Neural adaptations to strength training: Moving beyond transcranial magnetic stimulation and reflex studies

Acta Physiologica

Volumn 202, Issue 2, 2011, Pages 119-140

  Carroll, T J ^a   Selvanayagam, V S ^a,b   Riek, S ^a   Semmler, J G ^c  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF MALAYA   (Malaysia)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

H reflex; Muscle strength; Single motor unit; Transcranial magnetic stimulation; V wave

Indexed keywords

CENTRAL NERVOUS SYSTEM; ELECTROENCEPHALOGRAPHY; ELECTROSTIMULATION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HOFFMANN REFLEX; MOTOR UNIT; MUSCLE STRENGTH; MUSCLE TISSUE; NEUROPHYSIOLOGY; NON INVASIVE PROCEDURE; NONHUMAN; PERIPHERAL NERVE; PRIORITY JOURNAL; REVIEW; TRAINING; TRANSCRANIAL MAGNETIC STIMULATION;

ADAPTATION, PHYSIOLOGICAL; BRAIN; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, MOTOR; HUMANS; MAGNETIC RESONANCE IMAGING; MUSCLE, SKELETAL; REFLEX; RESISTANCE TRAINING; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 79955650280     PISSN: 17481708     EISSN: 17481716     Source Type: Journal    
DOI: 10.1111/j.1748-1716.2011.02271.x     Document Type: Review

References (154)

1. Aagaard, P., Simonsen, E.B., Andersen, J.L., Magnusson, P. & Dyhre-Poulsen, P. 2002. Neural adaptation to resistance training: changes in evoked V-wave and H-reflex responses. J Appl Physiol 92, 2309-2318.
2. Abraham, W.C. & Bear, M.F. 1996. Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19, 126-130.
3. Adkins, D.L., Boychuk, J., Remple, M.S. & Kleim, J.A. 2006. Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord. J Appl Physiol 101, 1776-1782.
4. Adrian, E.D. & Bronk, D.W. 1929. The discharge of impulses in motor nerve fibres: part II. The frequency of discharge in reflex and voluntary contractions. J Physiol 67, i3-i151.
5. Barker, A.T. 1991. An introduction to the basic principles of magnetic nerve-stimulation. J Clin Neurophysiol 8, 26-37.
6. Barker, A.T., Jalinous, R. & Freeston, I.L. 1985. Non-invasive magnetic stimulation of human motor cortex. Lancet 1, 1106-1107.
7. Bawa, P. & Calancie, B. 1983. Repetitive doublets in human flexor carpi radialis muscle. J Physiol 339, 123-132.
8. Beck, S., Taube, W., Gruber, M., Amtage, F., Gollhofer, A. & Schubert, M. 2007. Task-specific changes in motor evoked potentials of lower limb muscles after different training interventions. Brain Res 1179, 51-60.
9. Bigland-Ritchie, B., Jones, D.A. & Woods, J.J. 1979. Excitation frequency and muscle fatigue: electrical responses during human voluntary and stimulated contractions. Exp Neurol 64, 414-427.
10. Bostock, H. & Grafe, P. 1985. Activity-dependent excitability changes in normal and demyelinated rat spinal root axons. J Physiol 365, 239-257.
11. Brocke, J., Irlbacher, K., Hauptmann, B., Voss, M. & Brandt, S.A. 2005. Transcranial magnetic and electrical stimulation compared: does TES activate intracortical neuronal circuits? Clin Neurophysiol 116, 2748-2756.
12. Burke, D. & Gandevia, S.C. 1999. Properties of human peripheral nerves: implications for studies of human motor control. In: M.D. Binder (ed.) Peripheral and Spinal Mechanisms in the Neural Control of Movement, pp. 427-435. Elsevier Science, Amsterdam.
13. Burke, D., Gandevia, S.C. & McKeon, B. 1984. Mono-synaptic and oligosynaptic contributions to human ankle jerk and H-reflex. J Neurophysiol 52, 435-448.
14. Butler, E.G., Bourke, D.W. & Horne, M.K. 2000. The activity of primate ventrolateral thalamic neurones during motor adaptation. Exp Brain Res 133, 514-531.
15. Capaday, C. 1997. Neurophysiological methods for studies of the motor system in freely moving human subjects. J Neurosci Methods 74, 201-218.
16. Carroll, T.J., Barry, B., Riek, S. & Carson, R.G. 2001. Resistance training enhances the stability of sensorimotor coordination. Proc Biol Sci 268, 221-227.
17. Carroll, T.J., Riek, S. & Carson, R.G. 2002. The sites of neural adaptation induced by resistance training in humans. J Physiol 544, 641-652.
18. Carroll, T.J., Barton, J., Hsu, M. & Lee, M. 2009. The effect of strength training on the force of twitches evoked by corticospinal stimulation in humans. Acta Physiol 197, 161-173.
19. Carson, R.G. 2006. Changes in muscle coordination with training. J Appl Physiol 101, 1506-1513.
20. Chen, R., Classen, J., Gerloff, C., Celnik, P., Wassermann, E.M., Hallett, M. & Cohen, L.G. 1997. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48, 1398-1403.
21. Christie, A. & Kamen, G. 2006. Doublet discharges in motoneurons of young and older adults. J Neurophysiol 95, 2787-2795.
22. Christie, A. & Kamen, G. 2010. Short-term training adaptations in maximal motor unit firing rates and afterhyperpolarization duration. Muscle Nerve 41, 651-660.
23. Conway, B.A., Halliday, D.M., Farmer, S.F., Shahani, U., Maas, P., Weir, A.I. & Rosenberg, J.R. 1995. Synchronization between motor cortex and spinal motoneuronal pool during the performance of a maintained motor task in man. J Physiol 489, 917-924.
24. Dartnall, T.J., Nordstrom, M.A. & Semmler, J.G. 2008. Motor unit synchronization is increased in biceps brachii after exercise-induced damage to elbow flexor muscles. J Neurophysiol 99, 1008-1019.
25. Day, B.L., Dressler, D., Maertens de Noordhout, A., Marsden, C.D., Nakashima, K., Rothwell, J.C. & Thompson, P.D. 1989. Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. J Physiol 412, 449-473.
26. De Luca, C.J., LeFever, R.S., McCue, M.P. & Xenakis, A.P. 1982. Control scheme governing concurrently active human motor units during voluntary contractions. J Physiol 329, 129-142.
27. De Luca, C.J., Adam, A., Wotiz, R., Gilmore, L.D. & Nawab, S.H. 2006. Decomposition of surface EMG signals. J Neurophysiol 96, 1646-1657.
28. 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, 402-411.
29. Del Valle, A. & Thomas, C.K. 2005. Firing rates of motor units during strong dynamic contractions. Muscle Nerve 32, 316-325.
30. Di Lazzaro, V., Oliviero, A., Profice, P., Saturno, E., Pilato, F., Insola, A., Mazzone, P., Tonali, P. & Rothwell, J.C. 1998a. Comparison of descending volleys evoked by transcranial magnetic and electric stimulation in conscious humans. Electroencephalogr Clin Neurophysiol 109, 397-401.
31. Di Lazzaro, V., Restuccia, D., Oliviero, A., Profice, P., Ferrara, L., Insola, A., Mazzone, P., Tonali, P. & Rothwell, J.C. 1998b. Effects of voluntary contraction on descending volleys evoked by transcranial stimulation in conscious humans. J Physiol 508, 625-633.
32. Di Lazzaro, V., Oliviero, A., Pilato, F., Saturno, E., Dileone, M., Mazzone, P., Insola, A., Tonali, P.A. & Rothwell, J.C. 2004. The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol 115, 255-266.
33. Diedrichsen, J., Hashambhoy, Y., Rane, T. & Shadmehr, R. 2005. Neural correlates of reach errors. J Neurosci 25, 9919-9931.
34. Doherty, T.J. & Brown, W.F. 1994. A method for the longitudinal study of human thenar motor units. Muscle Nerve 17, 1029-1036.
35. Duclay, J., Martin, A., Robbe, A. & Pousson, M. 2008. Spinal reflex plasticity during maximal dynamic contractions after eccentric training. Med Sci Sports Exerc 40, 722-734.
36. Ekblom, M.M.N. 2010. Improvements in dynamic plantar flexor strength after resistance training are associated with increased voluntary activation and V-to-M ratio. J Appl Physiol 109, 19-26.
37. Enoka, R.M. 1996. Eccentric contractions require unique activation strategies by the nervous system. J Appl Physiol 81, 2339-2346.
38. Enoka, R.M., Robinson, G.A. & Kossev, A.R. 1988. A stable, selective electrode for recording single motor-unit potentials in humans. Exp Neurol 99, 761-764.
39. Falvo, M.J., Sirevaag, E.J., Rohrbaugh, J.W. & Earhart, G.M. 2010. Resistance training induces supraspinal adaptations: evidence from movement-related cortical potentials. Eur J Appl Physiol 109, 923-933.
40. Farina, D., Holobar, A., Merletti, R. & Enoka, R.M. 2010. Decoding the neural drive to muscles from the surface electromyogram. Clin Neurophysiol 121, 1616-1623.
41. Farmer, S.F., Bremner, F.D., Halliday, D.M., Rosenberg, J.R. & Stephens, J.A. 1993. The frequency content of common synaptic inputs to motoneurones studied during voluntary isometric contraction in man. J Physiol 470, 127-155.
42. Farmer, S.F., Halliday, D.M., Conway, B.A., Stephens, J.A. & Rosenberg, J.R. 1997. A review of recent applications of cross-correlation methodologies to human motor unit recording. J Neurosci Methods 74, 175-187.
43. Farthing, J.P., Borowsky, R., Chilibeck, P.D., Binsted, G. & Sarty, G.E. 2007. Neuro-physiological adaptations associated with cross-education of strength. Brain Topogr 20, 77-88.
44. Fimland, M.S., Helgerud, J., Gruber, M., Leivseth, G. & Hoff, J. 2009a. Functional maximal strength training induces neural transfer to single-joint tasks. Eur J Appl Physiol 107, 21-29.
45. Fimland, M.S., Helgerud, J., Solstad, G.M., Iversen, V.M., Leivseth, G. & Hoff, J. 2009b. Neural adaptations underlying cross-education after unilateral strength training. Eur J Appl Physiol 107, 723-730.
46. Fitzgerald, P.B., Fountain, S. & Daskalakis, Z.J. 2006. A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol 117, 2584-2596.
47. Fling, B.W., Christie, A. & Kamen, G. 2009. Motor unit synchronization in FDI and biceps brachii muscles of strength-trained males. J Electromyogr Kinesiol 19, 800-809.
48. Frigon, A., Carroll, T.J., Jones, K.E., Zehr, E.P. & Collins, D.F. 2007. Ankle position and voluntary contraction alter maximal M waves in soleus and tibialis anterior. Muscle Nerve 35, 756-766.
49. Gandevia, S.C. 2001. Spinal and supraspinal factors in human muscle fatigue. Physiol Rev 81, 1725-1789.
50. Gandevia, S.C., Allen, G.M., Butler, J.E. & Taylor, J.L. 1996. Supraspinal factors in human muscle fatigue: evidence for suboptimal output from the motor cortex. J Physiol 490, 529-536.
51. Gandevia, S.C., Petersen, N., Butler, J.E. & Taylor, J.L. 1999. Impaired response of human motoneurones to corticospinal stimulation after voluntary exercise. J Physiol 521, 749-759.
52. Garland, S.J. & Griffin, L. 1999. Motor unit double discharges: statistical anomaly or functional entity? Can J Appl Physiol 24, 113-130.
53. Geertsen, S.S., Lundbye-Jensen, J. & Nielsen, J.B. 2008. Increased central facilitation of antagonist reciprocal inhibition at the onset of dorsiflexion following explosive strength training. J Appl Physiol 105, 915-922.
54. Gondin, J., Duclay, J. & Martin, A. 2006. Soleus- and gastrocnemii-evoked V-wave responses increase after neuromuscular electrical stimulation training. J Neurophysiol 95, 3328-3335.
55. Gooch, C.L. & Harati, Y. 1997. Longitudinal tracking of the same single motor unit in amyotrophic lateral sclerosis. Muscle Nerve 20, 511-513.
56. Griffin, L. & Cafarelli, E. 2007. Transcranial magnetic stimulation during resistance training of the tibialis anterior muscle. J Electromyogr Kinesiol 17, 446-452.
57. Griffin, L., Painter, P.E., Wadhwa, A. & Spirduso, W.W. 2009. Motor unit firing variability and synchronization during short-term light-load training in older adults. Exp Brain Res 197, 337-345.
58. Gydikov, A., Kossev, A., Trayanova, N. & Radicheva, N. 1986. Selective recording of motor unit potentials. Electromyogr Clin Neurophysiol 26, 273-281.
59. Hashimoto, R. & Rothwell, J.C. 1999. Dynamic changes in corticospinal excitability during motor imagery. Exp Brain Res 125, 75-81.
60. Holtermann, A., Roeleveld, K., Engstrom, M. & Sand, T. 2007. Enhanced H-reflex with resistance training is related to increased rate of force development. Eur J Appl Physiol 101, 301-312.
61. Hortobagyi, T., Richardson, S.P., 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, 403-411.
62. Hultborn, H. & Nielsen, J.B. 1998. Modulation of transmitter release from Ia afferents by their preceding activity - a 'postactivation depression'. In: P. Rudomin & L. Mendell (eds) Presynaptic Inhibition and Neural Control, pp. 178-191. Oxford University Press, New York.
63. Jensen, J.L., Marstrand, P.C.D. & Nielsen, J.B. 2005. Motor skill training and strength training are associated with different plastic changes in the central nervous system. J Appl Physiol 99, 1558-1568.
64. Kamen, G. & Knight, C.A. 2004. Training-related adaptations in motor unit discharge rate in young and older adults. J Gerontol A Biol Sci Med Sci 59, 1334-1338.
65. Kamen, G., Sison, S.V., Du, C.C. & Patten, C. 1995. Motor unit discharge behavior in older adults during maximal-effort contractions. J Appl Physiol 79, 1908-1913.
66. Karni, A., Meyer, G., Jezzard, P., Adams, M.M., Turner, R. & Ungerleider, L.G. 1995. Functional MRI evidence for adults motor cortex plasticity during motor skiill learning. Nature 377, 155-158.
67. Keen, D.A., Yue, G.H. & Enoka, R.M. 1994. Training-related enhancement in the control of motor output in elderly humans. J Appl Physiol 77, 2648-2658.
68. Kelly, A.M. & Garavan, H. 2005. Human functional neuroimaging of brain changes associated with practice. Cereb Cortex 15, 1089-1102.
69. Kidgell, D.J. & Pearce, A.J. 2010. Corticospinal properties following short-term strength training of an intrinsic hand muscle. Hum Mov Sci 29, 631-641.
70. Kidgell, D.J., Sale, M.V. & Semmler, J.G. 2006. Motor unit synchronization measured by cross-correlation is not influenced by short-term strength training of a hand muscle. Exp Brain Res 175, 745-753.
71. Klass, M., Baudry, S. & Duchateau, J. 2008. Age-related decline in rate of torque development is accompanied by lower maximal motor unit discharge frequency during fast contractions. J Appl Physiol 104, 739-746.
72. Knight, C.A. & Kamen, G. 2004. Enhanced motor unit rate coding with improvements in a force-matching task. J Electromyogr Kinesiol 14, 619-629.
73. Kornatz, K.W., Christou, E.A. & Enoka, R.M. 2005. Practice reduces motor unit discharge variability in a hand muscle and improves manual dexterity in old adults. J Appl Physiol 98, 2072-2080.
74. Lagerquist, O., Zehr, E.P. & Docherty, D. 2006. Increased spinal reflex excitability is not associated with neural plasticity underlying the cross-education effect. J Appl Physiol 100, 83-90.
75. Laidlaw, D.H., Kornatz, K.W., Keen, D.A., Suzuki, S. & Enoka, R.M. 1999. Strength training improves the steadiness of slow lengthening contractions performed by old adults. J Appl Physiol 87, 1786-1795.
76. Lee, M. & Carroll, T.J. 2005. The amplitude of Mmax in human wrist flexors varies during different muscle contractions despite constant posture. J Neurosci Methods 149, 95-100.
77. Lee, M., Gandevia, S.C. & Carroll, T.J. 2008. Cortical voluntary activation can be reliably measured in human wrist extensors using transcranial magnetic stimulation. Clin Neurophysiol 119, 1130-1138.
78. Lee, M., Gandevia, S.C. & Carroll, T.J. 2009. Short-term strength training does not change cortical voluntary activation. Med Sci Sports Exerc 41, 1452-1460.
79. Lee, M., Hinder, M.R., Gandevia, S.C. & Carroll, T.J. 2010. The ipsilateral motor cortex contributes to cross-limb transfer of performance gains after ballistic motor practice. J Physiol 588, 201-212.
80. Logothetis, N.K. 2003. MR imaging in the non-human primate: studies of function and of dynamic connectivity. Curr Opin Neurobiol 13, 630-642.
81. Macefield, V.G., Gandevia, S.C., Bigland-Ritchie, B., Gorman, R.B. & Burke, D. 1993. The firing rates of human motoneurones voluntarily activated in the absence of muscle afferent feedback. J Physiol 471, 429-443.
82. Macefield, V.G., Fuglevand, A.J. & BiglandRitchie, B. 1996. Contractile properties of single motor units in human toe extensors assessed by intraneural motor axon stimulation. J Neurophysiol 75, 2509-2519.
83. Maffiuletti, N.A., 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, 601-607.
84. Magladery, J.W. & McDougal, D.B. 1950. Electrophysiological studies of nerve and reflex activity in normal man.1. Identification of certain reflexes in the electromyogram and the conduction velocity of peripheral nerve fibres. Bull Johns Hopkins Hosp 86, 265-290.
85. Magladery, J.W., Porter, W.E., Park, A.M. & Teasdall, R.D. 1951. Electrophysiological studies of nerve and reflex activity in normal man. IV. The two-neurone reflex and identification of certain action potentials from spinal roots and cord. Bull Johns Hopkins Hosp 88, 499-519.
86. Marchand-Pauvert, V., Nicolas, G., Burke, D. & Pierrot-Deseilligny, E. 2002. Suppression of the H reflex in humans by disynaptic autogenetic inhibitory pathways activated by the test volley. J Physiol 542, 963-976.
87. Matthews, P.B. 1999. The effect of firing on the excitability of a model motoneurone and its implications for cortical stimulation. J Physiol 518, 867-882.
88. McHugh, M.P. 2003. Recent advances in the understanding of the repeated bout effect: the protective effect against muscle damage from a single bout of eccentric exercise. Scand J Med Sci Sports 13, 88-97.
89. Merletti, R., Farina, D. & Gazzoni, M. 2003. The linear electrode array: a useful tool with many applications. J Electromyogr Kinesiol 13, 37-47.
90. Merletti, R., Holobar, A. & Farina, D. 2008. Analysis of motor units with high-density surface electromyography. J Electromyogr Kinesiol 18, 879-890.
91. Merton, P.A. 1954. Voluntary strength and fatigue. J Physiol 123, 553-564.
92. Miller, K.J., Garland, S.J., Ivanova, T. & Ohtsuki, T. 1996. Motor-unit behavior in humans during fatiguing arm movements. J Neurophysiol 75, 1629-1636.
93. Milner-Brown, H.S., Stein, R.B. & Yemm, R. 1973. The contractile properties of human motor units during voluntary isometric contractions. J Physiol 228, 285-306.
94. Milner-Brown, H.S., Stein, R.B. & Lee, R.G. 1975. Synchronization of human motor units-possible roles of exercise and supraspinal reflexes. Electroencephalogr Clin Neurophysiol 38, 245-254.
95. Misiaszek, J.E. 2003. The H-reflex as a tool in neurophysiology: its limitations and uses in understanding nervous system function. Muscle Nerve 28, 144-160.
96. Mogyoros, I., Kiernan, M.C. & Burke, D. 1996. Strength-duration properties of human peripheral nerve. Brain 119, 439-447.
97. Moritz, C.T., Barry, B.K., Pascoe, M.A. & Enoka, R.M. 2005. Discharge rate variability influences the variation in force fluctuations across the working range of a hand muscle. J Neurophysiol 93, 2449-2459.
98. Mottram, C.J., Jakobi, J.M., Semmler, J.G. & Enoka, R.M. 2005. Motor-unit activity differs with load type during a fatiguing contraction. J Neurophysiol 93, 1381-1392.
99. do Nascimento, O.F., Nielsen, K.D. & Voigt, M. 2005. Relationship between plantar-flexor torque generation and the magnitude of the movement-related potentials. Exp Brain Res 160, 154-165.
100. Nawab, S.H., Chang, S.S. & De Luca, C.J. 2010. High-yield decomposition of surface EMG signals. Clin Neurophysiol 121, 1602-1615.
101. Nicol, C., Avela, J. & Komi, P.V. 2006. The stretch-shortening cycle: a model to study naturally occurring neuromuscular fatigue. Sports Med 36, 977-999.
102. Nielsen, J., Petersen, N., Deuschl, G. & Ballegaard, M. 1993. Task-related changes in the effect of magnetic brain stimulation on spinal neurones in man. J Physiol 471, 223-243.
103. Oya, T., Riek, S. & Cresswell, A.G. 2009. Recruitment and rate coding organisation for soleus motor units across entire range of voluntary isometric plantar flexions. J Physiol 587, 4737-4748.
104. Pascual-Leone, A., Grafman, J. & Hallett, M. 1994. Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science 263, 1287-1289.
105. Pasquet, B., Carpentier, A. & Duchateau, J. 2006. Specific modulation of motor unit discharge for a similar change in fascicle length during shortening and lengthening contractions in humans. J Physiol 577, 753-765.
106. Patten, C., Kamen, G. & Rowland, D.M. 2001. Adaptations in maximal motor unit discharge rate to strength training in young and older adults. Muscle Nerve 24, 542-550.
107. Perez, M.A., Tanaka, S., Wise, S.P., Sadato, N., Tanabe, H.C., Willingham, D.T. & Cohen, L.G. 2007. Neural substrates of intermanual transfer of a newly acquired motor skill. Curr Biol 17, 1896-1902.
108. Petersen, N.T., Pyndt, H.S. & Nielsen, J.B. 2003. Investigating human motor control by transcranial magnetic stimulation. Exp Brain Res 152, 1-16.
109. Pierrot-Deseilligny, E. & Burke, D. 2005. The Circuitry of the Human Spinal Cord: Its Role in Motor Control and Movement Disorders. Cambridge University Press, Cambridge.
110. Poldrack, R.A. 2000. Imaging brain plasticity: conceptual and methodological issues - a theoretical review. Neuroimage 12, 1-13.
111. Porter, R. & Lemon, R.N. 1993. Corticospinal Function and Voluntary Movement. Oxford University Press, Oxford.
112. Pucci, A.R., Griffin, L. & Cafarelli, E. 2006. Maximal motor unit firing rates during isometric resistance training in men. Exp Physiol 91, 171-178.
113. Reis, J., Swayne, O.B., Vandermeeren, Y., Camus, M., Dimyan, M.A., Harris-Love, M., Perez, M.A., Ragert, P., Rothwell, J.C. & Cohen, L.G. 2008. Contribution of transcranial magnetic stimulation to the understanding of cortical mechanisms involved in motor control. J Physiol 586, 325-351.
114. Rioult-Pedotti, M.S., Friedman, D., Hess, G. & Donoghue, J.P. 1998. Strengthening of horizontal cortical connections following skill learning. Nat Neurosci 1, 230-234.
115. Rioult-Pedotti, M.S., Friedman, D. & Donoghue, J.P. 2000. Learning-induced LTP in neocortex. Science 290, 533-536.
116. Rosenkranz, K., Kacar, A. & Rothwell, J.C. 2007. Differential modulation of motor cortical plasticity and excitability in early and late phases of human motor learning. J Neurosci 27, 12058-12066.
117. Ruohonen, J. & Ilmoniemi, R.J. 1999. Modeling of the stimulating field generation in TMS. In: W. Paulus, M. Hallett, P.M. Rossini & J.C. Rothwell (eds) Transcranial Magnetic Stimulation. Electroencephalography and Clinical Neurophysiology (Supplement 51), pp. 30-40. Elsevier Science, Amsterdam.
118. Sakai, S.T., Inase, M. & Tanji, J. 2002. The relationship between MI and SMA afferents and cerebellar and pallidal efferents in the macaque monkey. Somatosens Mot Res 19, 139-148.
119. Sale, D.G., McComas, A.J., Macdougall, J.D. & Upton, A.R.M. 1982. Neuromuscular adaptation in human thenar muscles following strength training and immobilization. J Appl Physiol 53, 419-424.
120. Sale, D.G., Macdougall, J.D., Upton, A.R.M. & McComas, A.J. 1983. Effects of strength training upon motoneuron excitability in man. Med Sci Sports Exerc 15, 57-62.
121. Scaglioni, G., Ferri, A., Minetti, A.E., Martin, A., Van Hoecke, J., Capodaglio, P., Sartorio, A. & Narici, M.V. 2002. Plantar flexor activation capacity and H reflex in older adults: adaptations to strength training. J Appl Physiol 92, 2292-2302.
122. Schneider, J., Rau, G. & Silny, J. 1989. A noninvasive EMG technique for investigating the excitation propagation in single motor units. Electromyogr Clin Neurophysiol 29, 273-280.
123. Schubert, M., Beck, S., Taube, W., Amtage, F., Faist, M. & Gruber, M. 2008. Balance training and ballistic strength training are associated with task-specific corticospinal adaptations. Eur J Neurosci 27, 2007-2018.
124. Semmler, J.G. & Nordstrom, M.A. 1998. Motor unit discharge and force tremor in skill- and strength-trained individuals. Exp Brain Res 119, 27-38.
125. Semmler, J.G., Kornatz, K.W., Dinenno, D.V., Zhou, S. & Enoka, R.M. 2002. Motor unit synchronisation is enhanced during slow lengthening contractions of a hand muscle. J Physiol 545, 681-695.
126. Semmler, J.G., Sale, M.V., Meyer, F.G. & Nordstrom, M.A. 2004. Motor-unit coherence and its relation with synchrony are influenced by training. J Neurophysiol 92, 3320-3331.
127. Shibasaki, H. & Hallett, M. 2006. What is the Bereitschaftspotential? Clin Neurophysiol 117, 2341-2356.
128. Sidhu, S.K., Bentley, D.J. & Carroll, T.J. 2009. Cortical voluntary activation of the human knee extensors can be reliably estimated using transcranial magnetic stimulation. Muscle Nerve 39, 186-196.
129. Siemionow, V., Yue, G.H., Ranganathan, V.K., Liu, J.Z. & Sahgal, V. 2000. Relationship between motor activity-related cortical potential and voluntary muscle activation. Exp Brain Res 133, 303-311.
130. Stalberg, E., Nandedkar, S.D., Sanders, D.B. & Falck, B. 1996. Quantitative motor unit potential analysis. J Clin Neurophysiol 13, 401-422.
131. Stefan, K., Kunesch, E., Cohen, L.G., Benecke, R. & Classen, J. 2000. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123, 572-584.
132. Stefan, K., Wycislo, M., Gentner, R., Schramm, A., Naumann, M., Reiners, K. & Classen, J. 2006. Temporary occlusion of associative motor cortical plasticity by prior dynamic motor training. Cereb Cortex 16, 376-385.
133. Stuart, M., Butler, J.E., Collins, D.F., Taylor, J.L. & Gandevia, S.C. 2002. The history of contraction of the wrist flexors can change cortical excitability. J Physiol 545, 731-737.
134. Taylor, J.L. & Gandevia, S.C. 2004. Noninvasive stimulation of the human corticospinal tract. J Appl Physiol 96, 1496-1503.
135. Taylor, J.L., Petersen, N.T., Butler, J.E. & Gandevia, S.C. 2002. Interaction of transcranial magnetic stimulation and electrical transmastoid stimulation in human subjects. J Physiol 541, 949-958.
136. Taylor, A.M., Christou, E.A. & Enoka, R.M. 2003. Multiple features of motor-unit activity influence force fluctuations during isometric contractions. J Neurophysiol 90, 1350-1361.
137. Thomas, C.K., Butler, J.E. & Zijdewind, I. 2002. Patterns of pathological firing in human motor units. In: S.C. Gandevia, U. Proske & D.G. Stuart (eds) Sensorimotor Control of Movement and Posture, pp. 237-244. Kluwer Academic/Plenum Publishers, New York.
138. Todd, G., Taylor, J.L. & Gandevia, S.C. 2003. Measurement of voluntary activation of fresh and fatigued human muscles using transcranial magnetic stimulation. J Physiol 551, 661-671.
139. Todd, G., Taylor, J.L. & Gandevia, S.C. 2004. Reproducible measurement of voluntary activation of human elbow flexors with motor cortical stimulation. J Appl Physiol 97, 236-242.
140. Tracy, B.L., Maluf, K.S., Stephenson, J.L., Hunter, S.K. & Enoka, R.M. 2005. Variability of motor unit discharge and force fluctuations across a range of muscle forces in older adults. Muscle Nerve 32, 533-540.
141. Ugawa, Y., Rothwell, J.C., Day, B.L., Thompson, P.D. & Marsden, C.D. 1991. Precutaneous electric-stimulation of corticospinal pathways at the level of the pyramidal decussation in humans. Ann Neurol 29, 418-427.
142. Upton, A.R., McComas, A.J. & Sica, R.E. 1971. Potentiation of 'late' responses evoked in muscles during effort. J Neurol Neurosurg Psychiatry 34, 699-711.
143. Ushiyama, J., Takahashi, Y. & Ushiba, J. 2010. Muscle dependency of corticomuscular coherence in upper and lower limb muscles and training-related alterations in ballet dancers and weightlifters. J Appl Physiol 109, 1086-1095.
144. Vagg, R., Mogyoros, I., Kiernan, M.C. & Burke, D. 1998. Activity-dependent hyperpolarization of human motor axons produced by natural activity. J Physiol 507, 919-925.
145. 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, 295-305.
146. Vila-Cha, C., Falla, D. & Farina, D. 2010. Motor unit behavior during submaximal contractions following six weeks of either endurance or strength training. J Appl Physiol 109, 1455-1466.
147. Xiong, J.H., Ma, L.S., Wang, B.Q., Narayana, S., Duff, E.P., Egan, G.F. & Fox, P.T. 2009. Long-term motor training induced changes in regional cerebral blood flow in both task and resting states. Neuroimage 45, 75-82.
148. Yao, W.X., Fuglevand, A.J. & Enoka, R.M. 2000. Motor-unit synchronization increases EMG amplitude and decreases force steadiness of simulated contractions. J Neurophysiol 83, 441-452.
149. Yue, G., Fuglevand, A.J., Nordstrom, M.A. & Enoka, R.M. 1995. Limitations of the surface electromyography technique for estimating motor unit synchronization. Biol Cybern 73, 223-233.
150. Zehr, E.P. 2002. Considerations for use of the Hoffmann reflex in exercise studies. Eur J Appl Physiol 86, 455-468.
151. Zhou, P. & Rymer, W.Z. 2004. Factors governing the form of the relation between muscle force and the EMG: a simulation study. J Neurophysiol 92, 2878-2886.
152. Ziemann, U., Iliac, T.V., Pauli, C., Meintzschel, F. & Ruge, D. 2004. Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J Neurosci 24, 1666-1672.
153. Ziemann, U., Ilic, T.V. & Jung, P. 2006. Long-term potentiation (LTP)-like plasticity and learning in human motor cortex - investigations with transcranial magnetic stimulation (TMS). Suppl Clin Neurophysiol 59, 19-25.
154. Ziemann, U., Paulus, W., Nitsche, M.A., Pascual-Leone, A., Byblow, W.D., Berardelli, A., Siebner, H.R., Classen, J., Cohen, L.G. & Rothwell, J.C. 2008. Consensus: motor cortex plasticity protocols. Brain Stimul 1, 164-182.