Advertisement

European Journal of Applied Physiology

, Volume 111, Issue 10, pp 2489–2500 | Cite as

Electrical stimulation for testing neuromuscular function: from sport to pathology

  • Guillaume Y. MilletEmail author
  • Vincent Martin
  • Alain Martin
  • Samuel Vergès
Mini Review

Abstract

The use of electrical stimulation (ES) can contribute to our knowledge of how our neuromuscular system can adapt to physical stress or unloading. Although it has been recently challenged, the standard technique used to explore central modifications is the twitch interpolated method which consists in superimposing single twitches or high-frequency doublets on a maximal voluntary contraction (MVC) and to compare the superimposed response to the potentiated response obtained from the relaxed muscle. Alternative methods consist in (1) superimposing a train of stimuli (central activation ratio), (2) comparing the MVC response to the force evoked by a high-frequency tetanus or (3) examining the change in maximal EMG response during voluntary contractions, if this variable is normalized to the maximal M wave, i.e. EMG response to a single stimulus. ES is less used to examine supraspinal factors but it is useful for investigating changes at the spinal level, either by using H reflexes, F waves or cervicomedullary motor-evoked potentials. Peripheral changes can be examined with ES, usually by stimulating the muscle in the relaxed state. Neuromuscular propagation of action potentials on the sarcolemma (M wave, high-frequency fatigue), excitation–contraction coupling (e.g. low-frequency fatigue) and intrinsic force (high-frequency stimulation at supramaximal intensity) can all be used to non-invasively explore muscular function with ES. As for all indirect methods, there are limitations and these are discussed in this review. Finally, (1) ES as a method to measure respiratory muscle function and (2) the comparison between electrical and magnetic stimulation will also be considered.

Keywords

Evoked force M wave Voluntary activation Reflexes Magnetic stimulation Respiratory muscles 

References

  1. Aagaard P, Andersen JL, Dyhre-Poulsen P, Leffers AM, Wagner A, Magnusson SP, Halkjaer-Kristensen J, Simonsen EB (2001) A mechanism for increased contractile strength of human pennate muscle in response to strength training: changes in muscle architecture. J Physiol 534:613–623PubMedCrossRefGoogle Scholar
  2. 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 92:2309–2318PubMedGoogle Scholar
  3. Allen GM, Gandevia SC, Neering IR, Hickie I, Jones R, Middleton J (1994) Muscle performance, voluntary activation and perceived effort in normal subjects and patients with prior poliomyelitis. Brain 117(Pt 4):661–670PubMedCrossRefGoogle Scholar
  4. Allen GM, Gandevia SC, McKenzie DK (1995) Reliability of measurements of muscle strength and voluntary activation using twitch interpolation. Muscle Nerve 18:593–600PubMedCrossRefGoogle Scholar
  5. Amann M, Dempsey JA (2008) Locomotor muscle fatigue modifies central motor drive in healthy humans and imposes a limitation to exercise performance. J Physiol 586:161–173PubMedCrossRefGoogle Scholar
  6. Aubier M, Farkas G, De Troyer A, Mozes R, Roussos C (1981) Detection of diaphragmatic fatigue in man by phrenic stimulation. J Appl Physiol 50:538–544PubMedGoogle Scholar
  7. Awiszus F, Wahl B, Meinecke I (1997) Influence of stimulus cross talk on results of the twitch-interpolation technique at the biceps brachii muscle. Muscle Nerve 20:1187–1190PubMedCrossRefGoogle Scholar
  8. Babault N, Pousson M, Ballay Y, Van Hoecke J (2001) Activation of human quadriceps femoris during isometric, concentric, and eccentric contractions. J Appl Physiol 91:2628–2634PubMedGoogle Scholar
  9. Baudry S, Klass M, Pasquet B, Duchateau J (2007) Age-related fatigability of the ankle dorsiflexor muscles during concentric and eccentric contractions. Eur J Appl Physiol 100:515–525PubMedCrossRefGoogle Scholar
  10. Behm DG, St-Pierre DM, Perez D (1996) Muscle inactivation: assessment of interpolated twitch technique. J Appl Physiol 81:2267–2273PubMedGoogle Scholar
  11. Behm DG, Power K, Drinkwater E (2001) Comparison of interpolation and central activation ratios as measures of muscle inactivation. Muscle Nerve 24:925–934PubMedCrossRefGoogle Scholar
  12. Bellemare F, Bigland-Ritchie B (1987) Central components of diaphragmatic fatigue assessed by phrenic nerve stimulation. J Appl Physiol 62:1307–1316PubMedGoogle Scholar
  13. Bigland-Ritchie B (1981) EMG and fatigue of human voluntary and stimulated contractions. Ciba Found Symp 82:130–156PubMedGoogle Scholar
  14. Bigland-Ritchie B, Jones DA, Hosking GP, Edwards RH (1978) Central and peripheral fatigue in sustained maximum voluntary contractions of human quadriceps muscle. Clin Sci Mol Med 54:609–614PubMedGoogle Scholar
  15. Binder-Macleod SA, McDermond LR (1992) Changes in the force-frequency relationship of the human quadriceps femoris muscle following electrically and voluntarily induced fatigue. Phys Ther 72:95–104PubMedGoogle Scholar
  16. Bruton JD, Place N, Yamada T, Silva JP, Andrade FH, Dahlstedt AJ, Zhang SJ, Katz A, Larsson NG, Westerblad H (2008) Reactive oxygen species and fatigue-induced prolonged low-frequency force depression in skeletal muscle fibres of rats, mice and SOD2 overexpressing mice. J Physiol 586:175–184PubMedCrossRefGoogle Scholar
  17. Burke D (2002) Effects of activity on axonal excitability: implications for motor control studies. Adv Exp Med Biol 508:33–37PubMedCrossRefGoogle Scholar
  18. Chen R, Kayser B, Yan S, Macklem PT (2000) Twitch transdiaphragmatic pressure depends critically on thoracoabdominal configuration. J Appl Physiol 88:54–60PubMedGoogle Scholar
  19. Corona BT, Balog EM, Doyle JA, Rupp JC, Luke RC, Ingalls CP (2010) Junctophilin damage contributes to early strength deficits and EC coupling failure after eccentric contractions. Am J Physiol 298:C365–C376CrossRefGoogle Scholar
  20. Cupido CM, Galea V, McComas AJ (1996) Potentiation and depression of the M wave in human biceps brachii. J Physiol 491(Pt 2):541–550PubMedGoogle Scholar
  21. Darques JL, Bendahan D, Roussel M, Giannesini B, Tagliarini F, Le Fur Y, Cozzone PJ, Jammes Y (2003) Combined in situ analysis of metabolic and myoelectrical changes associated with electrically induced fatigue. J Appl Physiol 95:1476–1484PubMedGoogle Scholar
  22. de Haan A, Gerrits KH, de Ruiter CJ (2009) Counterpoint: the interpolated twitch does not provide a valid measure of the voluntary activation of muscle. J Appl Physiol 107:355–357 (discussion 357–358)PubMedCrossRefGoogle Scholar
  23. de Ruiter CJ, Kooistra RD, Paalman MI, de Haan A (2004) Initial phase of maximal voluntary and electrically stimulated knee extension torque development at different knee angles. J Appl Physiol 97:1693–1701PubMedCrossRefGoogle Scholar
  24. Dean JC, Yates LM, Collins DF (2007) Turning on the central contribution to contractions evoked by neuromuscular electrical stimulation. J Appl Physiol 103:170–176PubMedCrossRefGoogle Scholar
  25. Decorte N, Lafaix PA, Millet GY, Wuyam B, Verges S (in press) Central and peripheral fatigue kinetics during exhaustive constant-load cycling. Scandinavian journal of medicine & science in sportsGoogle Scholar
  26. Del Balso C, Cafarelli E (2007) Adaptations in the activation of human skeletal muscle induced by short-term isometric resistance training. J Appl Physiol 103:402–411PubMedCrossRefGoogle Scholar
  27. Dimitrova NA, Dimitrov GV (2002) Amplitude-related characteristics of motor unit and M wave potentials during fatigue.A simulation study using literature data on intracellular potential changes found in vitro. J Electromyogr Kinesiol 12:339–349PubMedCrossRefGoogle Scholar
  28. Dionne A, Parkes A, Engler B, Watson BV, Nicolle MW (2009) Determination of the best electrode position for recording of the diaphragm compound muscle action potential. Muscle Nerve 40:37–41PubMedCrossRefGoogle Scholar
  29. Duchateau J (2009) Stimulation conditions can improve the validity of the interpolated twitch technique. J Appl Physiol 107:361 (discussion 367–368)PubMedGoogle Scholar
  30. Duchateau J, Hainaut K (1984) Isometric or dynamic training: differential effects on mechanical properties of a human muscle. J Appl Physiol 56:296–301PubMedGoogle Scholar
  31. Duchateau J, Semmler JG, Enoka RM (2006) Training adaptations in the behavior of human motor units. J Appl Physiol 101:1766–1775PubMedCrossRefGoogle Scholar
  32. Edwards RH, Hill DK, Jones DA, Merton PA (1977) Fatigue of long duration in human skeletal muscle after exercise. J Physiol 272:769–778PubMedGoogle Scholar
  33. Gandevia SC (1998) Neural control in human muscle fatigue: changes in muscle afferents, motoneurones and motor cortical drive [corrected]. Acta Physiol Scand 162:275–283PubMedCrossRefGoogle Scholar
  34. Gandevia SC (2001) Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81:1725–1789PubMedGoogle Scholar
  35. Gandevia SC, McKenzie DK, Plassman BL (1990) Activation of human respiratory muscles during different voluntary manoeuvres. J Physiol 428:387–403PubMedGoogle Scholar
  36. Gandevia SC, Allen GM, Butler JE, Taylor JL (1996) Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex. J Physiol 490(Pt 2):529–536PubMedGoogle Scholar
  37. Gandevia SC, Herbert RD, Leeper JB (1998) Voluntary activation of human elbow flexor muscles during maximal concentric contractions. J Physiol 15(Pt 2):595–602CrossRefGoogle Scholar
  38. Gandevia SC, Petersen N, Butler JE, Taylor JL (1999) Impaired response of human motoneurones to corticospinal stimulation after voluntary exercise. J Physiol 521(Pt 3):749–759PubMedCrossRefGoogle Scholar
  39. Garland SJ, McComas AJ (1990) Reflex inhibition of human soleus muscle during fatigue. J Physiol 429:17–27PubMedGoogle Scholar
  40. Goodall S, Romer LM, Ross EZ (2009) Voluntary activation of human knee extensors measured using transcranial magnetic stimulation. Exp Physiol 94:995–1004PubMedCrossRefGoogle Scholar
  41. Harridge SD, Magnusson G, Gordon A (1996) Skeletal muscle contractile characteristics and fatigue resistance in patients with chronic heart failure. Eur Heart J 17:896–901PubMedGoogle Scholar
  42. Hill CA, Thompson MW, Ruell PA, Thom JM, White MJ (2001) Sarcoplasmic reticulum function and muscle contractile character following fatiguing exercise in humans. J Physiol 531:871–878PubMedCrossRefGoogle Scholar
  43. Horstman AM, Beltman MJ, Gerrits KH, Koppe P, Janssen TW, Elich P, de Haan A (2008) Intrinsic muscle strength and voluntary activation of both lower limbs and functional performance after stroke. Clin Physiol Funct Imaging 28:251–261PubMedCrossRefGoogle Scholar
  44. Hubmayr RD, Litchy WJ, Gay PC, Nelson SB (1989) Transdiaphragmatic twitch pressure. Effects of lung volume and chest wall shape. Am Rev Respir Dis 139:647–652PubMedGoogle Scholar
  45. Hultman E, Sjoholm H, Jaderholm-Ek I, Krynicki J (1983) Evaluation of methods for electrical stimulation of human skeletal muscle in situ. Pflugers Arch 398:139–141PubMedCrossRefGoogle Scholar
  46. Johnson BD, Babcock MA, Suman OE, Dempsey JA (1993) Exercise-induced diaphragmatic fatigue in healthy humans. J Physiol 460:385–405PubMedGoogle Scholar
  47. Jones DA (1996) High-and low-frequency fatigue revisited. Acta Physiol Scand 156:265–270PubMedCrossRefGoogle Scholar
  48. Kremenic IJ, Ben-Avi SS, Leonhardt D, McHugh MP (2004) Transcutaneous magnetic stimulation of the quadriceps via the femoral nerve. Muscle Nerve 30:379–381PubMedCrossRefGoogle Scholar
  49. Krishnan C, Allen EJ, Williams GN (2009) Torque-based triggering improves stimulus timing precision in activation tests. Muscle Nerve 40:130–133PubMedCrossRefGoogle Scholar
  50. Kufel TJ, Pineda LA, Mador MJ (2002) Comparison of potentiated and unpotentiated twitches as an index of muscle fatigue. Muscle Nerve 25:438–444PubMedCrossRefGoogle Scholar
  51. Kyroussis D, Mills GH, Polkey MI, Hamnegard CH, Koulouris N, Green M, Moxham J (1996) Abdominal muscle fatigue after maximal ventilation in humans. J Appl Physiol 81:1477–1483PubMedGoogle Scholar
  52. Kyroussis D, Polkey MI, Mills GH, Hughes PD, Moxham J, Green M (1997) Simulation of cough in man by magnetic stimulation of the thoracic nerve roots. Am J Respir Crit Care Med 156:1696–1699PubMedGoogle Scholar
  53. Laghi F (2009) Advancing femoral nerve stimulation into the stage of science. J Appl Physiol 106:356–357PubMedCrossRefGoogle Scholar
  54. Laghi F, Harrison MJ, Tobin MJ (1996) Comparison of magnetic and electrical phrenic nerve stimulation in assessment of diaphragmatic contractility. J Appl Physiol 80:1731–1742PubMedCrossRefGoogle Scholar
  55. Lepers R, Maffiuletti NA, Rochette L, Brugniaux J, Millet GY (2002) Neuromuscular fatigue during a long-duration cycling exercise. J Appl Physiol 92:1487–1493PubMedGoogle Scholar
  56. Lim J, Gorman RB, Saboisky JP, Gandevia SC, Butler JE (2007) Optimal electrode placement for noninvasive electrical stimulation of human abdominal muscles. J Appl Physiol 102:1612–1617PubMedCrossRefGoogle Scholar
  57. Linder SH (1993) Functional electrical stimulation to enhance cough in quadriplegia. Chest 103:166–169PubMedCrossRefGoogle Scholar
  58. Mador MJ, Magalang UJ, Kufel TJ (1994) Twitch potentiation following voluntary diaphragmatic contraction. Am J Respir Crit Care Med 149:739–743PubMedGoogle Scholar
  59. Mador MJ, Rodis A, Magalang UJ, Ameen K (1996) Comparison of cervical magnetic and transcutaneous phrenic nerve stimulation before and after threshold loading. Am J Respir Crit Care Med 154:448–453PubMedGoogle Scholar
  60. Martin A, Carpentier A, Guissard N, van Hoecke J, Duchateau J (1999) Effect of time of day on force variation in a human muscle. Muscle Nerve 22:1380–1387PubMedCrossRefGoogle Scholar
  61. Martin V, Millet GY, Lattier G, Perrod L (2004a) Effects of recovery modes after knee extensor muscles eccentric contractions. Med Sci Sports Exerc 36:1907–1915PubMedCrossRefGoogle Scholar
  62. Martin V, Millet GY, Martin A, Deley G, Lattier G (2004b) Assessment of low-frequency fatigue with two methods of electrical stimulation. J Appl Physiol 97:1923–1929PubMedCrossRefGoogle Scholar
  63. Martin V, Millet GY, Lattier G, Perrod L (2005) Why does knee extensor muscles torque decrease after eccentric-type exercise? J Sports Med Phys Fitness 45:143–151PubMedGoogle Scholar
  64. Martin V, Kerhervé H, Messonnier LA, Banfi JC, Geyssant A, Bonnefoy R, Féasson L, Millet GY (2010) Central and peripheral contributions to neuromuscular fatigue induced by a 24-h treadmill run. J Appl Physiol 108:1224–1233PubMedCrossRefGoogle Scholar
  65. Merton PA (1954) Voluntary strength and fatigue. J Physiol 123:553–564PubMedGoogle Scholar
  66. Merton PA, Morton HB (1980) Stimulation of the cerebral cortex in the intact human subject. Nature 285:227PubMedCrossRefGoogle Scholar
  67. Mettler JA, Griffin L (2010) What are the stimulation parameters that affect the extent of twitch force potentiation in the adductor pollicis muscle? Eur J Appl Physiol 110:1235–1242PubMedCrossRefGoogle Scholar
  68. Metzger JM, Fitts RH (1987) Fatigue from high- and low-frequency muscle stimulation: contractile and biochemical alterations. J Appl Physiol 62:2075–2082PubMedGoogle Scholar
  69. Mier A, Brophy C, Estenne M, Moxham J, Green M, De Troyer A (1985) Action of abdominal muscles on rib cage in humans. J Appl Physiol 58:1438–1443PubMedGoogle Scholar
  70. Mier A, Brophy C, Moxham J, Green M (1990) Influence of lung volume and rib cage configuration on transdiaphragmatic pressure during phrenic nerve stimulation in man. Respir Physiol 80:193–202PubMedCrossRefGoogle Scholar
  71. Mier-Jedrzejowicz A, Brophy C, Moxham J, Green M (1988) Assessment of diaphragm weakness. Am Rev Respir Dis 137:877–883PubMedGoogle Scholar
  72. Millet GY, Lepers R (2004) Alterations of neuromuscular function after prolonged running, cycling and skiing exercises. Sports Med 34:105–116PubMedCrossRefGoogle Scholar
  73. Millet GY, Lepers R, Maffiuletti NA, Babault N, Martin V, Lattier G (2002) Alterations of neuromuscular function after an ultramarathon. J Appl Physiol 92:486–492PubMedGoogle Scholar
  74. Millet GY, Martin V, Lattier G, Ballay Y (2003a) Mechanisms contributing to knee extensor strength loss after prolonged running exercise. J Appl Physiol 94:193–198PubMedGoogle Scholar
  75. Millet GY, Martin V, Maffiuletti NA, Martin A (2003b) Neuromuscular fatigue after a ski skating marathon. Can J Appl Physiol 28:434–445PubMedCrossRefGoogle Scholar
  76. Millet GY, Tomazin K, Verges S, Vincent C, Bonnefoy R, Boisson RC, Gergele L, Bonnefoy R, Féasson L, Martin V (2011) Neuromuscular consequences of an extreme mountain ultra-marathon. PLoS ONE 6:e17059PubMedCrossRefGoogle Scholar
  77. O’Brien TD, Reeves ND, Baltzopoulos V, Jones DA, Maganaris CN (2008) Assessment of voluntary muscle activation using magnetic stimulation. Eur J Appl Physiol 104:49–55PubMedCrossRefGoogle Scholar
  78. Orizio C, Gobbo M, Diemont B (2004) Changes of the force-frequency relationship in human tibialis anterior at fatigue. J Electromyogr Kinesiol 14:523–530PubMedCrossRefGoogle Scholar
  79. Pensini M, Martin A (2004) Effect of voluntary contraction intensity on the H-reflex and V wave responses. Neurosci Lett 367:369–374PubMedCrossRefGoogle Scholar
  80. Petersen NT, Taylor JL, Gandevia SC (2002) The effect of electrical stimulation of the corticospinal tract on motor units of the human biceps brachii. J Physiol 544:277–284PubMedCrossRefGoogle Scholar
  81. Place N, Lepers R, Deley G, Millet GY (2004) Time course of neuromuscular alterations during a prolonged running exercise. Med Sci Sports Exerc 36:1347–1356PubMedCrossRefGoogle Scholar
  82. Place N, Maffiuletti NA, Martin A, Lepers R (2007) Assessment of the reliability of central and peripheral fatigue after sustained maximal voluntary contraction of the quadriceps muscle. Muscle Nerve 35:486–495PubMedCrossRefGoogle Scholar
  83. Place N, Casartelli N, Glatthorn JF, Maffiuletti NA (2010) Comparison of quadriceps inactivation between nerve and muscle stimulation. Muscle Nerve 42:894–900PubMedCrossRefGoogle Scholar
  84. Polkey MI, Kyroussis D, Hamnegard CH, Mills GH, Green M, Moxham J (1996) Quadriceps strength and fatigue assessed by magnetic stimulation of the femoral nerve in man. Muscle Nerve 19:549–555PubMedCrossRefGoogle Scholar
  85. Racinais S, Girard O, Micallef JP, Perrey S (2007) Failed excitability of spinal motoneurons induced by prolonged running exercise. J Neurophysiol 97:596–603PubMedCrossRefGoogle Scholar
  86. Rankin LL, Enoka RM, Volz KA, Stuart DG (1988) Coexistence of twitch potentiation and tetanic force decline in rat hindlimb muscle. J Appl Physiol 65:2687–2695PubMedGoogle Scholar
  87. Rassier DE, Macintosh BR (2000) Coexistence of potentiation and fatigue in skeletal muscle. Braz J Med Biol Res 33:499–508PubMedCrossRefGoogle Scholar
  88. Rothwell JC (1991) Physiological studies of electric and magnetic stimulation of the human brain. Electroencephalogr Clin Neurophysiol 43:29–35Google Scholar
  89. Rothwell JC, Thompson PD, Day BL, Boyd S, Marsden CD (1991) Stimulation of the human motor cortex through the scalp. Exp Physiol 76:159–200PubMedGoogle Scholar
  90. Rutherford OM, Jones DA, Newham DJ (1986) Clinical and experimental application of the percutaneous twitch superimposition technique for the study of human muscle activation. J Neurol Neurosurg Psychiatry 49:1288–1291PubMedCrossRefGoogle Scholar
  91. Sale DG (1988) Neural adaptation to resistance training. Med Sci Sports Exerc 20:S135–S145PubMedCrossRefGoogle Scholar
  92. Schillings ML, Kalkman JS, Janssen HM, van Engelen BG, Bleijenberg G, Zwarts MJ (2007) Experienced and physiological fatigue in neuromuscular disorders. Clin Neurophysiol 118:292–300PubMedCrossRefGoogle Scholar
  93. Seynnes OR, Maffiuletti NA, Horstman AM, Narici MV (2011) Increased H-reflex excitability is not accompanied by changes in neural drive following 24 days of unilateral lower limb suspension. Muscle Nerve 42:749–755Google Scholar
  94. Shehu I, Peli E (2008) Phrenic nerve stimulation. Eur J Anaesthesiol Suppl 42:186–191PubMedCrossRefGoogle Scholar
  95. Sidhu SK, Bentley DJ, Carroll TJ (2009a) Cortical voluntary activation of the human knee extensors can be reliably estimated using transcranial magnetic stimulation. Muscle Nerve 39:186–196PubMedCrossRefGoogle Scholar
  96. Sidhu SK, Bentley DJ, Carroll TJ (2009b) Locomotor exercise induces long-lasting impairments in the capacity of the human motor cortex to voluntarily activate knee extensor muscles. J Appl Physiol 106:556–565PubMedCrossRefGoogle Scholar
  97. Sieck GC, Mantilla CB (2009) Novel method for physiological recruitment of diaphragm motor units after upper cervical spinal cord injury. J Appl Physiol 107:641–642PubMedCrossRefGoogle Scholar
  98. Similowski T, Yan S, Gauthier AP, Macklem PT, Bellemare F (1991) Contractile properties of the human diaphragm during chronic hyperinflation. N Engl J Med 325:917–923PubMedCrossRefGoogle Scholar
  99. Strojnik V, Komi PV (1998) Neuromuscular fatigue after maximal stretch-shortening cycle exercise. J Appl Physiol 84:344–350PubMedGoogle Scholar
  100. Suzuki J, Tanaka R, Yan S, Chen R, Macklem PT, Kayser B (1999) Assessment of abdominal muscle contractility, strength, and fatigue. Am J Respir Crit Care Med 159:1052–1060PubMedGoogle Scholar
  101. Swallow EB, Gosker HR, Ward KA, Moore AJ, Dayer MJ, Hopkinson NS, Schols AM, Moxham J, Polkey MI (2007) A novel technique for nonvolitional assessment of quadriceps muscle endurance in humans. J Appl Physiol 103:739–746PubMedCrossRefGoogle Scholar
  102. Taylor JL (2007) Magnetic muscle stimulation produces fatigue without effort. J Appl Physiol 103:733–734PubMedCrossRefGoogle Scholar
  103. Taylor JL (2009) Point: the interpolated twitch does/does not provide a valid measure of the voluntary activation of muscle. J Appl Physiol 107:354–355PubMedCrossRefGoogle Scholar
  104. Taylor JL, Gandevia SC (2001) Transcranial magnetic stimulation and human muscle fatigue. Muscle Nerve 24:18–29PubMedCrossRefGoogle Scholar
  105. Todd G, Taylor JL, Gandevia SC (2003) Measurement of voluntary activation of fresh and fatigued human muscles using transcranial magnetic stimulation. J Physiol 551:661–671PubMedCrossRefGoogle Scholar
  106. Todd G, Gorman RB, Gandevia SC (2004) Measurement and reproducibility of strength and voluntary activation of lower-limb muscles. Muscle Nerve 29:834–842PubMedCrossRefGoogle Scholar
  107. Tomazin K, Verges S, Decorte N, Oulerich A, Millet GY (2010) Effects of coil characteristics for femoral nerve magnetic stimulation. Muscle Nerve 41:406–409PubMedCrossRefGoogle Scholar
  108. Tomazin K, Verges S, Decorte N, Oulerich A, Maffiuletti NA, Millet GY (2011) Fat tissue alters quadriceps response to femoral nerve magnetic stimulation. Clin Neurophysiol 122:842–847PubMedCrossRefGoogle Scholar
  109. Upton ARM, McComas AJ, Sica REP (1971) Potentiation of “late” responses evoked in muscles during effor. J Neurol Neurosurg Psychiatry 34:699–711PubMedCrossRefGoogle Scholar
  110. Vagg R, Mogyoros I, Kiernan MC, Burke D (1998) Activity-dependent hyperpolarization of human motor axons produced by natural activity. J Physiol 507(Pt 3):919–925PubMedCrossRefGoogle Scholar
  111. Vallier JM, Gruet M, Mely L, Pensini M, Brisswalter J (2011) Neuromuscular fatigue after maximal exercise in patients with cystic fibrosis. J Electromyogr Kinesiol (in press) Google Scholar
  112. Van Cutsem M, Duchateau J, Hainaut K (1998) Changes in single motor unit behaviour contribute to the increase in contraction speed after dynamic training in humans. J Physiol 513(Pt 1):295–305PubMedCrossRefGoogle Scholar
  113. Verges S, Maffiuletti NA, Kerherve H, Decorte N, Wuyam B, Millet GY (2009) Comparison of electrical and magnetic stimulations to assess quadriceps muscle function. J Appl Physiol 106:701–710PubMedCrossRefGoogle Scholar
  114. Westerblad H, Duty S, Allen DG (1993) Intracellular calcium concentration during low-frequency fatigue in isolated single fibers of mouse skeletal muscle. J Appl Physiol 75:382–388PubMedGoogle Scholar
  115. Wragg S, Aquilina R, Moran J, Ridding M, Hamnegard C, Fearn T, Green M, Moxham J (1994) Comparison of cervical magnetic stimulation and bilateral percutaneous electrical stimulation of the phrenic nerves in normal subjects. Eur Respir J 7:1788–1792PubMedCrossRefGoogle Scholar
  116. Yue GH, Ranganathan VK, Siemionow V, Liu JZ, Sahgal V (1999) Older adults exhibit a reduced ability to fully activate their biceps brachii muscle. J Gerontol 54:M249–M253Google Scholar
  117. Zehr PE (2002) Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86:455–468PubMedCrossRefGoogle Scholar
  118. Zierath JR, Hawley JA (2004) Skeletal muscle fiber type: influence on contractile and metabolic properties. PLoS Biol 2:e348PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Guillaume Y. Millet
    • 1
    • 2
    • 3
    Email author
  • Vincent Martin
    • 4
  • Alain Martin
    • 5
  • Samuel Vergès
    • 2
    • 6
  1. 1.Université de LyonSaint-EtienneFrance
  2. 2.Inserm U1042GrenobleFrance
  3. 3.Exercise Physiology LaboratoryBâtiment Médecine du Sport, Myologie, Hôpital BellevueSaint-Etienne Cedex 2France
  4. 4.Clermont Université, Blaise Pascal University, EA 3533, Laboratory of Biology of Physical ActivityClermont-FerrandFrance
  5. 5.INSERM U887 LaboratoryUniversity of BurgundyDijonFrance
  6. 6.HP2 Laboratory, Joseph Fourier University and Exercise Research Unit, University HospitalGrenobleFrance

Personalised recommendations