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Transcranial magnetic stimulation and the motor learning-associated cortical plasticity

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Abstract

It has been well established that repetitive motor performance and skill learning alter the functional organization of human corticomotoneuronal system. Over the past decade, transcranial magnetic stimulation (TMS) has helped to demonstrate motor practice and learning-related changes in corticomotoneuronal excitability and representational plasticity. It has also provided some insights into the mechanisms underlying such plasticity. TMS-derived indices show that motor practice, skill acquisition and learning are associated with an increase in cortical excitability and a modulation of intracortical inhibition partly related to the amount of GABA-related inhibition. It has been suggested that these changes in excitability might be related to learning and motor memory formation in the motor cortex. However, it has proved difficult to relate different aspects of TMS-derived representational plasticity with specific behavioral outcomes. A better understanding of the relationship between TMS measurements of practice-related cortical plasticity and underlying mechanisms, in the context of associated changes in behavior, will facilitate the development of techniques and protocols that will allow predictable modulation of cortical plasticity in health and disease.

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References

  • Barker AT (1999) The history and basic principles of magnetic nerve stimulation. Electroencephalogr Clin Neurophysiol Suppl 51:3–21

    PubMed  CAS  Google Scholar 

  • Brasil-Neto JP, Cohen LG, Pascual-Leone A, Jabir FK, Wall RT, Hallett M (1992) Rapid reversible modulation of human motor outputs after transient deafferentation of the forearm: a study with transcranial magnetic stimulation. Neurology 42:1302–1306

    PubMed  CAS  Google Scholar 

  • Butefisch CM, Davis BC, Wise SP, Sawaki L, Kopylev L, Classen J, Cohen LG (2000) Mechanisms of use-dependent plasticity in the human motor cortex. Proc Natl Acad Sci USA 97:3661–3665

    Article  PubMed  CAS  Google Scholar 

  • Butefisch CM, Davis BC, Sawaki L, Waldvogel D, Classen J, Kopylev L, Cohen LG (2002) Modulation of use-dependent plasticity by d-amphetamine. Ann Neurol 51:59–68

    Article  PubMed  CAS  Google Scholar 

  • Castro-Alamancos MA, Donoghue JP, Connors BW (1995) Different forms of synaptic plasticity in somatosensory and motor areas of the neocortex. J Neurosci 15:5324–5333

    PubMed  CAS  Google Scholar 

  • Chen R, Classen J, Gerloff C, Celnik P, Wassermann EM, Hallett M, Cohen LG (1997) Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48:1398–1403

    PubMed  CAS  Google Scholar 

  • Classen J, Liepert J, Wise SP, Hallett M, Cohen LG (1998) Rapid plasticity of human cortical movement representation induced by practice. J Neurophysiol 79:1117–1123

    PubMed  CAS  Google Scholar 

  • Classen J, Liepert J, Hallett M, Cohen L (1999a) Plasticity of movement representation in the human motor cortex. Electroencephalogr Clin Neurophysiol Suppl 51:162–173

    CAS  Google Scholar 

  • Classen J, Liepert J, Hallett M, Cohen LG (1999b) Plasticity of movement representation in the human motor cortex. In: Paulus W, Rothwell JC, Hallett M, Rossini PM (eds) Transcranial magnetic stimulation. Elsevier Press, Amsterdam, pp 162–173

    Google Scholar 

  • Devanne H, Lavoie BA, Capaday C (1997) Input–output properties and gain changes in the human corticospinal pathway. Exp.Brain Res 114:329–338

    Article  PubMed  CAS  Google Scholar 

  • Donoghue JP (1995) Plasticity of adult sensorimotor representations. Curr Opin Neurobiol 5:749–754

    Article  PubMed  CAS  Google Scholar 

  • Elbert T, Pantev C, Wienbruch C, Rockstroh B, Taub E (1995) Increased cortical representation of the fingers of the left hand in string players. Science 270:305–307

    Article  PubMed  CAS  Google Scholar 

  • Hallett M (2000) Transcranial magnetic stimulation and the human brain. Nature 406:147–150

    Article  PubMed  CAS  Google Scholar 

  • Jacobs KM, Donoghue JP (1991) Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251:944–947

    Article  PubMed  CAS  Google Scholar 

  • Jensen JL, Marstrand PC, Nielsen JB (2005) Motor skill training and strength training are associated with different plastic changes in the central nervous system. J Appl Physiol 99:1558–1568

    Article  PubMed  Google Scholar 

  • Kujirai T, Caramia MD, Rothwell JC, Day BL, Thompson PD, Ferbert A, Wroe S, Asselman P, Marsden CD (1993) Corticocortical inhibition in human motor cortex. J Physiol 471:501–519

    PubMed  CAS  Google Scholar 

  • Lefaucheur JP, Drouot X, Menard-Lefaucheur I, Zerah F, Bendib B, Cesaro P, Keravel Y, Nguyen JP (2004) Neurogenic pain relief by repetitive transcranial magnetic cortical stimulation depends on the origin and the site of pain. J Neurol Neurosurg Psychiatr 75:612–616

    Article  PubMed  Google Scholar 

  • Liepert J, Schwenkreis P, Tegenthoff M, Malin JP (1997) The glutamate antagonist riluzole suppresses intracortical facilitation. J Neural Transm 104:1207–1214

    Article  PubMed  CAS  Google Scholar 

  • Liepert J, Oreja-Guevara C, Cohen LG, Tegenthoff M, Hallett M, Malin JP (1999a) Plasticity of cortical hand muscle representation in patients with hemifacial spasm. Neurosci Lett 272:33–36

    Article  CAS  Google Scholar 

  • Liepert J, Terborg C, Weiller C (1999b) Motor plasticity induced by synchronized thumb and foot movements. Exp.Brain Res 125:435–439

    Article  CAS  Google Scholar 

  • Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000a) Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp.Brain Res 133:425–430

    Article  CAS  Google Scholar 

  • Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000b) Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol 111:800–805

    Article  CAS  Google Scholar 

  • Malinow R, Mainen ZF, Hayashi Y (2000) LTP mechanisms: from silence to four-lane traffic. Curr Opin Neurobiol 10:352–357

    Article  PubMed  CAS  Google Scholar 

  • Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649–711

    Article  PubMed  CAS  Google Scholar 

  • Muellbacher W, Ziemann U, Boroojerdi B, Hallett M (2000) Effects of low-frequency transcranial magnetic stimulation on motor excitability and basic motor behavior. Clin Neurophysiol 111:1002–1007

    Article  PubMed  CAS  Google Scholar 

  • Muellbacher W, Ziemann U, Boroojerdi B, Cohen L, Hallett M (2001) Role of the human motor cortex in rapid motor learning. Exp Brain Res 136:431–438

    Article  PubMed  CAS  Google Scholar 

  • Muellbacher W, Ziemann U, Wissel J, Dang N, Kofler M, Facchini S, Boroojerdi B, Poewe W, Hallett M (2002) Early consolidation in human primary motor cortex. Nature 415:640–644

    Article  PubMed  CAS  Google Scholar 

  • Pascual-Leone A, Torres F (1993) Plasticity of the sensorimotor cortex representation of the reading finger in Braille readers. Brain 116(Pt 1):39–52

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pascual-Leone A, Nguyet D, Cohen LG, Brasil-Neto JP, Cammarota A, Hallett M (1995a) Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 74:1037–1045

    CAS  Google Scholar 

  • Pascual-Leone A, Wassermann EM, Sadato N, Hallett M (1995b) The role of reading activity on the modulation of motor cortical outputs to the reading hand in Braille readers. Ann Neurol 38:910–915

    Article  CAS  Google Scholar 

  • Pascual-Leone A, Rubio B, Pallardo F, Catala MD (1996) Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression. Lancet 348:233–237

    Article  PubMed  CAS  Google Scholar 

  • Pearce AJ, Thickbroom GW, Byrnes ML, Mastaglia FL (2000) Functional reorganisation of the corticomotor projection to the hand in skilled racquet players. Exp Brain Res 130:238–243

    Article  PubMed  CAS  Google Scholar 

  • Ridding MC, Brouwer B, Nordstrom MA (2000) Reduced interhemispheric inhibition in musicians. Exp Brain Res 133:249–253

    Article  PubMed  CAS  Google Scholar 

  • Rossi S, Rossini PM (2004) TMS in cognitive plasticity and the potential for rehabilitation. Trends Cogn Sci 8:273–279

    Article  PubMed  Google Scholar 

  • Rossi S, Pasqualetti P, Rossini PM, Feige B, Ulivelli M, Glocker FX, Battistini N, Lucking CH, Kristeva-Feige R (2000) Effects of repetitive transcranial magnetic stimulation on movement-related cortical activity in humans. Cereb Cortex 10:802–808

    Article  PubMed  CAS  Google Scholar 

  • Rossini PM, Barker AT, Berardelli A, Caramia MD, Caruso G, Cracco RQ, Dimitrijevic MR, Hallett M, Katayama Y, Lucking CH (1994) Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 91:79–92

    Article  PubMed  CAS  Google Scholar 

  • Rothwell JC (2003) Techniques of transcranial magnetic stimulation. In: Boniface SJ, Ziemann U (eds) Plasticity in the human nervous system. Investigations with transcranial magnetic stimulation. Cambridge University Press, Cambridge, pp 26–62

    Google Scholar 

  • Rothwell JC, Hallett M, Berardelli A, Eisen A, Rossini P, Paulus W (1999) Magnetic stimulation: motor evoked potentials. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 52:97–103

    PubMed  CAS  Google Scholar 

  • Sanes JN, Donoghue JP (2000) Plasticity and primary motor cortex. Annu Rev Neurosci 23:393–415

    Article  PubMed  CAS  Google Scholar 

  • Sawaki L, Boroojerdi B, Kaelin-Lang A, Burstein AH, Butefisch CM, Kopylev L, Davis B, Cohen LG (2002a) Cholinergic influences on use-dependent plasticity. J Neurophysiol. 87:166–171

    CAS  Google Scholar 

  • Sawaki L, Cohen LG, Classen J, Davis BC, Butefisch CM (2002b) Enhancement of use-dependent plasticity by D-amphetamine. Neurology 59:1262–1264

    CAS  Google Scholar 

  • Sawaki L, Werhahn KJ, Barco R, Kopylev L, Cohen LG (2003) Effect of an alpha(1)-adrenergic blocker on plasticity elicited by motor training. Exp Brain Res 148:504–508

    PubMed  CAS  Google Scholar 

  • Schwenkreis P, Pleger B, Hoffken O, Malin JP, Tegenthoff M (2001) Repetitive training of a synchronised movement induces short-term plastic changes in the human primary somatosensory cortex. Neurosci Lett 312:99–102

    Article  PubMed  CAS  Google Scholar 

  • Siebner HR, Rothwell J (2003) Transcranial magnetic stimulation: new insights into representational cortical plasticity. Exp.Brain Res 148:1–16

    Article  PubMed  Google Scholar 

  • Siebner HR, Auer C, Ceballos-Baumann A, Conrad B (1999a) Has repetitive transcranial magnetic stimulation of the primary motor hand area a therapeutic application in writer’s cramp? Electroencephalogr Clin Neurophysiol.Suppl 51:265–275

    CAS  Google Scholar 

  • Siebner HR, Tormos JM, Ceballos-Baumann AO, Auer C, Catala MD, Conrad B, Pascual-Leone A (1999b) Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer’s cramp. Neurology 52:529–537

    CAS  Google Scholar 

  • Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J (2000) Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123(Pt 3):572–584

    Article  PubMed  Google Scholar 

  • Stefan K, Kunesch E, Benecke R, Cohen LG, Classen J (2002) Mechanisms of enhancement of human motor cortex excitability induced by interventional paired associative stimulation. J Physiol 543:699–708

    Article  PubMed  CAS  Google Scholar 

  • Stefan K, Wycislo M, Gentner R, Schramm A, Naumann M, Reiners K, Classen J (2005) Temporary occlusion of associative motor cortical plasticity by prior dynamic motor training. Cereb Cortex 16(3):376–385

    Article  PubMed  Google Scholar 

  • Tergau F, Naumann U, Paulus W, Steinhoff BJ (1999) Low-frequency repetitive transcranial magnetic stimulation improves intractable epilepsy. Lancet 353:2209

    Article  PubMed  CAS  Google Scholar 

  • Touge T, Gerschlager W, Brown P, Rothwell JC (2001) Are the after-effects of low-frequency rTMS on motor cortex excitability due to changes in the efficacy of cortical synapses? Clin Neurophysiol 112:2138–2145

    Article  PubMed  CAS  Google Scholar 

  • Walsh V, Rushworth M (1999) A primer of magnetic stimulation as a tool for neuropsychology. Neuropsychologia 37:125–135

    PubMed  CAS  Google Scholar 

  • Wolters A, Sandbrink F, Schlottmann A, Kunesch E, Stefan K, Cohen LG, Benecke R, Classen J (2003) A temporally asymmetric Hebbian rule governing plasticity in the human motor cortex. J Neurophysiol. 89:2339–2345

    Article  PubMed  Google Scholar 

  • Woody CD, Gruen E, Birt D (1991) Changes in membrane currents during Pavlovian conditioning of single cortical neurons. Brain Res. 539:76–84

    Article  PubMed  CAS  Google Scholar 

  • Ziemann U (2004) TMS induced plasticity in human cortex. Rev Neurosci 15:253–266

    PubMed  Google Scholar 

  • Ziemann U, Lonnecker S, Paulus W (1995) Inhibition of human motor cortex by ethanol. A transcranial magnetic stimulation study. Brain 118(Pt 6):1437–1446

    Article  PubMed  Google Scholar 

  • Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W (1996a) Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 40:367–378

    Article  CAS  Google Scholar 

  • Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W (1996b) The effect of lorazepam on the motor cortical excitability in man. Exp.Brain Res 109:127–135

    Article  CAS  Google Scholar 

  • Ziemann U, Muellbacher W, Hallett M, Cohen LG (2001) Modulation of practice-dependent plasticity in human motor cortex. Brain 124:1171–1181

    Article  PubMed  CAS  Google Scholar 

  • Ziemann U, Ilic TV, 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

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The author acknowledges the support of the Serbian Ministry for Science, Technology and Development Grant 145083.

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Correspondence to Milos Ljubisavljevic.

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Ljubisavljevic, M. Transcranial magnetic stimulation and the motor learning-associated cortical plasticity. Exp Brain Res 173, 215–222 (2006). https://doi.org/10.1007/s00221-006-0538-z

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