European Journal of Applied Physiology

, Volume 118, Issue 3, pp 501–521 | Cite as

Determinants, analysis and interpretation of the muscle compound action potential (M wave) in humans: implications for the study of muscle fatigue

Invited Review

Abstract

The compound muscle action potential (M wave) has been commonly used to assess the peripheral properties of the neuromuscular system. More specifically, changes in the M-wave features are used to examine alterations in neuromuscular propagation that can occur during fatiguing contractions. The utility of the M wave is based on the assumption that impaired neuromuscular propagation results in a decrease in M-wave size. However, there remains controversy on whether the size of the M wave is increased or decreased during and/or after high-intensity exercise. The controversy partly arises from the fact that previous authors have considered the M wave as a whole, i.e., without analyzing separately its first and second phases. However, in a series of studies we have demonstrated that the first and second phases of the M wave behave in a different manner during and after fatiguing contractions. The present review is aimed at five main objectives: (1) to describe the mechanistic factors that determine the M-wave shape; (2) to analyze the various factors influencing M-wave properties; (3) to emphasize the need to analyze separately the first and second M-wave phases to adequately identify and interpret changes in muscle fiber membrane properties; (4) to advance the hypothesis that it is an increase (and not a decrease) of the M-wave first phase which reflects impaired sarcolemmal membrane excitability; and (5) to revisit the involvement of impaired sarcolemmal membrane excitability in the reduction of the force generating capacity.

Keywords

Compound muscle action potential End-of-fiber signals Sarcolemmal membrane excitability Conduction velocity Quadriceps Surface electromyography Transcutaneous electrical stimulation 

Abbreviations

AmpliFIRST

Amplitude of the first phase of the M wave

AmpliSECOND

Amplitude of the second phase of the M wave

AreaFIRST

Area of the first phase of the M wave

AreaSECOND

Area of the second phase of the M wave

DurFIRST

Duration of the first phase of the M wave

DurSECOND

Duration of the second phase of the M wave

EMG

Electromyographic

MUAP

Motor unit action potential

MVC

Maximal voluntary contraction

N.M.P.

No mechanism proposed

NS

Not significant

SFAP

Single fiber action potential

References

  1. Arabadzhiev TI, Dimitrov GV, Chakarov VE, Dimitrov AG, Dimitrova NA (2008) Effects of changes in intracellular action potential on potentials recorded by single-fiber, macro, and belly-tendon electrodes. Muscle Nerve 37(6):700–712.  https://doi.org/10.1002/mus.21024 PubMedCrossRefGoogle Scholar
  2. Arendt-Nielsen L, Zwarts M (1989) Measurement of muscle fiber conduction velocity in humans: techniques and applications. J Clin Neurophysiol 6(2):173–190PubMedCrossRefGoogle Scholar
  3. Behm DG, St-Pierre DM (1997) Effects of fatigue duration and muscle type on voluntary and evoked contractile properties. J Appl Physiol (1985) 82(5):1654–1661CrossRefGoogle Scholar
  4. Bellemare F, Garzaniti N (1988) Failure of neuromuscular propagation during human maximal voluntary contraction. J Appl Physiol (1985) 64(3):1084–1093CrossRefGoogle Scholar
  5. Bigland-Ritchie B (1981) EMG and fatigue of human voluntary and stimulated contractions. Ciba Found Symp 82:130–156PubMedGoogle Scholar
  6. Bigland-Ritchie B, Kukulka CG, Lippold OC, Woods JJ (1982) The absence of neuromuscular transmission failure in sustained maximal voluntary contractions. J Physiol 330:265–278PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bigland-Ritchie B, Johansson R, Lippold OC, Woods JJ (1983) Contractile speed and EMG changes during fatigue of sustained maximal voluntary contractions. J Neurophysiol 50(1):313–324PubMedCrossRefGoogle Scholar
  8. Bilodeau M, Henderson TK, Nolta BE, Pursley PJ, Sandfort GL (2001) Effect of aging on fatigue characteristics of elbow flexor muscles during sustained submaximal contraction. J Appl Physiol (1985) 91(6):2654–2664CrossRefGoogle Scholar
  9. Bodine SC, Roy RR, Eldred E, Edgerton VR (1987) Maximal force as a function of anatomical features of motor units in the cat tibialis anterior. J Neurophysiol 57(6):1730–1745PubMedCrossRefGoogle Scholar
  10. Botter A, Oprandi G, Lanfranco F, Allasia S, Maffiuletti NA, Minetto MA (2011) Atlas of the muscle motor points for the lower limb: implications for electrical stimulation procedures and electrode positioning. Eur J Appl Physiol 111:2461–2471PubMedCrossRefGoogle Scholar
  11. Burke D (2002) Effects of activity on axonal excitability: implications for motor control studies. Adv Exp Med Biol 508:33–37PubMedCrossRefGoogle Scholar
  12. Chan KM, Andres LP, Polykovskaya Y, Brown WF (1998) Dissociation of the electrical and contractile properties in single human motor units during fatigue. Muscle Nerve 21(12):1786–1789PubMedCrossRefGoogle Scholar
  13. Crone C, Johnsen LL, Hultborn H, Orsnes GB (1999) Amplitude of the maximum motor response (Mmax) in human muscles typically decreases during the course of an experiment. Exp Brain Res 124(2):265–270PubMedCrossRefGoogle Scholar
  14. Cupido CM, Galea V, McComas AJ (1996) Potentiation and depression of the M wave in human biceps brachii. J Physiol 491(Pt 2):541–550PubMedPubMedCentralCrossRefGoogle Scholar
  15. Dalpozzo F, Gerard P, De Pasqua V, Wang F, Maertens de Noordhout A (2002) Single motor axon conduction velocities of human upper and lower limb motor units. A study with transcranial electrical stimulation. Clin Neurophysiol 113(2):284–291PubMedCrossRefGoogle Scholar
  16. 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(5):339–349PubMedCrossRefGoogle Scholar
  17. Dimitrova NA, Dimitrov GV (2003) Interpretation of EMG changes with fatigue: facts, pitfalls, and fallacies. J Electromyogr Kinesiol 13(1):13–36PubMedCrossRefGoogle Scholar
  18. Dimitrova NA, Dimitrov GV (2006) Electromyography (EMG) modeling. In: Hoboken MA (ed) Wiley encyclopedia of biomedical engineering. Wiley, OxfordGoogle Scholar
  19. Dimitrova NA, Dimitrov GV, Dimitrov AG (2001) Calculation of spatially filtered signals produced by a motor unit comprising muscle fibres with non-uniform propagation. Med Biol Eng Comput 39(2):202–207PubMedCrossRefGoogle Scholar
  20. Disselhorst-Klug C, Silny J, Rau G (1997) Improvement of spatial resolution in surface-EMG: a theoretical and experimental comparison of different spatial filters. IEEE Trans Biomed Eng 44(7):567–574.  https://doi.org/10.1109/10.594897 PubMedCrossRefGoogle Scholar
  21. Duchateau J, Hainaut K (1985) Electrical and mechanical failures during sustained and intermittent contractions in humans. J Appl Physiol (1985) 58(3):942–947CrossRefGoogle Scholar
  22. Duchateau J, Balestra C, Carpentier A, Hainaut K (2002) Reflex regulation during sustained and intermittent submaximal contractions in humans. J Physiol 541(Pt 3):959–967PubMedPubMedCentralCrossRefGoogle Scholar
  23. Enoka RM, Stuart DG (1992) Neurobiology of muscle fatigue. J Appl Physiol (1985) 72(5):1631–1648CrossRefGoogle Scholar
  24. Enoka RM, Trayanova N, Laouris Y, Bevan L, Reinking RM, Stuart DG (1992) Fatigue-related changes in motor unit action potentials of adult cats. Muscle Nerve 15(2):138–150.  https://doi.org/10.1002/mus.880150204 PubMedCrossRefGoogle Scholar
  25. Everts ME, Retterstol K, Clausen T (1988) Effects of adrenaline on excitation-induced stimulation of the sodium-potassium pump in rat skeletal muscle. Acta Physiol Scand 134(2):189–198.  https://doi.org/10.1111/j.1748-1716.1988.tb08479.x PubMedCrossRefGoogle Scholar
  26. Farina D, Rainoldi A (1999) Compensation of the effect of sub-cutaneous tissue layers on surface EMG: a simulation study. Med Eng Phys 21(6–7):487–497PubMedCrossRefGoogle Scholar
  27. Farina D, Fosci M, Merletti R (2002a) Motor unit recruitment strategies investigated by surface EMG variables. J Appl Physiol 92(1):235–247PubMedCrossRefGoogle Scholar
  28. Farina D, Merletti R, Indino B, Nazzaro M, Pozzo M (2002b) Surface EMG crosstalk between knee extensor muscles: experimental and model results. Muscle Nerve 26(5):681–695.  https://doi.org/10.1002/mus.10256 PubMedCrossRefGoogle Scholar
  29. Fitch S, McComas A (1985) Influence of human muscle length on fatigue. J Physiol 362:205–213PubMedPubMedCentralCrossRefGoogle Scholar
  30. Fortune E, Lowery MM (2009) Effect of extracellular potassium accumulation on muscle fiber conduction velocity: a simulation study. Ann Biomed Eng 37(10):2105–2117.  https://doi.org/10.1007/s10439-009-9756-4 PubMedCrossRefGoogle Scholar
  31. Fowles JR, Green HJ, Tupling R, O’Brien S, Roy BD (2002) Human neuromuscular fatigue is associated with altered Na+–K+-ATPase activity following isometric exercise. J Appl Physiol (1985) 92(4):1585–1593.  https://doi.org/10.1152/japplphysiol.00668.2001 CrossRefGoogle Scholar
  32. Fuglevand AJ (1995) The role of the sarcolemma action potential in fatigue. Adv Exp Med Biol 384:101–108PubMedCrossRefGoogle Scholar
  33. Fuglevand AJ, Zackowski KM, Huey KA, Enoka RM (1993) Impairment of neuromuscular propagation during human fatiguing contractions at submaximal forces. J Physiol 460:549–572PubMedPubMedCentralCrossRefGoogle Scholar
  34. Garland SJ, Garner SH, McComas AJ (1988) Reduced voluntary electromyographic activity after fatiguing stimulation of human muscle. J Physiol 401:547–556PubMedPubMedCentralCrossRefGoogle Scholar
  35. Gobbo M, Maffiuletti NA, Orizio C, Minetto MA (2014) Muscle motor point identification is essential for optimizing neuromuscular electrical stimulation use. J Neuroeng Rehabil 11:17.  https://doi.org/10.1186/1743-0003-11-17 PubMedPubMedCentralCrossRefGoogle Scholar
  36. Gydikov A, Kosarov D (1972) Volume conduction of the potentials from separate motor units in human muscle. Electromyogr Clin Neurophysiol 12(2):127–147PubMedGoogle Scholar
  37. Hamada T, Sale DG, MacDougall JD, Tarnopolsky MA (2000) Postactivation potentiation, fiber type, and twitch contraction time in human knee extensor muscles. J Appl Physiol (1985) 88(6):2131–2137CrossRefGoogle Scholar
  38. Hanson J (1974) Effects of repetitive stimulation on membrane potentials and twitch in human and rat intercostal muscle fibres. Acta Physiol Scand 92(2):238–248.  https://doi.org/10.1111/j.1748-1716.1974.tb05741.x PubMedCrossRefGoogle Scholar
  39. Harris AJ, Duxson MJ, Butler JE, Hodges PW, Taylor JL, Gandevia SC (2005) Muscle fiber and motor unit behavior in the longest human skeletal muscle. J Neurosci 25(37):8528–8533PubMedCrossRefGoogle Scholar
  40. Hicks A, McComas AJ (1989) Increased sodium pump activity following repetitive stimulation of rat soleus muscles. J Physiol 414:337–349PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hicks A, Fenton J, Garner S, McComas AJ (1989) M wave potentiation during and after muscle activity. J Appl Physiol (1985) 66(6):2606–2610PubMedCrossRefGoogle Scholar
  42. Hodges PW, Pengel LH, Herbert RD, Gandevia SC (2003) Measurement of muscle contraction with ultrasound imaging. Muscle Nerve 27(6):682–692.  https://doi.org/10.1002/mus.10375 PubMedCrossRefGoogle Scholar
  43. Hodgkin AL, Horowicz P (1959) The influence of potassium and chloride ions on the membrane potential of single muscle fibres. J Physiol 148:127–160PubMedPubMedCentralCrossRefGoogle Scholar
  44. Hultman E, Sjoholm H (1983) Electromyogram, force and relaxation time during and after continuous electrical stimulation of human skeletal muscle in situ. J Physiol 339:33–40PubMedPubMedCentralCrossRefGoogle Scholar
  45. Ito K, Hotta Y (2012) EMG-based detection of muscle fatigue during low-level isometric contraction by recurrence quantification analysis and monopolar configuration. Conf Proc IEEE Eng Med Biol Soc 2012:4237–4241.  https://doi.org/10.1109/EMBC.2012.6346902 PubMedGoogle Scholar
  46. Johnson MA, Polgar J, Weightman D, Appleton D (1973) Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. J Neurol Sci 18(1):111–129PubMedCrossRefGoogle Scholar
  47. Jones DA (1981) Muscle fatigue due to changes beyond the neuromuscular junction. In: Whelan RPaJ (ed) Human muscle fatigue: physiological mechanisms. Pitman, London, pp 178–196Google Scholar
  48. Jones DA (1996) High-and low-frequency fatigue revisited. Acta Physiol Scand 156(3):265–270.  https://doi.org/10.1046/j.1365-201X.1996.192000.x PubMedCrossRefGoogle Scholar
  49. 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(1):e56–e62.  https://doi.org/10.1111/j.1600-0838.2009.00897.x PubMedCrossRefGoogle Scholar
  50. Juel C (1988) Muscle action potential propagation velocity changes during activity. Muscle Nerve 11(7):714–719.  https://doi.org/10.1002/mus.880110707 PubMedCrossRefGoogle Scholar
  51. Kanda K, Hashizume K (1992) Factors causing difference in force output among motor units in the rat medial gastrocnemius muscle. J Physiol 448:677–695PubMedPubMedCentralCrossRefGoogle Scholar
  52. Keenan KG, Farina D, Merletti R, Enoka RM (2006) Influence of motor unit properties on the size of the simulated evoked surface EMG potential. Exp Brain Res 169(1):37–49.  https://doi.org/10.1007/s00221-005-0126-7 PubMedCrossRefGoogle Scholar
  53. Knight CA, Kamen G (2005) Superficial motor units are larger than deeper motor units in human vastus lateralis muscle. Muscle Nerve 31(4):475–480.  https://doi.org/10.1002/mus.20265 PubMedCrossRefGoogle Scholar
  54. Kranz H, Williams AM, Cassell J, Caddy DJ, Silberstein RB (1983) Factors determining the frequency content of the electromyogram. J Appl Physiol Respir Environ Exerc Physiol 55(2):392–399PubMedGoogle Scholar
  55. Krnjevic K, Miledi R (1958) Failure of neuromuscular propagation in rats. J Physiol 140(3):440–461PubMedPubMedCentralGoogle Scholar
  56. Kubo K, Kanehisa H, Kawakami Y, Fukunaga T (2001) Influences of repetitive muscle contractions with different modes on tendon elasticity in vivo. J Appl Physiol (1985) 91(1):277–282CrossRefGoogle Scholar
  57. Kuchinad RA, Ivanova TD, Garland SJ (2004) Modulation of motor unit discharge rate and H-reflex amplitude during submaximal fatigue of the human soleus muscle. Exp Brain Res 158(3):345–355.  https://doi.org/10.1007/s00221-004-1907-0 PubMedCrossRefGoogle Scholar
  58. Kukulka CG, Russell AG, Moore MA (1986) Electrical and mechanical changes in human soleus muscle during sustained maximum isometric contractions. Brain Res 362(1):47–54PubMedCrossRefGoogle Scholar
  59. Lange F, Van Weerden TW, Van Der Hoeven JH (2002) A new surface electromyography analysis method to determine spread of muscle fiber conduction velocities. J Appl Physiol (1985) 93(2):759–764.  https://doi.org/10.1152/japplphysiol.00594.2001 CrossRefGoogle Scholar
  60. Lännergren J, Westerblad H (1987) Action potential fatigue in single skeletal muscle fibres of Xenopus. Acta Physiol Scand 129(3):311–318.  https://doi.org/10.1111/j.1748-1716.1987.tb08074.x PubMedCrossRefGoogle Scholar
  61. Lateva ZC, McGill KC (1998) The physiological origin of the slow afterwave in muscle action potentials. Electroencephalogr Clin Neurophysiol 109(5):462–469PubMedCrossRefGoogle Scholar
  62. Lateva ZC, McGill KC, Burgar CG (1996) Anatomical and electrophysiological determinants of the human thenar compound muscle action potential. Muscle Nerve 19 (11):1457–1468.  https://doi.org/10.1002/(SICI)1097-4598(199611)19:11<1457::AID-MUS10>3.0.CO;2-Q PubMedCrossRefGoogle Scholar
  63. Levenez M, Kotzamanidis C, Carpentier A, Duchateau J (2005) Spinal reflexes and coactivation of ankle muscles during a submaximal fatiguing contraction. J Appl Physiol (1985) 99(3):1182–1188.  https://doi.org/10.1152/japplphysiol.00284.2005 CrossRefGoogle Scholar
  64. Lexell J, Henriksson-Larsen K, Sjostrom M (1983) Distribution of different fibre types in human skeletal muscles. 2. A study of cross-sections of whole m. vastus lateralis. Acta Physiol Scand 117(1):115–122.  https://doi.org/10.1111/j.1748-1716.1983.tb07185.x PubMedCrossRefGoogle Scholar
  65. Lieber RL (2009) Skeletal muscle structure, function, and plasticity: the physiological basis of rehabilitation, 3rd edn. edn. Lippincott Williams & Wilkins, BaltimoreGoogle Scholar
  66. Linnamo V, Strojnik V, Komi PV (2001) Electromyogram power spectrum and features of the superimposed maximal M-wave during voluntary isometric actions in humans at different activation levels. Eur J Appl Physiol 86(1):28–33.  https://doi.org/10.1007/s004210100462 PubMedCrossRefGoogle Scholar
  67. Lüttgau HC (1965) The effect of metabolic inhibitors on the fatigue of the action potential in single muscle fibres. J Physiol 178:45–67PubMedCentralCrossRefGoogle Scholar
  68. Mademli L, Arampatzis A (2005) Behaviour of the human gastrocnemius muscle architecture during submaximal isometric fatigue. Eur J Appl Physiol 94(5–6):611–617.  https://doi.org/10.1007/s00421-005-1366-8 PubMedCrossRefGoogle Scholar
  69. Maganaris CN, Baltzopoulos V, Sargeant AJ (2002) Repeated contractions alter the geometry of human skeletal muscle. J Appl Physiol (1985) 93(6):2089–2094.  https://doi.org/10.1152/japplphysiol.00604.2002 CrossRefGoogle Scholar
  70. Marsden CD, Meadows JC, Merton PA (1983) “Muscular wisdom” that minimizes fatigue during prolonged effort in man: peak rates of motoneuron discharge and slowing of discharge during fatigue. Adv Neurol 39:169–211PubMedGoogle Scholar
  71. Masuda T, Miyano H, Sadoyama T (1985) The position of innervation zones in the biceps brachii investigated by surface electromyography. IEEE Trans Biomed Eng 32:36–42PubMedCrossRefGoogle Scholar
  72. Matkowski B, Place N, Martin A, Lepers R (2011) Neuromuscular fatigue differs following unilateral vs bilateral sustained submaximal contractions. Scand J Med Sci Sports 21(2):268–276.  https://doi.org/10.1111/j.1600-0838.2009.01040.x PubMedCrossRefGoogle Scholar
  73. McComas AJ, Galea V, Einhorn RW (1994) Pseudofacilitation: a misleading term. Muscle Nerve 17(6):599–607.  https://doi.org/10.1002/mus.880170606 PubMedCrossRefGoogle Scholar
  74. McGill KC, Lateva ZC, Xiao S (2001) A model of the muscle action potential for describing the leading edge, terminal wave, and slow afterwave. IEEE Trans Biomed Eng 48(12):1357–1365.  https://doi.org/10.1109/10.966595 PubMedCrossRefGoogle Scholar
  75. Merton PA (1954) Voluntary strength and fatigue. J Physiol 123(3):553–564PubMedPubMedCentralCrossRefGoogle Scholar
  76. Metzger JM, Fitts RH (1986) Fatigue from high- and low-frequency muscle stimulation: role of sarcolemma action potentials. Exp Neurol 93(2):320–333PubMedCrossRefGoogle Scholar
  77. Millet GY, Martin V, Martin A, Verges S (2011) Electrical stimulation for testing neuromuscular function: from sport to pathology. Eur J Appl Physiol 111(10):2489–2500.  https://doi.org/10.1007/s00421-011-1996-y PubMedCrossRefGoogle Scholar
  78. Milner-Brown HS, Miller RG (1986) Muscle membrane excitation and impulse propagation velocity are reduced during muscle fatigue. Muscle Nerve 9(4):367–374.  https://doi.org/10.1002/mus.880090415 PubMedCrossRefGoogle Scholar
  79. Moritani T, Muro M, Kijima A (1985) Electromechanical changes during electrically induced and maximal voluntary contractions: electrophysiologic responses of different muscle fiber types during stimulated contractions. Exp Neurol 88(3):471–483PubMedCrossRefGoogle Scholar
  80. Narici MV, Binzoni T, Hiltbrand E, Fasel J, Terrier F, Cerretelli P (1996) In vivo human gastrocnemius architecture with changing joint angle at rest and during graded isometric contraction. J Physiol 496(Pt 1):287–297PubMedPubMedCentralCrossRefGoogle Scholar
  81. Neyroud D, Maffiuletti NA, Kayser B, Place N (2012) Mechanisms of fatigue and task failure induced by sustained submaximal contractions. Med Sci Sports Exerc 44(7):1243–1251.  https://doi.org/10.1249/MSS.0b013e318245cc4d PubMedCrossRefGoogle Scholar
  82. Neyroud D, Ruttimann J, Mannion AF, Millet GY, Maffiuletti NA, Kayser B, Place N (2013) Comparison of neuromuscular adjustments associated with sustained isometric contractions of four different muscle groups. J Appl Physiol (1985) 114(10):1426–1434.  https://doi.org/10.1152/japplphysiol.01539.2012 CrossRefGoogle Scholar
  83. Nielsen OB, Clausen T (2000) The Na+/K(+)-pump protects muscle excitability and contractility during exercise. Exerc Sport Sci Rev 28(4):159–164PubMedGoogle Scholar
  84. Ounjian M, Roy RR, Eldred E, Garfinkel A, Payne JR, Armstrong A, Toga AW, Edgerton VR (1991) Physiological and developmental implications of motor unit anatomy. J Neurobiol 22(5):547–559.  https://doi.org/10.1002/neu.480220510 PubMedCrossRefGoogle Scholar
  85. Overgaard K, Nielsen OB, Flatman JA, Clausen T (1999) Relations between excitability and contractility in rat soleus muscle: role of the Na+–K+ pump and Na+/K+ gradients. J Physiol 518(Pt 1):215–225PubMedPubMedCentralCrossRefGoogle Scholar
  86. Pageaux B, Marcora SM, Lepers R (2013) Prolonged mental exertion does not alter neuromuscular function of the knee extensors. Med Sci Sports Exerc 45(12):2254–2264.  https://doi.org/10.1249/MSS.0b013e31829b504a PubMedCrossRefGoogle Scholar
  87. Pappas GP, Asakawa DS, Delp SL, Zajac FE, Drace JE (2002) Nonuniform shortening in the biceps brachii during elbow flexion. J Appl Physiol 92(6):2381–2389PubMedCrossRefGoogle Scholar
  88. Place N, Maffiuletti NA, Ballay Y, Lepers R (2005) Twitch potentiation is greater after a fatiguing submaximal isometric contraction performed at short vs. long quadriceps muscle length. J Appl Physiol (1985) 98(2):429–436.  https://doi.org/10.1152/japplphysiol.00664.2004 CrossRefGoogle Scholar
  89. Place N, Matkowski B, Martin A, Lepers R (2006) Synergists activation pattern of the quadriceps muscle differs when performing sustained isometric contractions with different EMG biofeedback. Exp Brain Res 174(4):595–603.  https://doi.org/10.1007/s00221-006-0504-9 PubMedCrossRefGoogle Scholar
  90. Place N, Martin A, Ballay Y, Lepers R (2007) Neuromuscular fatigue differs with biofeedback type when performing a submaximal contraction. J Electromyogr Kinesiol 17(3):253–263.  https://doi.org/10.1016/j.jelekin.2006.04.001 PubMedCrossRefGoogle Scholar
  91. Place N, Yamada T, Bruton JD, Westerblad H (2010) Muscle fatigue: from observations in humans to underlying mechanisms studied in intact single muscle fibres. Eur J Appl Physiol 110(1):1–15.  https://doi.org/10.1007/s00421-010-1480-0 PubMedCrossRefGoogle Scholar
  92. Plaskett CJ, Cafarelli E (2001) Caffeine increases endurance and attenuates force sensation during submaximal isometric contractions. J Appl Physiol (1985) 91(4):1535–1544CrossRefGoogle Scholar
  93. Prutchi D (1995) A high-resolution large array (HRLA) surface EMG system. Med Eng Phys 17(6):442–454PubMedCrossRefGoogle Scholar
  94. Radicheva NI, Kolev VB, Peneva NE (1993) Influence of intracellular potential and conduction velocity on extracellular muscle fibre potential. J Electromyogr Kinesiol 3(2):95–102.  https://doi.org/10.1016/1050-6411(93)90004-G PubMedCrossRefGoogle Scholar
  95. Rodriguez-Falces J (2016) The formation of extracellular potentials over the innervation zone: are these potentials affected by changes in fibre membrane properties? Med Biol Eng Comput 54(12):1845–1858.  https://doi.org/10.1007/s11517-016-1487-8 PubMedCrossRefGoogle Scholar
  96. Rodriguez-Falces J, Place N (2014) Effects of muscle fibre shortening on the characteristics of surface motor unit potentials. Med Biol Eng Comput 52(2):95–107.  https://doi.org/10.1007/s11517-013-1112-z PubMedCrossRefGoogle Scholar
  97. Rodriguez-Falces J, Place N (2015) Power spectral changes of the superimposed M wave during isometric voluntary contractions of increasing strength. Muscle Nerve 51(4):580–591.  https://doi.org/10.1002/mus.24418 PubMedCrossRefGoogle Scholar
  98. Rodriguez-Falces J, Place N (2016) Differences in the recruitment curves obtained with monopolar and bipolar electrode configurations in the quadriceps femoris. Muscle Nerve 54(1):118–131.  https://doi.org/10.1002/mus.25006 PubMedCrossRefGoogle Scholar
  99. Rodriguez-Falces J, Place N (2017a) New insights into the potentiation of the first and second phases of the M-wave after voluntary contractions in the quadriceps muscle. Muscle Nerve 55(1):35–45.  https://doi.org/10.1002/mus.25186 PubMedCrossRefGoogle Scholar
  100. Rodriguez-Falces J, Place N (2017b) Muscle excitability during sustained maximal voluntary contractions by a separate analysis of the M-wave phases. Scand J Med Sci Sports. 27(12):1761–1775Google Scholar
  101. Rodriguez-Falces J, Neyroud D, Place N (2015a) Influence of inter-electrode distance, contraction type, and muscle on the relationship between the sEMG power spectrum and contraction force. Eur J Appl Physiol 115(3):627–638.  https://doi.org/10.1007/s00421-014-3041-4 PubMedCrossRefGoogle Scholar
  102. Rodriguez-Falces J, Duchateau J, Muraoka Y, Baudry S (2015b) M-wave potentiation after voluntary contractions of different durations and intensities in the tibialis anterior. J Appl Physiol (1985) 118(8):953–964.  https://doi.org/10.1152/japplphysiol.01144.2014 CrossRefGoogle Scholar
  103. Rodriguez-Falces J, Malanda A, Latasa I, Lavilla-Oiz A, Navallas J (2016) Influence of timing variability between motor unit potentials on M-wave characteristics. J Electromyogr Kinesiol 30:249–262.  https://doi.org/10.1016/j.jelekin.2016.08.003 PubMedCrossRefGoogle Scholar
  104. Roeleveld K, Stegeman DF, Vingerhoets HM, Van Oosterom A (1997a) Motor unit potential contribution to surface electromyography. Acta Physiol Scand 160(2):175–183.  https://doi.org/10.1046/j.1365-201X.1997.00152.x PubMedCrossRefGoogle Scholar
  105. Roeleveld K, Blok JH, Stegeman DF, van Oosterom A (1997b) Volume conduction models for surface EMG; confrontation with measurements. J Electromyogr Kinesiol 7(4):221–232PubMedCrossRefGoogle Scholar
  106. Rozand V, Cattagni T, Theurel J, Martin A, Lepers R (2015) Neuromuscular fatigue following isometric contractions with similar torque time integral. Int J Sports Med 36(1):35–40.  https://doi.org/10.1055/s-0034-1375614 PubMedGoogle Scholar
  107. Rutkove SB (2000) Pseudofacilitation: a temperature-sensitive phenomenon. Muscle Nerve 23(1):115–118PubMedCrossRefGoogle Scholar
  108. Sale DG, McComas AJ, MacDougall JD, Upton AR (1982) Neuromuscular adaptation in human thenar muscles following strength training and immobilization. J Appl Physiol Respir Environ Exerc Physiol 53(2):419–424PubMedGoogle Scholar
  109. Sieck GC, Prakash YS (1995) Fatigue at the neuromuscular junction. Branch point vs. presynaptic vs. postsynaptic mechanisms. Adv Exp Med Biol 384:83–100PubMedCrossRefGoogle Scholar
  110. Solomonow M, Baratta R, Bernardi M, Zhou B, Lu Y, Zhu M, Acierno S (1994) Surface and wire EMG crosstalk in neighbouring muscles. J Electromyogr Kinesiol 4(3):131–142.  https://doi.org/10.1016/1050-6411(94)90014-0 PubMedCrossRefGoogle Scholar
  111. Stalberg E (1966) Propagation velocity in human muscle fibers in situ. Acta Physiol Scand Suppl 287:1–112PubMedGoogle Scholar
  112. Stephens JA, Taylor A (1972) Fatigue of maintained voluntary muscle contraction in man. J Physiol 220(1):1–18PubMedPubMedCentralCrossRefGoogle Scholar
  113. Thesleff S (1959) Motor end-plate ‘desensitization’ by repetitive nerve stimuli. J Physiol 148:659–664PubMedPubMedCentralCrossRefGoogle Scholar
  114. Thomas CK, Woods JJ, Bigland-Ritchie B (1989) Impulse propagation and muscle activation in long maximal voluntary contractions. J Appl Physiol (1985) 67(5):1835–1842CrossRefGoogle Scholar
  115. Tucker KJ, Turker KS (2005) A new method to estimate signal cancellation in the human maximal M-wave. J Neurosci Methods 149(1):31–41.  https://doi.org/10.1016/j.jneumeth.2005.05.010 PubMedCrossRefGoogle Scholar
  116. 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):919–925PubMedPubMedCentralCrossRefGoogle Scholar
  117. van Vugt JP, van Dijk JG (2001) A convenient method to reduce crosstalk in surface EMG. Cobb Award-winning article, 2001. Clin Neurophysiol 112(4):583–592PubMedCrossRefGoogle Scholar
  118. Vyskočil F, Hnik P, Rehfeldt H, Vejsada R, Ujec E (1983) The measurement of K+ e concentration changes in human muscles during volitional contractions. Pflugers Arch 399(3):235–237PubMedCrossRefGoogle Scholar
  119. West W, Hicks A, McKelvie R, O’Brien J (1996) The relationship between plasma potassium, muscle sarcolemmal membrane excitability and force following quadriceps fatigue. Pflugers Arch 432(1):43–49PubMedCrossRefGoogle Scholar
  120. Ye X, Beck TW, Wages NP (2015) Relationship between innervation zone width and mean muscle fiber conduction velocity during a sustained isometric contraction. J Musculoskelet Neuronal Interact 15(1):95–102PubMedPubMedCentralGoogle Scholar
  121. Yu D, Yin H, Han T, Jiang H, Cao X (2016) Intramuscular innervations of lower leg skeletal muscles: applications in their clinical use in functional muscular transfer. Surg Radiol Anat 38(6):675–685PubMedCrossRefGoogle Scholar
  122. Zijdewind C, Bosch W, Goessens L, Kandou TW, Kernell D (1990) Electromyogram and force during stimulated fatigue tests of muscles in dominant and non-dominant hands. Eur J Appl Physiol Occup Physiol 60(2):127–132PubMedCrossRefGoogle Scholar
  123. Zory R, Boerio D, Jubeau M, Maffiuletti NA (2005) Central and peripheral fatigue of the knee extensor muscles induced by electromyostimulation. Int J Sports Med 26(10):847–853.  https://doi.org/10.1055/s-2005-837459 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Electrical and Electronical EngineeringPublic University of NavarraPamplonaSpain
  2. 2.Institute of Sport SciencesUniversity of LausanneLausanneSwitzerland

Personalised recommendations