Neural adaptations to electrical stimulation strength training

European Journal of Applied Physiology

Volumn 111, Issue 10, 2011, Pages 2439-2449

  Hortobágyi, Tibor ^a   Maffiuletti, Nicola A ^b  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b SCHULTHESS CLINIC   (Switzerland)

Author keywords

Magnetic brain stimulation; MRI; Muscle; Rehabilitation; Strength training

Indexed keywords

ADAPTATION; ANIMAL; BRAIN; ELECTROSTIMULATION; HUMAN; METHODOLOGY; MOTONEURON; MUSCLE STRENGTH; PHYSIOLOGY; RESISTANCE TRAINING; REVIEW;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BRAIN; ELECTRIC STIMULATION; HUMANS; MOTOR NEURONS; MUSCLE STRENGTH; RESISTANCE TRAINING;

EID: 80053923352     PISSN: 14396319     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00421-011-2012-2     Document Type: Review

References (113)

1. P Aagaard EB Simonsen JL Andersen P Magnusson P Dyhre-Poulsen 2002 Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses J Appl Physiol 92 2309 2318 12015341 (Pubitemid 34666352)
2. T Arya S Bajwa SA Edgley 1991 Crossed reflex actions from group II muscle afferents in the lumbar spinal cord of the anaesthetized cat J Physiol 444 117 131 1822547 1:STN:280:DyaK38zkvFaqsA%3D%3D
3. ER Baldwin PM Klakowicz DF Collins 2006 Wide-pulse-width, high-frequency neuromuscular stimulation: implications for functional electrical stimulation J Appl Physiol 101 228 240 16627680 (Pubitemid 44035369)
4. L Bax F Staes A Verhagen 2005 Does neuromuscular electrical stimulation strengthen the quadriceps femoris? A systematic review of randomised controlled trials Sports Med 35 191 212 15730336 (Pubitemid 40461561)
5. 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)
6. P Bezerra S Zhou Z Crowley L Brooks A Hooper 2009 Effects of unilateral electromyostimulation superimposed on voluntary training on strength and cross-sectional area Muscle Nerve 40 430 437 19705423
7. A Blickenstorfer R Kleiser T Keller B Keisker M Meyer R Riener S Kollias 2009 Cortical and subcortical correlates of functional electrical stimulation of wrist extensor and flexor muscles revealed by fMRI Hum Brain Mapp 30 963 975 18344193
8. F Brocherie N Babault G Cometti N Maffiuletti JC Chatard 2005 Electrostimulation training effects on the physical performance of ice hockey players Med Sci Sports Exerc 37 455 460 15741845 (Pubitemid 40354456)
9. M Cabric HJ Appell 1987 Effect of electrical stimulation of high and low frequency on maximum isometric force and some morphological characteristics in men Int J Sports Med 8 256 260 3667021 1:STN:280:DyaL1c%2FjtFymsQ%3D%3D (Pubitemid 17122790)
10. M Cabric HJ Appell A Resic 1987 Effects of electrical stimulation of different frequencies on the myonuclei and fiber size in human muscle Int J Sports Med 8 323 326 3679646 1:STN:280:DyaL1c%2Flslyjsw%3D%3D
11. TJ Carroll S Riek RG Carson 2001 Neural adaptations to resistance training: implications for movement control Sports Med 31 829 840 11665911 1:STN:280:DC%2BD3MrmsVKlsA%3D%3D (Pubitemid 32959905)
12. TJ Carroll S Riek RG Carson 2002 The sites of neural adaptation induced by resistance training in humans J Physiol 544 641 652 12381833 1:CAS:528:DC%2BD38XoslSjsr4%3D (Pubitemid 35244276)
13. TJ Carroll VS Selvanayagam S Riek JG Semmler 2011 Neural adaptations to strength training: moving beyond TMS and reflex studies Acta Physiol (Oxf) 202 2 119 140 1:CAS:528:DC%2BC3MXmvFGls7w%3D
14. P Cavallari E Fournier R Katz K Malmgren E Pierrot-Deseilligny M Shindo 1985 Cutaneous facilitation of transmission in Ib reflex pathways in the human upper limb Exp Brain Res 60 197 199 4043278 1:STN:280:DyaL28%2FgsFaltQ%3D%3D (Pubitemid 16252121)
15. 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
16. A Christie G Kamen 2010 Short-term training adaptations in maximal motor unit firing rates and afterhyperpolarization duration Muscle Nerve 41 651 660 19941348
17. DF Collins 2007 Central contributions to contractions evoked by tetanic neuromuscular electrical stimulation Exerc Sport Sci Rev 35 102 109 17620928 (Pubitemid 47056546)
18. DF Collins D Burke SC Gandevia 2002 Sustained contractions produced by plateau-like behaviour in human motoneurones J Physiol 538 289 301 11773336 1:CAS:528:DC%2BD38XislGmtrY%3D (Pubitemid 35190057)
19. SS Colson A Martin J Van Hoecke 2009 Effects of electromyostimulation versus voluntary isometric training on elbow flexor muscle strength J Electromyogr Kinesiol 19 311 319
20. A Costa H Dalloul H Hegyesi P Apor Z Csende L Racz M Vaczi J Tihanyi 2007 Impact of repeated bouts of eccentric exercise on myogenic gene expression Eur J Appl Physiol 101 427 436 17641910 (Pubitemid 47500361)
21. A de Haan KHL Gerrits CJ de Ruiter 2009 Counterpoint: the interpolated twitch does not provide a valid measure of the voluntary activation of muscle J Appl Physiol 107 355 357 19567806
22. C Del Balso E Cafarelli 2007 Adaptations in the activation of human skeletal muscle induced by short-term isometric resistance training J Appl Physiol 103 402 411 17446407 (Pubitemid 47092318)
23. K Dragert EP Zehr 2011 Bilateral neuromuscular plasticity from unilateral training of the ankle dorsiflexors Exp Brain Res 208 217 227 21069308
24. J Duchateau K Hainaut 1988 Training effects of sub-maximal electrostimulation in a human muscle Med Sci Sports Exerc 20 99 104 3343922 1:STN:280:DyaL1c7kt1ChtA%3D%3D
25. J Duclay A Martin A Robbe M Pousson 2008 Spinal reflex plasticity during maximal dynamic contractions after eccentric training Med Sci Sports Exerc 40 722 734 18317371 (Pubitemid 351416847)
26. RM Enoka 1988 Muscle strength and its development. New perspectives Sports Med 6 146 168 3055145 1:STN:280:DyaL1M%2Fktlertg%3D%3D
27. 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
28. E Eriksson T Haggmark KH Kiessling J Karlsson 1981 Effect of electrical stimulation on human skeletal muscle Int J Sports Med 2 18 22 7333731 1:STN:280:DyaL387ktFamtg%3D%3D (Pubitemid 11118318)
29. DG Everaert AK Thompson SL Chong RB Stein 2010 Does functional electrical stimulation for foot drop strengthen corticospinal connections? Neurorehabil Neural Repair 24 168 177 19861590
30. D Farina A Holobar R Merletti RM Enoka 2010 Decoding the neural drive to muscles from the surface electromyogram Clin Neurophysiol 121 1616 1623 20444646
31. JP Farthing 2009 Cross-education of strength depends on limb dominance: implications for theory and application Exerc Sport Sci Rev 37 179 187 19955867
32. 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)
33. MS Fimland J Helgerud GM Solstad VM Iversen G Leivseth J Hoff 2009 Neural adaptations underlying cross-education after unilateral strength training Eur J Appl Physiol 107 723 730 19756705
34. 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
35. S Francis X Lin S Aboushoushah TP White M Phillips R Bowtell CS Constantinescu 2009 fMRI analysis of active, passive and electrically stimulated ankle dorsiflexion Neuroimage 44 469 479 18950717
36. DA Gabriel G Kamen G Frost 2006 Neural adaptations to resistive exercise: mechanisms and recommendations for training practices Sports Med 36 133 149 16464122 (Pubitemid 43242218)
37. J Glinsky L Harvey P van Es S Chee SC Gandevia 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 23 696 704 19470552
38. SM Golaszewski J Bergmann M Christova R Nardone M Kronbichler D Rafolt E Gallasch W Staffen G Ladurner R Beisteiner 2010 Increased motor cortical excitability after whole-hand electrical stimulation: a TMS study Clin Neurophysiol 121 248 254 20036618
39. J Gondin M Guette Y Ballay A Martin 2005 Electromyostimulation training effects on neural drive and muscle architecture Med Sci Sports Exerc 37 1291 1299 16118574 (Pubitemid 41209282)
40. J Gondin J Duclay A Martin 2006 Soleus- and gastrocnemii-evoked V-wave responses increase after neuromuscular electrical stimulation training J Neurophysiol 95 3328 3335 16481458 (Pubitemid 43846144)
41. J Gondin L Brocca E Bellinzona G D'Antona NA Maffiuletti D Miotti MA Pellegrino R Bottinelli 2011 Neuromuscular electrical stimulation training induces atypical adaptations of the human skeletal muscle phenotype: a functional and proteomic analysis J Appl Physiol 110 433 450 21127206 1:CAS:528:DC%2BC3MXis1Cisrw%3D
42. CM Gregory CS Bickel 2005 Recruitment patterns in human skeletal muscle during electrical stimulation Phys Ther 85 358 364 15794706 (Pubitemid 40411546)
43. M Gruber W Taube A Gollhofer S Beck F Amtage M Schubert 2007 Training-specific adaptations of H- and stretch reflexes in human soleus muscle J Mot Behav 39 68 78 17251172 1:STN:280:DC%2BD2s%2FkslGntw%3D%3D (Pubitemid 46175723)
44. BS Han SH Jang Y Chang WM Byun SK Lim DS Kang 2003 Functional magnetic resonance image finding of cortical activation by neuromuscular electrical stimulation on wrist extensor muscles Am J Phys Med Rehabil 82 17 20 12510180 (Pubitemid 36043758)
45. T Hortobágyi P DeVita 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 B410 10952362 (Pubitemid 32009018)
46. T Hortobágyi J Lambert K Scott 1998 Incomplete muscle activation after training with electromyostimulation Can J Appl Physiol 23 261 270 9615868 (Pubitemid 128445061)
47. T Hortobágyi K Scott J Lambert G Hamilton J Tracy 1999 Cross-education of muscle strength is greater with stimulated than voluntary contractions Mot Control 3 205 219
48. T Hortobágyi P Devita J Money J Barrier 2001 Effects of standard and eccentric overload strength training in young women Med Sci Sports Exerc 33 1206 1212 11445770 (Pubitemid 32641323)
49. T Hortobágyi JL Taylor G Russell N Petersen SC Gandevia 2003 Changes in segmental and motor cortical output with contralateral muscle contractions and altered sensory inputs in humans J Neurophysiol 90 2451 2459 14534271 (Pubitemid 37266513)
50. T Hortobágyi SP Richardson M Lomarev E Shamim S Meunier H Russman N Dang M Hallett 2009 Chronic low-frequency rTMS of primary motor cortex diminishes exercise training-induced gains in maximal voluntary force in humans J Appl Physiol 106 403 411 19008488
51. 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)
52. JD Howard RM Enoka 1991 Maximum bilateral contractions are modified by neurally mediated interlimb effects J Appl Physiol 70 306 316 2010386 1:STN:280:DyaK3M7osFamsg%3D%3D
53. LP Huang S Zhou Z Lu Q Tian X Li LJ Cao JH Yu H Wang 2007 Bilateral effect of unilateral electroacupuncture on muscle strength J Altern Complement Med 13 539 546 17604558 (Pubitemid 47015338)
54. JC Jarvis T Mokrusch MM Kwende H Sutherland S Salmons 1996 Fast-to-slow transformation in stimulated rat muscle Muscle Nerve 19 1469 1475 8874405 1:STN:280:DyaK2s%2FivVeqsA%3D%3D (Pubitemid 26349504)
55. M Jubeau R Zory J Gondin A Martin NA Maffiuletti 2006 Late neural adaptations to electrostimulation resistance training of the plantar flexor muscles Eur J Appl Physiol 98 202 211 16944193 (Pubitemid 44349901)
56. M Jubeau J Gondin A Martin J Van Hoecke NA Maffiuletti 2010 Differences in twitch potentiation between voluntary and stimulated quadriceps contractions of equal intensity Scand J Med Sci Sports 20 56 62
57. A Kaelin-Lang AR Luft L Sawaki AH Burstein YH Sohn LG Cohen 2002 Modulation of human corticomotor excitability by somatosensory input J Physiol 540 623 633 11956348 1:CAS:528:DC%2BD38XjsFWru7s%3D (Pubitemid 35190136)
58. TL Kendall CD Black CP Elder A Gorgey GA Dudley 2006 Determining the extent of neural activation during maximal effort Med Sci Sports Exerc 38 1470 1475 16888461 (Pubitemid 44215756)
59. JA Kent-Braun R Le Blanc 1996 Quantitation of central activation failure during maximal voluntary contractions in humans Muscle Nerve 19 861 869 8965840 1:STN:280:DyaK283kslGltQ%3D%3D (Pubitemid 26190646)
60. S Khaslavskaia T Sinkjaer 2005 Motor cortex excitability following repetitive electrical stimulation of the common peroneal nerve depends on the voluntary drive Exp Brain Res 162 497 502 15702321 (Pubitemid 40684784)
61. CK Kim TE Takala J Seger J Karpakka 1995 Training effects of electrically induced dynamic contractions in human quadriceps muscle Aviat Space Environ Med 66 251 255 7661836 1:STN:280:DyaK2MzptV2nsw%3D%3D
62. TJ Kimberley SM Lewis EJ Auerbach LL Dorsey JM Lojovich JR Carey 2004 Electrical stimulation driving functional improvements and cortical changes in subjects with stroke Exp Brain Res 154 450 460 14618287 (Pubitemid 38293735)
63. PM Klakowicz ER Baldwin DF Collins 2006 Contribution of M-waves and H-reflexes to contractions evoked by tetanic nerve stimulation in humans J Neurophysiol 96 1293 1302 16611843 (Pubitemid 44371522)
64. M Klass S Baudry J Duchateau 2007 Voluntary activation during maximal contraction with advancing age: a brief review Eur J Appl Physiol 100 543 551 16763836 (Pubitemid 47023749)
65. O Lagerquist EP Zehr D Docherty 2006 Increased spinal reflex excitability is not associated with neural plasticity underlying the cross-education effect J Appl Physiol 100 83 90 16357081 (Pubitemid 43671093)
66. E Langzam Y Nemirovsky E Isakov J Mizrahi 2006 Partition between volitional and induced forces in electrically augmented dynamic isometric muscle contractions IEEE Trans Neural Syst Rehabil Eng 14 322 335 17009492 (Pubitemid 44543556)
67. E Langzam Y Nemirovsky E Isakov J Mizrahi 2007 Muscle enhancement using closed-loop electrical stimulation: volitional versus induced torque J Electromyogr Kinesiol 17 275 284 16690326 1:STN:280:DC%2BD2s3hs1WktQ%3D%3D (Pubitemid 46529485)
68. M Lee MR Hinder SC Gandevia TJ Carroll 2010 The ipsilateral motor cortex contributes to cross-limb transfer of performance gains after ballistic motor practice J Physiol 588 201 212 19917563 1:CAS:528:DC%2BC3cXntFKlsw%3D%3D
69. RL Lieber PD Silva DM Daniel 1996 Equal effectiveness of electrical and volitional strength training for quadriceps femoris muscles after anterior cruciate ligament surgery J Orthop Res 14 131 138 8618155 1:STN:280: DyaK287otFKmsw%3D%3D (Pubitemid 26091613)
70. T Lloyd G De Domenico GR Strauss K Singer 1986 A review of the use of electro-motor stimulation in human muscles Aust J Physiother 32 18 30 (Pubitemid 16036930)
71. NA Maffiuletti 2010 Physiological and methodological considerations for the use of neuromuscular electrical stimulation Eur J Appl Physiol 110 223 234 20473619
72. NA Maffiuletti M Pensini A Martin 2002 Activation of human plantar flexor muscles increases after electromyostimulation training J Appl Physiol 92 1383 1392 11896001 (Pubitemid 34670890)
73. NA Maffiuletti M Pensini G Scaglioni A Ferri Y Ballay A Martin 2003 Effect of electromyostimulation training on soleus and gastrocnemii H- and T-reflex properties Eur J Appl Physiol 90 601 607 12923640 (Pubitemid 37508867)
74. L Martin G Cometti M Pousson B Morlon 1993 Effect of electrical stimulation training on the contractile characteristics of the triceps surae muscle Eur J Appl Physiol Occup Physiol 67 457 461 8299618 1:STN:280: DyaK2c7jtVykuw%3D%3D (Pubitemid 23343678)
75. L Martin G Cometti M Pousson B Morlon 1994 The influence of electrostimulation on mechanical and morphological characteristics of the triceps surae J Sports Sci 12 377 381 7932948 1:STN:280:DyaK2M%2FhvVCksA%3D%3D (Pubitemid 24224572)
76. DF McMiken M Todd-Smith C Thompson 1983 Strengthening of human quadriceps muscles by cutaneous electrical stimulation Scand J Rehabil Med 15 25 28 6828830 1:STN:280:DyaL3s7ks1altQ%3D%3D
77. P Merton 1954 Voluntary strength and muscle fatigue J Physiol 123 553 564 13152698 1:STN:280:DyaG2c%2Fnt1Knuw%3D%3D
78. RJ Nudo EJ Plautz SB Frost 2001 Role of adaptive plasticity in recovery of function after damage to motor cortex Muscle Nerve 24 1000 1019 11439375 1:STN:280:DC%2BD3MzosFemsw%3D%3D (Pubitemid 32656186)
79. M Nuhr R Crevenna B Gohlsch C Bittner J Pleiner G Wiesinger V Fialka-Moser M Quittan D Pette 2003 Functional and biochemical properties of chronically stimulated human skeletal muscle Eur J Appl Physiol 89 202 208 12665986 1:CAS:528:DC%2BD3sXisVGhur4%3D (Pubitemid 36747978)
80. M Ogino N Shiba T Maeda K Iwasa Y Tagawa S Matsuo H Nishimura T Yamamoto K Nagata JR Basford 2002 MRI quantification of muscle activity after volitional exercise and neuromuscular electrical stimulation Am J Phys Med Rehabil 81 446 451 12023602 (Pubitemid 34564116)
81. T Paillard F Noe P Passelergue P Dupui 2005 Electrical stimulation superimposed onto voluntary muscular contraction Sports Med 35 951 966 16271009 (Pubitemid 41606572)
82. T Paillard E Margnes J Maitre V Chaubet Y Francois JL Jully G Gonzalez L Borel 2010 Electrical stimulation superimposed onto voluntary muscular contraction reduces deterioration of both postural control and quadriceps femoris muscle strength Neuroscience 165 1471 1475 19958816 1:CAS:528: DC%2BC3cXnsFWmug%3D%3D
83. M Perez A Lucia JL Rivero AL Serrano JA Calbet MA Delgado JL Chicharro 2002 Effects of transcutaneous short-term electrical stimulation on M.vastus lateralis characteristics of healthy young men Pflugers Arch 443 866 874 11889587 1:CAS:528:DC%2BD38Xhs1yqt7c%3D (Pubitemid 34234094)
84. C Perot F Goubel I Mora 1991 Quantification of T- and H-responses before and after a period of endurance training Eur J Appl Physiol Occup Physiol 63 368 375 1773814 1:STN:280:DyaK387ivVCqsg%3D%3D
85. D Pette G Vrbova 1992 Adaptation of mammalian skeletal muscle fibers to chronic electrical stimulation Rev Physiol Biochem Pharmacol 120 115 202 1519018 1:CAS:528:DyaK38XmtlSltbk%3D
86. F Pichon JC Chatard A Martin G Cometti 1995 Electrical stimulation and swimming performance Med Sci Sports Exerc 27 1671 1676 8614324 1:STN:280:DyaK287pt12jsQ%3D%3D
87. E Pierrot-Deseilligny B Bussel G Sideri HP Cathala P Castaigne 1973 Effect of voluntary contraction on H reflex changes induced by cutaneous stimulation in normal man Electroencephalogr Clin Neurophysiol 34 185 192 4119532 1:STN:280:DyaE3s%2FptVyjtw%3D%3D
88. E Pierrot-Deseilligny C Bergego R Katz C Morin 1981 Cutaneous depression of Ib reflex pathways to motoneurones in man Exp Brain Res 42 351 361 7238675 1:STN:280:DyaL3M3ht1Gjug%3D%3D (Pubitemid 11112364)
89. MR Popovic A Curt T Keller V Dietz 2001 Functional electrical stimulation for grasping and walking: indications and limitations Spinal Cord 39 403 412 11512070 1:STN:280:DC%2BD3MvmslWhsw%3D%3D (Pubitemid 32769801)
90. MC Ridding B Brouwer TS Miles JB Pitcher PD Thompson 2000 Changes in muscle responses to stimulation of the motor cortex induced by peripheral nerve stimulation in human subjects Exp Brain Res 131 135 143 10759179 1:STN:280:DC%2BD3c3itV2huw%3D%3D (Pubitemid 30137824)
91. MC Ridding DR McKay PD Thompson TS Miles 2001 Changes in corticomotor representations induced by prolonged peripheral nerve stimulation in humans Clin Neurophysiol 112 1461 1469 11459686 1:STN:280:DC%2BD3MvgvVShug%3D%3D (Pubitemid 32673715)
92. KL Robinson JS McIlwain KC Hayes 1979 Effects of H-reflex conditioning upon the contralateral alpha motoneuron pool Electroencephalogr Clin Neurophysiol 46 65 71 88332 1:STN:280:DyaE1M3htlamsw%3D%3D (Pubitemid 9047373)
93. CL Ruther CL Golden RT Harris GA Dudley 1995 Hypertrophy, resistance training, and the nature of skeletal muscle activation J Strength Cond Res 9 155 159
94. DG Sale 1988 Neural adaptation to resistance training Med Sci Sports Exerc 20 S135 S145 3057313 1:STN:280:DyaL1M%2Fls1KmtQ%3D%3D (Pubitemid 18266401)
95. G Scaglioni A Ferri AE Minetti A Martin J Van Hoecke P Capodaglio A Sartorio MV Narici 2002 Plantar flexor activation capacity and H reflex in older adults: adaptations to strength training J Appl Physiol 92 2292 2302 12015339 1:STN:280:DC%2BD383nsVygsw%3D%3D (Pubitemid 34666350)
96. S Schiaffino L Gorza S Sartore L Saggin S Ausoni M Vianello K Gundersen T Lomo 1989 Three myosin heavy chain isoforms in type 2 skeletal muscle fibres J Muscle Res Cell Motil 10 197 205 2547831 1:CAS:528:DyaL1MXltFalsrg%3D
97. OM Scott G Vrbova SA Hyde V Dubowitz 1985 Effects of chronic low frequency electrical stimulation on normal human tibialis anterior muscle J Neurol Neurosurg Psychiatry 48 774 781 4031929 1:STN:280:DyaL2M3ptFyrsw%3D%3D (Pubitemid 15005979)
98. GV Smith G Alon SR Roys RP Gullapalli 2003 Functional MRI determination of a dose-response relationship to lower extremity neuromuscular electrical stimulation in healthy subjects Exp Brain Res 150 33 39 12698214 (Pubitemid 36543141)
99. D St Pierre AW Taylor M Lavoie W Sellers YM Kots 1986 Effects of 2,500 Hz sinusoidal current on fibre area and strength of the quadriceps femoris J Sports Med Phys Fitness 26 60 66 2940419 1:STN:280:DyaL283ivFSguw%3D%3D (Pubitemid 16080361)
100. RB Stein DG Everaert AK Thompson SL Chong M Whittaker J Robertson G Kuether 2010 Long-term therapeutic and orthotic effects of a foot drop stimulator on walking performance in progressive and nonprogressive neurological disorders Neurorehabil Neural Repair 24 152 167 19846759
101. JE Stevens RL Mizner L Snyder-Mackler 2004 Neuromuscular electrical stimulation for quadriceps muscle strengthening after bilateral total knee arthroplasty: a case series J Orthop Sports Phys Ther 34 21 29 14964588 (Pubitemid 38155645)
102. SW Stevenson GA Dudley 2001 Dietary creatine supplementation and muscular adaptation to resistive overload Med Sci Sports Exerc 33 1304 1310 11474331 1:CAS:528:DC%2BD3MXmsF2gtrg%3D (Pubitemid 32729846)
103. T Tamaki S Uchiyama Y Uchiyama A Akatsuka S Yoshimura RR Roy VR Edgerton 2000 Limited myogenic response to a single bout of weight-lifting exercise in old rats Am J Physiol Cell Physiol 278 C1143 C1152 10837342 1:CAS:528: DC%2BD3cXks1KnsLc%3D (Pubitemid 30432398)
104. W Taube N Kullmann C Leukel O Kurz F Amtage A Gollhofer 2007 Differential reflex adaptations following sensorimotor and strength training in young elite athletes Int J Sports Med 28 999 1005 17497570 1:STN:280:DC%2BD2snptVyisg%3D%3D (Pubitemid 350273332)
105. J Taylor 2009 The interpolated twitch does provide a valid measure of the voluntary activation of muscle J Appl Physiol 107 354 358 18801954
106. R Theriault MR Boulay G Theriault JA Simoneau 1996 Electrical stimulation-induced changes in performance and fiber type proportion of human knee extensor muscles Eur J Appl Physiol Occup Physiol 74 311 317 8911822 1:STN:280:DyaK2s%2FmvVGlsA%3D%3D (Pubitemid 26345825)
107. A Thorstensson B Hulten W von Dobeln J Karlsson 1976 Effect of strength training on enzyme activities and fibre characteristics in human skeletal muscle Acta Physiol Scand 96 392 398 179278 1:CAS:528:DyaE28XhtVehtrs%3D
108. Trimble MH, Enoka RM (1991) Mechanisms underlying the training effects associated with neuromuscular electrical stimulation. Phys Ther 71:273-280; discussion 280-282
109. M Vanderthommen S Duteil C Wary JS Raynaud A Leroy-Willig JM Crielaard PG Carlier 2003 A comparison of voluntary and electrically induced contractions by interleaved 1H- and 31P-NMRS in humans J Appl Physiol 94 1012 1024 12571132 1:STN:280:DC%2BD3s%2FmtV2msA%3D%3D (Pubitemid 36232017)
110. M Voigt F Chelli C Frigo 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 78 522 532 9840407 1:STN:280:DyaK1M%2FlsVWnsA%3D%3D (Pubitemid 28502472)
111. JR Wolpaw 2007 Spinal cord plasticity in acquisition and maintenance of motor skills Acta Physiol (Oxf) 189 155 169 1:CAS:528:DC%2BD2sXksFSqtLw%3D (Pubitemid 46148326)
112. PE Zehr 2002 Considerations for use of the Hoffmann reflex in exercise studies Eur J Appl Physiol 86 455 468 11944092
113. S Zhou 2000 Chronic neural adaptations to unilateral exercise: mechanisms of cross education Exerc Sport Sci Rev 28 177 184 11064852 1:STN:280: DC%2BD3crhtFahsA%3D%3D