimulation: a TMS study. Clin Neurophysiol 121:248–254PubMed
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 37:1291–1299PubMed Gondin J, Guette M, Ballay Y, Martin A (2005) Electromyostimulation training effects on neural drive and muscle architecture. Med Sci Sports Exerc 37:1291–1299PubMed
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 95:3328–3335PubMed Gondin J, Duclay J, Martin A (2006) Soleus- and gastrocnemii-evoked V-wave responses increase after neuromuscular electrical stimulation training. J Neurophysiol 95:3328–3335PubMed
go back to reference Gondin J, Brocca L, Bellinzona E, D’Antona G, Maffiuletti NA, Miotti D, Pellegrino MA, Bottinelli R (2011) Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: a functional and proteomic analysis. J Appl Physiol 110:433–450PubMed Gondin J, Brocca L, Bellinzona E, D’Antona G, Maffiuletti NA, Miotti D, Pellegrino MA, Bottinelli R (2011) Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: a functional and proteomic analysis. J Appl Physiol 110:433–450PubMed
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 Gruber M, Taube W, Gollhofer A, Beck S, Amtage F, Schubert M (2007) Training-specific adaptations of H- and stretch reflexes in human soleus muscle. J Mot Behav 39:68–78PubMed Gruber M, Taube W, Gollhofer A, Beck S, Amtage F, Schubert M (2007) Training-specific adaptations of H- and stretch reflexes in human soleus muscle. J Mot Behav 39:68–78PubMed
go back to reference Han BS, Jang SH, Chang Y, Byun WM, Lim SK, Kang DS (2003) Functional magnetic resonance image finding of cortical activation by neuromuscular electrical stimulation on wrist extensor muscles. Am J Phys Med Rehabil 82:17–20PubMed Han BS, Jang SH, Chang Y, Byun WM, Lim SK, Kang DS (2003) Functional magnetic resonance image finding of cortical activation by neuromuscular electrical stimulation on wrist extensor muscles. Am J Phys Med Rehabil 82:17–20PubMed
go back to reference Hortobágyi T, DeVita P (2000) Favorable neuromuscular and cardiovascular responses to 7 days of exercise with an eccentric overload in elderly women. J Gerontol A Biol Sci Med Sci 55:B401–B410PubMed Hortobágyi T, DeVita P (2000) Favorable neuromuscular and cardiovascular responses to 7 days of exercise with an eccentric overload in elderly women. J Gerontol A Biol Sci Med Sci 55:B401–B410PubMed
go back to reference Hortobágyi T, Lambert J, Scott K (1998) Incomplete muscle activation after training with electromyostimulation. Can J Appl Physiol 23:261–270PubMed Hortobágyi T, Lambert J, Scott K (1998) Incomplete muscle activation after training with electromyostimulation. Can J Appl Physiol 23:261–270PubMed
go back to reference Hortobágyi T, Scott K, Lambert J, Hamilton G, Tracy J (1999) Cross-education of muscle strength is greater with stimulated than voluntary contractions. Mot Control 3:205–219 Hortobágyi T, Scott K, Lambert J, Hamilton G, Tracy J (1999) Cross-education of muscle strength is greater with stimulated than voluntary contractions. Mot Control 3:205–219
go back to reference Hortobágyi T, Devita P, Money J, Barrier J (2001) Effects of standard and eccentric overload strength training in young women. Med Sci Sports Exerc 33:1206–1212PubMed Hortobágyi T, Devita P, Money J, Barrier J (2001) Effects of standard and eccentric overload strength training in young women. Med Sci Sports Exerc 33:1206–1212PubMed
go back to reference Hortobágyi T, Taylor JL, Russell G, Petersen N, Gandevia SC (2003) Changes in segmental and motor cortical output with contralateral muscle contractions and altered sensory inputs in humans. J Neurophysiol 90:2451–2459PubMed Hortobágyi T, Taylor JL, Russell G, Petersen N, Gandevia SC (2003) Changes in segmental and motor cortical output with contralateral muscle contractions and altered sensory inputs in humans. J Neurophysiol 90:2451–2459PubMed
go back to reference Hortobágyi T, Richardson SP, Lomarev M, Shamim E, Meunier S, Russman H, Dang N, Hallett M (2009) Chronic low-frequency rTMS of primary motor cortex diminishes exercise training-induced gains in maximal voluntary force in humans. J Appl Physiol 106:403–411PubMed Hortobágyi T, Richardson SP, Lomarev M, Shamim E, Meunier S, Russman H, Dang N, Hallett M (2009) Chronic low-frequency rTMS of primary motor cortex diminishes exercise training-induced gains in maximal voluntary force in humans. J Appl Physiol 106:403–411PubMed
go back to reference Hortobágyi T, Richardson SP, Lomarev M, Shamim E, Meunier S, Russman H, Dang N, Hallett M (2011) Interhemispheric plasticity in humans. Med Sci Sports Exerc (in press) Hortobágyi T, Richardson SP, Lomarev M, Shamim E, Meunier S, Russman H, Dang N, Hallett M (2011) Interhemispheric plasticity in humans. Med Sci Sports Exerc (in press)
go back to reference Howard JD, Enoka RM (1991) Maximum bilateral contractions are modified by neurally mediated interlimb effects. J Appl Physiol 70:306–316PubMed Howard JD, Enoka RM (1991) Maximum bilateral contractions are modified by neurally mediated interlimb effects. J Appl Physiol 70:306–316PubMed
go back to reference Huang LP, Zhou S, Lu Z, Tian Q, Li X, Cao LJ, Yu JH, Wang H (2007) Bilateral effect of unilateral electroacupuncture on muscle strength. J Altern Complement Med 13:539–546PubMed Huang LP, Zhou S, Lu Z, Tian Q, Li X, Cao LJ, Yu JH, Wang H (2007) Bilateral effect of unilateral electroacupuncture on muscle strength. J Altern Complement Med 13:539–546PubMed
go back to reference Jarvis JC, Mokrusch T, Kwende MM, Sutherland H, Salmons S (1996) Fast-to-slow transformation in stimulated rat muscle. Muscle Nerve 19:1469–1475PubMed Jarvis JC, Mokrusch T, Kwende MM, Sutherland H, Salmons S (1996) Fast-to-slow transformation in stimulated rat muscle. Muscle Nerve 19:1469–1475PubMed
go back to reference Jubeau M, Zory R, Gondin J, Martin A, Maffiuletti NA (2006) Late neural adaptations to electrostimulation resistance training of the plantar flexor muscles. Eur J Appl Physiol 98:202–211PubMed Jubeau M, Zory R, Gondin J, Martin A, Maffiuletti NA (2006) Late neural adaptations to electrostimulation resistance training of the plantar flexor muscles. Eur J Appl Physiol 98:202–211PubMed
go back to reference Jubeau M, Gondin J, Martin A, Van Hoecke J, Maffiuletti NA (2010) Differences in twitch potentiation between voluntary and stimulated quadriceps contractions of equal intensity. Scand J Med Sci Sports 20:56–62 Jubeau M, Gondin J, Martin A, Van Hoecke J, Maffiuletti NA (2010) Differences in twitch potentiation between voluntary and stimulated quadriceps contractions of equal intensity. Scand J Med Sci Sports 20:56–62
go back to reference Kaelin-Lang A, Luft AR, Sawaki L, Burstein AH, Sohn YH, Cohen LG (2002) Modulation of human corticomotor excitability by somatosensory input. J Physiol 540:623–633PubMed Kaelin-Lang A, Luft AR, Sawaki L, Burstein AH, Sohn YH, Cohen LG (2002) Modulation of human corticomotor excitability by somatosensory input. J Physiol 540:623–633PubMed
go back to reference Kendall TL, Black CD, Elder CP, Gorgey A, Dudley GA (2006) Determining the extent of neural activation during maximal effort. Med Sci Sports Exerc 38:1470–1475PubMed Kendall TL, Black CD, Elder CP, Gorgey A, Dudley GA (2006) Determining the extent of neural activation during maximal effort. Med Sci Sports Exerc 38:1470–1475PubMed
go back to reference Kent-Braun JA, Le Blanc R (1996) Quantitation of central activation failure during maximal voluntary contractions in humans. Muscle Nerve 19:861–869PubMed Kent-Braun JA, Le Blanc R (1996) Quantitation of central activation failure during maximal voluntary contractions in humans. Muscle Nerve 19:861–869PubMed
go back to reference Khaslavskaia S, Sinkjaer T (2005) Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive. Exp Brain Res 162:497–502PubMed Khaslavskaia S, Sinkjaer T (2005) Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive. Exp Brain Res 162:497–502PubMed
go back to reference Kim CK, Takala TE, Seger J, Karpakka J (1995) Training effects of electrically induced dynamic contractions in human quadriceps muscle. Aviat Space Environ Med 66:251–255PubMed Kim CK, Takala TE, Seger J, Karpakka J (1995) Training effects of electrically induced dynamic contractions in human quadriceps muscle. Aviat Space Environ Med 66:251–255PubMed
go back to reference Kimberley TJ, Lewis SM, Auerbach EJ, Dorsey LL, Lojovich JM, Carey JR (2004) Electrical stimulation driving functional improvements and cortical changes in subjects with stroke. Exp Brain Res 154:450–460PubMed Kimberley TJ, Lewis SM, Auerbach EJ, Dorsey LL, Lojovich JM, Carey JR (2004) Electrical stimulation driving functional improvements and cortical changes in subjects with stroke. Exp Brain Res 154:450–460PubMed
go back to reference Klakowicz PM, Baldwin ER, Collins DF (2006) Contribution of M-waves and H-reflexes to contractions evoked by tetanic nerve stimulation in humans. J Neurophysiol 96:1293–1302PubMed Klakowicz PM, Baldwin ER, Collins DF (2006) Contribution of M-waves and H-reflexes to contractions evoked by tetanic nerve stimulation in humans. J Neurophysiol 96:1293–1302PubMed
go back to reference Klass M, Baudry S, Duchateau J (2007) Voluntary activation during maximal contraction with advancing age: a brief review. Eur J Appl Physiol 100:543–551PubMed Klass M, Baudry S, Duchateau J (2007) Voluntary activation during maximal contraction with advancing age: a brief review. Eur J Appl Physiol 100:543–551PubMed
go back to reference Lagerquist O, Zehr EP, Docherty D (2006) Increased spinal reflex excitability is not associated with neural plasticity underlying the cross-education effect. J Appl Physiol 100:83–90PubMed Lagerquist O, Zehr EP, Docherty D (2006) Increased spinal reflex excitability is not associated with neural plasticity underlying the cross-education effect. J Appl Physiol 100:83–90PubMed
go back to reference Langzam E, Nemirovsky Y, Isakov E, Mizrahi J (2006) Partition between volitional and induced forces in electrically augmented dynamic isometric muscle contractions. IEEE Trans Neural Syst Rehabil Eng 14:322–335PubMed Langzam E, Nemirovsky Y, Isakov E, Mizrahi J (2006) Partition between volitional and induced forces in electrically augmented dynamic isometric muscle contractions. IEEE Trans Neural Syst Rehabil Eng 14:322–335PubMed
go back to reference Langzam E, Nemirovsky Y, Isakov E, Mizrahi J (2007) Muscle enhancement using closed-loop electrical stimulation: volitional versus induced torque. J Electromyogr Kinesiol 17:275–284PubMed Langzam E, Nemirovsky Y, Isakov E, Mizrahi J (2007) Muscle enhancement using closed-loop electrical stimulation: volitional versus induced torque. J Electromyogr Kinesiol 17:275–284PubMed
go back to reference Lee M, Hinder MR, Gandevia SC, Carroll TJ (2010) The ipsilateral motor cortex contributes to cross-limb transfer of performance gains after ballistic motor practice. J Physiol 588:201–212PubMed Lee M, Hinder MR, Gandevia SC, Carroll TJ (2010) The ipsilateral motor cortex contributes to cross-limb transfer of performance gains after ballistic motor practice. J Physiol 588:201–212PubMed
go back to reference Lieber RL, Silva PD, Daniel DM (1996) Equal effectiveness of electrical and volitional strength training for quadriceps femoris muscles after anterior cruciate ligament surgery. J Orthop Res 14:131–138PubMed Lieber RL, Silva PD, Daniel DM (1996) Equal effectiveness of electrical and volitional strength training for quadriceps femoris muscles after anterior cruciate ligament surgery. J Orthop Res 14:131–138PubMed
go back to reference Lloyd T, De Domenico G, Strauss GR, Singer K (1986) A review of the use of electro-motor stimulation in human muscles. Aust J Physiother 32:18–30 Lloyd T, De Domenico G, Strauss GR, Singer K (1986) A review of the use of electro-motor stimulation in human muscles. Aust J Physiother 32:18–30
go back to reference Maffiuletti NA (2010) Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 110:223–234PubMed Maffiuletti NA (2010) Physiological and methodological considerations for the use of neuromuscular electrical stimulation. Eur J Appl Physiol 110:223–234PubMed
go back to reference Maffiuletti NA, Pensini M, Martin A (2002) Activation of human plantar flexor muscles increases after electromyostimulation training. J Appl Physiol 92:1383–1392PubMed Maffiuletti NA, Pensini M, Martin A (2002) Activation of human plantar flexor muscles increases after electromyostimulation training. J Appl Physiol 92:1383–1392PubMed
go back to reference Maffiuletti NA, Pensini M, Scaglioni G, Ferri A, Ballay Y, Martin A (2003) Effect of electromyostimulation training on soleus and gastrocnemii H- and T-reflex properties. Eur J Appl Physiol 90:601–607PubMed Maffiuletti NA, Pensini M, Scaglioni G, Ferri A, Ballay Y, Martin A (2003) Effect of electromyostimulation training on soleus and gastrocnemii H- and T-reflex properties. Eur J Appl Physiol 90:601–607PubMed
go back to reference Martin L, Cometti G, Pousson M, Morlon B (1993) Effect of electrical stimulation training on the contractile characteristics of the triceps surae muscle. Eur J Appl Physiol Occup Physiol 67:457–461PubMed Martin L, Cometti G, Pousson M, Morlon B (1993) Effect of electrical stimulation training on the contractile characteristics of the triceps surae muscle. Eur J Appl Physiol Occup Physiol 67:457–461PubMed
go back to reference Martin L, Cometti G, Pousson M, Morlon B (1994) The influence of electrostimulation on mechanical and morphological characteristics of the triceps surae. J Sports Sci 12:377–381PubMed Martin L, Cometti G, Pousson M, Morlon B (1994) The influence of electrostimulation on mechanical and morphological characteristics of the triceps surae. J Sports Sci 12:377–381PubMed
go back to reference McMiken DF, Todd-Smith M, Thompson C (1983) Strengthening of human quadriceps muscles by cutaneous electrical stimulation. Scand J Rehabil Med 15:25–28PubMed McMiken DF, Todd-Smith M, Thompson C (1983) Strengthening of human quadriceps muscles by cutaneous electrical stimulation. Scand J Rehabil Med 15:25–28PubMed
go back to reference Merton P (1954) Voluntary strength and muscle fatigue. J Physiol 123:553–564PubMed Merton P (1954) Voluntary strength and muscle fatigue. J Physiol 123:553–564PubMed
go back to reference Nudo RJ, Plautz EJ, Frost SB (2001) Role of adaptive plasticity in recovery of function after damage to motor cortex. Muscle Nerve 24:1000–1019PubMed Nudo RJ, Plautz EJ, Frost SB (2001) Role of adaptive plasticity in recovery of function after damage to motor cortex. Muscle Nerve 24:1000–1019PubMed
go back to reference Nuhr M, Crevenna R, Gohlsch B, Bittner C, Pleiner J, Wiesinger G, Fialka-Moser V, Quittan M, Pette D (2003) Functional and biochemical properties of chronically stimulated human skeletal muscle. Eur J Appl Physiol 89:202–208PubMed Nuhr M, Crevenna R, Gohlsch B, Bittner C, Pleiner J, Wiesinger G, Fialka-Moser V, Quittan M, Pette D (2003) Functional and biochemical properties of chronically stimulated human skeletal muscle. Eur J Appl Physiol 89:202–208PubMed
go back to reference Ogino M, Shiba N, Maeda T, Iwasa K, Tagawa Y, Matsuo S, Nishimura H, Yamamoto T, Nagata K, Basford JR (2002) MRI quantification of muscle activity after volitional exercise and neuromuscular electrical stimulation. Am J Phys Med Rehabil 81:446–451PubMed Ogino M, Shiba N, Maeda T, Iwasa K, Tagawa Y, Matsuo S, Nishimura H, Yamamoto T, Nagata K, Basford JR (2002) MRI quantification of muscle activity after volitional exercise and neuromuscular electrical stimulation. Am J Phys Med Rehabil 81:446–451PubMed
go back to reference Paillard T, Noe F, Passelergue P, Dupui P (2005) Electrical stimulation superimposed onto voluntary muscular contraction. Sports Med 35:951–966PubMed Paillard T, Noe F, Passelergue P, Dupui P (2005) Electrical stimulation superimposed onto voluntary muscular contraction. Sports Med 35:951–966PubMed
go back to reference Paillard T, Margnes E, Maitre J, Chaubet V, Francois Y, Jully JL, Gonzalez G, Borel L (2010) Electrical stimulation superimposed onto voluntary muscular contraction reduces deterioration of both postural control and quadriceps femoris muscle strength. Neuroscience 165:1471–1475PubMed Paillard T, Margnes E, Maitre J, Chaubet V, Francois Y, Jully JL, Gonzalez G, Borel L (2010) Electrical stimulation superimposed onto voluntary muscular contraction reduces deterioration of both postural control and quadriceps femoris muscle strength. Neuroscience 165:1471–1475PubMed
go back to reference Perez M, Lucia A, Rivero JL, Serrano AL, Calbet JA, Delgado MA, Chicharro JL (2002) Effects of transcutaneous short-term electrical stimulation on M.vastus lateralis characteristics of healthy young men. Pflugers Arch 443:866–874PubMed Perez M, Lucia A, Rivero JL, Serrano AL, Calbet JA, Delgado MA, Chicharro JL (2002) Effects of transcutaneous short-term electrical stimulation on M.vastus lateralis characteristics of healthy young men. Pflugers Arch 443:866–874PubMed
go back to reference Perot C, Goubel F, Mora I (1991) Quantification of T- and H-responses before and after a period of endurance training. Eur J Appl Physiol Occup Physiol 63:368–375PubMed Perot C, Goubel F, Mora I (1991) Quantification of T- and H-responses before and after a period of endurance training. Eur J Appl Physiol Occup Physiol 63:368–375PubMed
go back to reference Pette D, Vrbova G (1992) Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev Physiol Biochem Pharmacol 120:115–202PubMed Pette D, Vrbova G (1992) Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation. Rev Physiol Biochem Pharmacol 120:115–202PubMed
go back to reference Pichon F, Chatard JC, Martin A, Cometti G (1995) Electrical stimulation and swimming performance. Med Sci Sports Exerc 27:1671–1676PubMed Pichon F, Chatard JC, Martin A, Cometti G (1995) Electrical stimulation and swimming performance. Med Sci Sports Exerc 27:1671–1676PubMed
go back to reference Pierrot-Deseilligny E, Bussel B, Sideri G, Cathala HP, Castaigne P (1973) Effect of voluntary contraction on H reflex changes induced by cutaneous stimulation in normal man. Electroencephalogr Clin Neurophysiol 34:185–192PubMed Pierrot-Deseilligny E, Bussel B, Sideri G, Cathala HP, Castaigne P (1973) Effect of voluntary contraction on H reflex changes induced by cutaneous stimulation in normal man. Electroencephalogr Clin Neurophysiol 34:185–192PubMed
go back to reference Pierrot-Deseilligny E, Bergego C, Katz R, Morin C (1981) Cutaneous depression of Ib reflex pathways to motoneurones in man. Exp Brain Res 42:351–361PubMed Pierrot-Deseilligny E, Bergego C, Katz R, Morin C (1981) Cutaneous depression of Ib reflex pathways to motoneurones in man. Exp Brain Res 42:351–361PubMed
go back to reference Popovic MR, Curt A, Keller T, Dietz V (2001) Functional electrical stimulation for grasping and walking: indications and limitations. Spinal Cord 39:403–412PubMed Popovic MR, Curt A, Keller T, Dietz V (2001) Functional electrical stimulation for grasping and walking: indications and limitations. Spinal Cord 39:403–412PubMed
go back to reference Ridding MC, Brouwer B, Miles TS, Pitcher JB, Thompson PD (2000) Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp Brain Res 131:135–143PubMed Ridding MC, Brouwer B, Miles TS, Pitcher JB, Thompson PD (2000) Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects. Exp Brain Res 131:135–143PubMed
go back to reference Ridding MC, McKay DR, Thompson PD, Miles TS (2001) Changes in corticomotor representations induced by prolonged peripheral nerve stimulation in humans. Clin Neurophysiol 112:1461–1469PubMed Ridding MC, McKay DR, Thompson PD, Miles TS (2001) Changes in corticomotor representations induced by prolonged peripheral nerve stimulation in humans. Clin Neurophysiol 112:1461–1469PubMed
go back to reference Robinson KL, McIlwain JS, Hayes KC (1979) Effects of H-reflex conditioning upon the contralateral alpha motoneuron pool. Electroencephalogr Clin Neurophysiol 46:65–71PubMed Robinson KL, McIlwain JS, Hayes KC (1979) Effects of H-reflex conditioning upon the contralateral alpha motoneuron pool. Electroencephalogr Clin Neurophysiol 46:65–71PubMed
go back to reference Ruther CL, Golden CL, Harris RT, Dudley GA (1995) Hypertrophy, resistance training, and the nature of skeletal muscle activation. J Strength Cond Res 9:155–159 Ruther CL, Golden CL, Harris RT, Dudley GA (1995) Hypertrophy, resistance training, and the nature of skeletal muscle activation. J Strength Cond Res 9:155–159
go back to reference Sale DG (1988) Neural adaptation to resistance training. Med Sci Sports Exerc 20:S135–S145PubMed Sale DG (1988) Neural adaptation to resistance training. Med Sci Sports Exerc 20:S135–S145PubMed
go back to reference Scaglioni G, Ferri A, Minetti AE, Martin A, Van Hoecke J, Capodaglio P, Sartorio A, Narici MV (2002) Plantar flexor activation capacity and H reflex in older adults: adaptations to strength training. J Appl Physiol 92:2292–2302PubMed Scaglioni G, Ferri A, Minetti AE, Martin A, Van Hoecke J, Capodaglio P, Sartorio A, Narici MV (2002) Plantar flexor activation capacity and H reflex in older adults: adaptations to strength training. J Appl Physiol 92:2292–2302PubMed
go back to reference Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, Vianello M, Gundersen K, Lomo T (1989) Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Muscle Res Cell Motil 10:197–205PubMed Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, Vianello M, Gundersen K, Lomo T (1989) Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Muscle Res Cell Motil 10:197–205PubMed
go back to reference Scott OM, Vrbova G, Hyde SA, Dubowitz V (1985) Effects of chronic low frequency electrical stimulation on normal human tibialis anterior muscle. J Neurol Neurosurg Psychiatry 48:774–781PubMed Scott OM, Vrbova G, Hyde SA, Dubowitz V (1985) Effects of chronic low frequency electrical stimulation on normal human tibialis anterior muscle. J Neurol Neurosurg Psychiatry 48:774–781PubMed
go back to reference Smith GV, Alon G, Roys SR, Gullapalli RP (2003) Functional MRI determination of a dose-response relationship to lower extremity neuromuscular electrical stimulation in healthy subjects. Exp Brain Res 150:33–39PubMed Smith GV, Alon G, Roys SR, Gullapalli RP (2003) Functional MRI determination of a dose-response relationship to lower extremity neuromuscular electrical stimulation in healthy subjects. Exp Brain Res 150:33–39PubMed
go back to reference St Pierre D, Taylor AW, Lavoie M, Sellers W, Kots YM (1986) Effects of 2,500 Hz sinusoidal current on fibre area and strength of the quadriceps femoris. J Sports Med Phys Fitness 26:60–66PubMed St Pierre D, Taylor AW, Lavoie M, Sellers W, Kots YM (1986) Effects of 2,500 Hz sinusoidal current on fibre area and strength of the quadriceps femoris. J Sports Med Phys Fitness 26:60–66PubMed
go back to reference Stein RB, Everaert DG, Thompson AK, Chong SL, Whittaker M, Robertson J, Kuether G (2010) Long-term therapeutic and orthotic effects of a foot drop stimulator on walking performance in progressive and nonprogressive neurological disorders. Neurorehabil Neural Repair 24:152–167PubMed Stein RB, Everaert DG, Thompson AK, Chong SL, Whittaker M, Robertson J, Kuether G (2010) Long-term therapeutic and orthotic effects of a foot drop stimulator on walking performance in progressive and nonprogressive neurological disorders. Neurorehabil Neural Repair 24:152–167PubMed
go back to reference Stevens JE, Mizner RL, Snyder-Mackler L (2004) Neuromuscular electrical stimulation for quadriceps muscle strengthening after bilateral total knee arthroplasty: a case series. J Orthop Sports Phys Ther 34:21–29PubMed Stevens JE, Mizner RL, Snyder-Mackler L (2004) Neuromuscular electrical stimulation for quadriceps muscle strengthening after bilateral total knee arthroplasty: a case series. J Orthop Sports Phys Ther 34:21–29PubMed
go back to reference Stevenson SW, Dudley GA (2001) Dietary creatine supplementation and muscular adaptation to resistive overload. Med Sci Sports Exerc 33:1304–1310PubMed Stevenson SW, Dudley GA (2001) Dietary creatine supplementation and muscular adaptation to resistive overload. Med Sci Sports Exerc 33:1304–1310PubMed
go back to reference Tamaki T, Uchiyama S, Uchiyama Y, Akatsuka A, Yoshimura S, Roy RR, Edgerton VR (2000) Limited myogenic response to a single bout of weight-lifting exercise in old rats. Am J Physiol Cell Physiol 278:C1143–C1152PubMed Tamaki T, Uchiyama S, Uchiyama Y, Akatsuka A, Yoshimura S, Roy RR, Edgerton VR (2000) Limited myogenic response to a single bout of weight-lifting exercise in old rats. Am J Physiol Cell Physiol 278:C1143–C1152PubMed
go back to reference Taube W, Kullmann N, Leukel C, Kurz O, Amtage F, Gollhofer A (2007) Differential reflex adaptations following sensorimotor and strength training in young elite athletes. Int J Sports Med 28:999–1005PubMed Taube W, Kullmann N, Leukel C, Kurz O, Amtage F, Gollhofer A (2007) Differential reflex adaptations following sensorimotor and strength training in young elite athletes. Int J Sports Med 28:999–1005PubMed
go back to reference Taylor J (2009) The interpolated twitch does provide a valid measure of the voluntary activation of muscle. J Appl Physiol 107:354–358PubMed Taylor J (2009) The interpolated twitch does provide a valid measure of the voluntary activation of muscle. J Appl Physiol 107:354–358PubMed
go back to reference Theriault R, Boulay MR, Theriault G, Simoneau JA (1996) Electrical stimulation-induced changes in performance and fiber type proportion of human knee extensor muscles. Eur J Appl Physiol Occup Physiol 74:311–317PubMed Theriault R, Boulay MR, Theriault G, Simoneau JA (1996) Electrical stimulation-induced changes in performance and fiber type proportion of human knee extensor muscles. Eur J Appl Physiol Occup Physiol 74:311–317PubMed
go back to reference Thorstensson A, Hulten B, von Dobeln W, Karlsson J (1976) Effect of strength training on enzyme activities and fibre characteristics in human skeletal muscle. Acta Physiol Scand 96:392–398PubMed Thorstensson A, Hulten B, von Dobeln W, Karlsson J (1976) Effect of strength training on enzyme activities and fibre characteristics in human skeletal muscle. Acta Physiol Scand 96:392–398PubMed
go back to reference Trimble MH, Enoka RM (1991) Mechanisms underlying the training effects associated with neuromuscular electrical stimulation. Phys Ther 71:273–280; discussion 280–282 Trimble MH, Enoka RM (1991) Mechanisms underlying the training effects associated with neuromuscular electrical stimulation. Phys Ther 71:273–280; discussion 280–282
go back to reference Vanderthommen M, Duteil S, Wary C, Raynaud JS, Leroy-Willig A, Crielaard JM, Carlier PG (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, Raynaud JS, Leroy-Willig A, Crielaard JM, Carlier PG (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 Voigt M, Chelli F, Frigo C (1998) Changes in the excitability of soleus muscle short latency stretch reflexes during human hopping after 4 weeks of hopping training. Eur J Appl Physiol Occup Physiol 78:522–532PubMed Voigt M, Chelli F, Frigo C (1998) Changes in the excitability of soleus muscle short latency stretch reflexes during human hopping after 4 weeks of hopping training. Eur J Appl Physiol Occup Physiol 78:522–532PubMed
go back to reference Wolpaw JR (2007) Spinal cord plasticity in acquisition and maintenance of motor skills. Acta Physiol (Oxf) 189:155–169 Wolpaw JR (2007) Spinal cord plasticity in acquisition and maintenance of motor skills. Acta Physiol (Oxf) 189:155–169
go back to reference Zehr PE (2002) Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86:455–468PubMed Zehr PE (2002) Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86:455–468PubMed
go back to reference Zhou S (2000) Chronic neural adaptations to unilateral exercise: mechanisms of cross education. Exerc Sport Sci Rev 28:177–184PubMed Zhou S (2000) Chronic neural adaptations to unilateral exercise: mechanisms of cross education. Exerc Sport Sci Rev 28:177–184PubMed
Metadata
Title
Neural adaptations to electrical stimulation strength training
Authors
Tibor Hortobágyi
Nicola A. Maffiuletti
Publication date
01-10-2011
Publisher
Springer-Verlag
Published in
European Journal of Applied Physiology / Issue 10/2011
Print ISSN: 1439-6319
Electronic ISSN: 1439-6327
DOI
https://doi.org/10.1007/s00421-011-2012-2

Other articles of this Issue 10/2011

European Journal of Applied Physiology 10/2011 Go to the issue