Principles of therapeutic use of transcranial and epidural cortical stimulation

Clinical Neurophysiology

Volumn 119, Issue 10, 2008, Pages 2179-2184

  Lefaucheur, Jean Pascal ^a  

^a HENRI MONDOR HOSPITAL   (France)

Author keywords

Epidural cortical stimulation; Mechanisms of action; Parameters of stimulation; Transcranial direct current stimulation; Transcranial magnetic stimulation; Treatment

Indexed keywords

ALGORITHM; BRAIN DEPTH STIMULATION; CELL ACTIVATION; DIRECT CURRENT; ELECTRIC FIELD; ELECTROCONVULSIVE THERAPY; ELECTRODE; ELECTROSTIMULATION; HUMAN; MOTOR CORTEX; NERVE CELL PLASTICITY; NEUROIMAGING; NEUROMODULATION; NEUROPATHIC PAIN; NON INVASIVE PROCEDURE; PAIRED ASSOCIATE LEARNING; PRIORITY JOURNAL; REVIEW; SOMATOSENSORY CORTEX; STROKE; STROKE PATIENT; THETA RHYTHM; TRANSCRANIAL MAGNETIC STIMULATION;

CEREBRAL CORTEX; ELECTRIC STIMULATION THERAPY; ELECTRODES; HUMANS; MENTAL DISORDERS; NERVOUS SYSTEM DISEASES; TRANSCRANIAL MAGNETIC STIMULATION;

EID: 52949154648     PISSN: 13882457     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.clinph.2008.07.007     Document Type: Review

References (113)

1. Abraham W.C., and Tate W.P. Metaplasticity: a new vista across the field of synaptic plasticity. Prog Neurobiol 52 (1997) 303-323
2. Amassian V.E., and Stewart M. Motor cortical and other cortical interneuronal networks that generate very high frequency waves. Suppl Clin Neurophysiol 56 (2003) 119-142
3. Amassian V.E., Stewart M., Quirk G.J., and Rosenthal J.L. Physiological basis of motor effects of a transient stimulus to cerebral cortex. Neurosurgery 20 (1987) 74-93
4. Barker A.T., Jalinous R., and Freeston I.L. Non-invasive magnetic stimulation of human motor cortex. Lancet 1 (1985) 1106-1107
5. Bäumer T., Lange R., Liepert J., Weiller C., Siebner H.R., Rothwell J.C., et al. Repeated premotor rTMS leads to cumulative plastic changes of motor cortex excitability in humans. Neuroimage 20 (2003) 550-560
6. Bezard E., Boraud T., Nguyen J.P., Velasco F., Keravel Y., and Gross C. Cortical stimulation and epileptic seizure: a study of the potential risk in primates. Neurosurgery 45 (1999) 346-350
7. Bienenstock E.L., Cooper L.N., and Munro P.W. Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex. J Neurosci 2 (1982) 32-48
8. Bindman L.J., Lippold O.C., and Redfearn J.W. The action of brief polarizing currents on the cerebral cortex of the rat (1) during current flow and (2) in the production of long-lasting after-effects. J Physiol (London) 172 (1964) 369-382
9. Brown J.A., Lutsep H.L., Weinand M., and Cramer S.C. Motor cortex stimulation for the enhancement of recovery from stroke: a prospective, multicenter safety study. Neurosurgery 58 (2006) 464-473
10. Buhmann C., Gorsler A., Baumer T., Hidding U., Demiralay C., Hinkelmann K., et al. Abnormal excitability of premotor-motor connections in de novo Parkinson's disease. Brain 127 (2004) 2732-2746
11. Canavero S., Bonicalzi V., Paolotti R., Castellano G., Greco-Crasto S., Rizzo L., et al. Therapeutic extradural cortical stimulation for movement disorders: a review. Neurol Res 25 (2003) 118-122
12. Chen R., Classen J., Gerloff C., Celnik P., Wassermann E.M., Hallett M., et al. Depression of motor cortex excitability by low-frequency transcranial magnetic stimulation. Neurology 48 (1997) 1398-1403
13. Conforto A.B., Kaelin-Lang A., and Cohen L.G. Increase in hand muscle strength of stroke patients after somatosensory stimulation. Ann Neurol 51 (2002) 122-125
14. Cooper I.S., and Upton A.R. Use of chronic cerebellar stimulation for disorders of disinhibition. Lancet 1 (1978) 595-600
15. Daskalakis Z.J., Moller B., Christensen B.K., Fitzgerald P.B., Gunraj C., and Chen R. The effects of repetitive transcranial magnetic stimulation on cortical inhibition in healthy human subjects. Exp Brain Res 174 (2006) 403-412
16. Di Lazzaro V., Oliviero A., Pilato F., Saturno E., Dileone M., Mazzone P., et al. The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol 115 (2004) 255-266
17. Edwards M.J., Huang Y.Z., Mir P., Rothwell J.C., and Bhatia K.P. Abnormalities in motor cortical plasticity differentiate manifesting and nonmanifesting DYT1 carriers. Mov Disord 21 (2006) 2181-2186
18. Eichhammer P., Langguth B., Marienhagen J., Kleinjung T., and Hajak G. Neuronavigated repetitive transcranial magnetic stimulation in patients with tinnitus: a short case series. Biol Psychiatry 54 (2003) 862-865
19. Fink M. Convulsive therapy: a review of the first 55 years. J Affect Disord 63 (2001) 1-15
20. Fitzgerald P.B., Brown T.L., Marston N.A., Oxley T., De Castella A., Daskalakis Z.J., et al. Reduced plastic brain responses in schizophrenia: a transcranial magnetic stimulation study. Schizophr Res 71 (2004) 17-26
21. Fitzgerald P.B., Fountain S., and Daskalakis Z.J. A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol 117 (2006) 2584-2596
22. Fregni F., and Pascual-Leone A. Technology insight: noninvasive brain stimulation in neurology-perspectives on the therapeutic potential of rTMS and tDCS. Nat Clin Pract Neurol 3 (2007) 383-393
23. Fregni F., Boggio P.S., Valle A.C., Otachi P., Thut G., Rigonatti S.P., et al. Homeostatic effects of plasma valproate levels on corticospinal excitability changes induced by 1 Hz rTMS in patients with juvenile myoclonic epilepsy. Clin Neurophysiol 117 (2006) 1217-1227
24. Garcia L., D'Alessandro G., Bioulac B., and Hammond C. High-frequency stimulation in Parkinson's disease: more or less?. Trends Neurosci 28 (2005) 209-216
25. Garcia-Larrea L., and Peyron R. Motor cortex stimulation for neuropathic pain: from phenomenology to mechanisms. Neuroimage 37S1 (2007) S71-S79
26. George M.S., Wassermann E.M., Williams W.A., Callahan A., Ketter T.A., Basser P., et al. Daily repetitive transcranial magnetic stimulation (rTMS) improves mood in depression. Neuroreport 6 (1995) 1853-1856
27. George M.S., Wassermann E.M., Williams W.A., Steppel J., Pascual-Leone A., Basser P., et al. Changes in mood and hormone levels after rapid-rate transcranial magnetic stimulation (rTMS) of the prefrontal cortex. J Neuropsychiatry Clin Neurosci 8 (1996) 172-180
28. Gershon A.A., Dannon P.N., and Grunhaus L. Transcranial magnetic stimulation in the treatment of depression. Am J Psychiatry 160 (2003) 835-845
29. Gilio F., Curra A., Inghilleri M., Lorenzano C., Manfredi M., and Berardelli A. Repetitive magnetic stimulation of cortical motor areas in Parkinson's disease: implications for the pathophysiology of cortical function. Mov Disord 17 (2002) 467-473
30. Gorman A.L. Differential patterns of activation of the pyramidal system elicited by surface anodal and cathodal cortical stimulation. J Neurophysiol 29 (1966) 547-564
31. Hallett M. Transcranial magnetic stimulation: a primer. Neuron 55 (2007) 187-199
32. Hoffman R.E., Boutros N.N., Berman R.M., Roessler E., Belger A., Krystal J.H., et al. Transcranial magnetic stimulation of left temporoparietal cortex in three patients reporting hallucinated voices. Biol Psychiatry 46 (1999) 130-132
33. Huang Y.Z., Edwards M.J., Rounis E., Bhatia K.P., and Rothwell J.C. Theta burst stimulation of the human motor cortex. Neuron 45 (2005) 201-206
34. Inghilleri M., Conte A., Curra A., Frasca V., Lorenzano C., and Berardelli A. Ovarian hormones and cortical excitability. An rTMS study in humans. Clin Neurophysiol 115 (2004) 1063-1068
35. Inghilleri M., Conte A., Frasca V., Scaldaferri N., Gilio F., Santini M., et al. Altered response to rTMS in patients with Alzheimer's disease. Clin Neurophysiol 117 (2006) 103-109
36. Iyer M.B., Schleper N., and Wassermann E.M. Priming stimulation enhances the depressant effect of low-frequency repetitive transcranial magnetic stimulation. J Neurosci 23 (2003) 10867-10872
37. Kaneko K., Kawai S., Fuchigami Y., Morita H., and Ofuji A. The effect of current direction induced by transcranial magnetic stimulation on the corticospinal excitability in human brain. Electroencephalogr Clin Neurophysiol 101 (1996) 478-482
38. Khedr E.M., Gilio F., and Rothwell J. Effects of low frequency and low intensity repetitive paired pulse stimulation of the primary motor cortex. Clin Neurophysiol 115 (2004) 1259-1263
39. Khedr E.M., Ahmed M.A., Fathy N., and Rothwell J.C. Therapeutic trial of repetitive transcranial magnetic stimulation after acute ischemic stroke. Neurology 65 (2005) 466-468
40. Khedr E.M., Kotb H., Kamel N.F., Ahmed M.A., Sadek R., and Rothwell J.C. Longlasting antalgic effects of daily sessions of repetitive transcranial magnetic stimulation in central and peripheral neuropathic pain. J Neurol Neurosurg Psychiatry 76 (2005) 833-838
41. Khedr E.M., Rothwell J.C., Shawky O.A., Ahmed M.A., and Hamdy A. Effect of daily repetitive transcranial magnetic stimulation on motor performance in Parkinson's disease. Mov Disord 21 (2006) 2201-2205
42. Kim Y.H., You S.H., Ko M.H., Park J.W., Lee K.H., Jang S.H., et al. Repetitive transcranial magnetic stimulation-induced corticomotor excitability and associated motor skill acquisition in chronic stroke. Stroke 37 (2006) 1471-1476
43. Kleim J.A., Chan S., Pringle E., Schallert K., Procaccio V., Jimenez R., et al. BDNF val66met polymorphism is associated with modified experience-dependent plasticity in human motor cortex. Nat Neurosci 9 (2006) 735-737
44. Klein E., Kreinin I., Chistyakov A., Koren D., Mecz L., Marmur S., et al. Therapeutic efficacy of right prefrontal slow repetitive transcranial magnetic stimulation in major depression: a double-blind controlled study. Arch Gen Psychiatry 56 (1999) 315-320
45. Lang N., Siebner H.R., Ernst D., Nitsche M.A., Paulus W., Lemon R.N., et al. Preconditioning with transcranial direct current stimulation sensitizes the motor cortex to rapid-rate transcranial magnetic stimulation and controls the direction of after-effects. Biol Psychiatry 56 (2004) 634-639
46. Lang N., Siebner H.R., Ward N.S., Lee L., Nitsche M.A., Paulus W., et al. How does transcranial DC stimulation of the primary motor cortex alter regional neuronal activity in the human brain?. Eur J Neurosci 22 (2005) 495-504
47. Langguth B., Eichhammer P., Wiegand R., Marienhegen J., Maenner P., Jacob P., et al. Neuronavigated rTMS in a patient with chronic tinnitus. Effects of 4 weeks treatment. Neuroreport 14 (2003) 977-980
48. Larson J., Wong D., and Lynch G. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res 368 (1986) 347-350
49. Lefaucheur J.P. Stroke recovery can be enhanced by using repetitive transcranial magnetic stimulation (rTMS). Neurophysiol Clin 36 (2006) 105-115
50. Lefaucheur J.P., Drouot X., Keravel Y., and Nguyen J.P. Pain relief induced by repetitive transcranial magnetic stimulation of precentral cortex. Neuroreport 12 (2001) 2963-2965
51. Lefaucheur J.P., Drouot X., and Nguyen J.P. Interventional neurophysiology for pain control: duration of pain relief following repetitive transcranial magnetic stimulation of the motor cortex. Neurophysiol Clin 31 (2001) 247-252
52. Lefaucheur J.P., Drouot X., Ménard-Lefaucheur I., Zerah F., Bendib B., Cesaro P., et al. Neurogenic pain relief by repetitive transcranial magnetic cortical stimulation depends on the origin and the site of pain. J Neurol Neurosurg Psychiatry 75 (2004) 612-616
53. Lefaucheur J.P., Drouot X., Von Raison F., Ménard-Lefaucheur I., Cesaro P., and Nguyen J.P. Improvement of motor performance and modulation of cortical excitability by repetitive transcranial magnetic stimulation of the motor cortex in Parkinson's disease. Clin Neurophysiol 115 (2004) 2530-2541
54. Lefaucheur J.P., Fénelon G., Ménard-Lefaucheur I., Wendling S., and Nguyen J.P. Low-frequency repetitive TMS of premotor cortex can reduce painful axial spasms in generalized secondary dystonia: a pilot study of three patients. Neurophysiol Clin 34 (2004) 141-145
55. Lefaucheur J.P., Drouot X., Ménard-Lefaucheur I., Keravel Y., and Nguyen J.P. Motor cortex rTMS restores defective intracortical inhibition in chronic neuropathic pain. Neurology 67 (2006) 1568-1574
56. Lefaucheur J.P., Hatem S., Nineb A., Menard-Lefaucheur I., Wendling S., Keravel Y., et al. Somatotopic organization of the analgesic effects of motor cortex rTMS in neuropathic pain. Neurology 67 (2006) 1998-2004
57. Liepert J. Motor cortex excitability in stroke before and after constraint-induced movement therapy. Cogn Behav Neurol 19 (2006) 41-47
58. Limoge A., Robert C., and Stanley T.H. Transcutaneous cranial electrical stimulation (TCES): a review 1998. Neurosci Biobehav Rev 23 (1999) 529-538
59. Lisanby S.H. Update on magnetic seizure therapy: a novel form of convulsive therapy. J ECT 18 (2002) 182-188
60. Lomarev M.P., Kanchana S., Bara-Jimenez W., Iyer M., Wassermann E.M., and Hallett M. Placebo-controlled study of rTMS for the treatment of Parkinson's disease. Mov Disord 21 (2006) 325-331
61. Lorenzano C., Dinapoli L., Gilio F., Suppa A., Bagnato S., Curra A., et al. Motor cortical excitability studied with repetitive transcranial magnetic stimulation in patients with Huntington's disease. Clin Neurophysiol 117 (2006) 1677-1681
62. Manola L., Roelofsen B.H., Holsheimer J., Marani E., and Geelen J. Modelling motor cortex stimulation for chronic pain control: electrical potential field, activating functions and responses of simple nerve fibre models. Med Biol Eng Comput 43 (2005) 335-343
63. Manola L., Holsheimer J., Veltink P., and Buitenweg J.R. Anodal vs cathodal stimulation of motor cortex: a modeling study. Clin Neurophysiol 118 (2007) 464-474
64. Mansur C.G., Fregni F., Boggio P.S., Riberto M., Gallucci-Neto J., Santos C.M., et al. A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology 64 (2005) 1802-1804
65. McIntyre C.C., and Grill W.M. Extracellular stimulation of central neurons: influence of stimulus waveform and frequency on neuronal output. J Neurophysiol 88 (2002) 1592-1604
66. McKay D.R., Ridding M.C., Thompson P.D., and Miles T.S. Induction of persistent changes in the organisation of the human motor cortex. Exp Brain Res 143 (2002) 342-349
67. Merton P.A., and Morton H.B. Stimulation of the cerebral cortex in the intact human subject. Nature 285 (1980) 227
68. Mir P., Matsunaga K., Gilio F., Quinn N.P., Siebner H.R., and Rothwell J.C. Dopaminergic drugs restore facilitatory premotor-motor interactions in Parkinson disease. Neurology 64 (2005) 1906-1912
69. Muller J.F., Orekhov Y., Liu Y., and Ziemann U. Homeostatic plasticity in human motor cortex demonstrated by two consecutive sessions of paired associative stimulation. Eur J Neurosci 25 (2007) 3461-3468
70. Murase N., Rothwell J.C., Kaji R., Urushihara R., Nakamura K., Murayama N., et al. Subthreshold low-frequency repetitive transcranial magnetic stimulation over the premotor cortex modulates writer's cramp. Brain 128 (2005) 104-115
71. Nakamura H., Kitagawa H., Kawaguchi Y., and Tsuji H. Direct and indirect activation of human corticospinal neurons by transcranial magnetic and electrical stimulation. Neurosci Lett 210 (1996) 45-48
72. Nguyen J.P., Lefaucheur J.P., Decq P., Uchiyama T., Carpentier A., Fontaine D., et al. Chronic motor cortex stimulation in the treatment of central and neuropathic pain. Correlations between clinical, electrophysiological and anatomical data. Pain 82 (1999) 245-251
73. Nitsche M.A., and Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J Physiol (London) 527 (2000) 633-639
74. Nitsche M.A., Liebetanz D., Antal A., Lang N., Tergau F., and Paulus W. Modulation of cortical excitability by weak direct current stimulation - technical, safety and functional aspects. Suppl Clin Neurophysiol 56 (2003) 255-276
75. Nitsche M.A., Grundey J., Liebetanz D., Lang N., Tergau F., and Paulus W. Catecholaminergic consolidation of motor cortical neuroplasticity in humans. Cereb Cortex 14 (2004) 1240-1245
76. Nitsche M.A., Jaussi W., Liebetanz D., Lang N., Tergau F., and Paulus W. Consolidation of human motor cortical neuroplasticity by d-cycloserine. Neuropsychopharmacology 29 (2004) 1573-1578
77. Nitsche M.A., Lampe C., Antal A., Liebetanz D., Lang N., Tergau F., et al. Dopaminergic modulation of long-lasting direct current-induced cortical excitability changes in the human motor cortex. Eur J Neurosci 23 (2006) 1651-1657
78. Nowak L.G., and Bullier J. Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. I: Evidence from chronaxie measurements. Exp Brain Res 118 (1998) 477-488
79. Oxley T., Fitzgerald P.B., Brown T.L., de Castella A., Daskalakis Z.J., and Kulkarni J. Repetitive transcranial magnetic stimulation reveals abnormal plastic response to premotor cortex stimulation in schizophrenia. Biol Psychiatry 56 (2004) 628-633
80. Padberg F., Goldstein-Muller B., Zwanzger P., and Moller H.J. Prefrontal cortex stimulation as antidepressant treatment: mode of action and clinical effectiveness of rTMS. Suppl Clin Neurophysiol 56 (2003) 406-432
81. Pagni C.A., Altibrandi M.G., Bentivoglio A., Caruso G., Cioni B., Fiorella C., et al. Extradural motor cortex stimulation (EMCS) for Parkinson's disease. History and first results by the study group of the Italian neurosurgical society. Acta Neurochir Suppl (Wien) 93 (2005) 113-119
82. Pascual-Leone A., Grafman J., and Hallett M. Modulation of cortical motor output maps during development of implicit and explicit knowledge. Science 263 (1994) 1287-1289
83. Pascual-Leone A., Nguyet D., Cohen L.G., Brasil-Neto J.P., Cammarota A., and Hallett M. Modulation of muscle responses evoked by transcranial magnetic stimulation during the acquisition of new fine motor skills. J Neurophysiol 74 (1995) 1037-1045
84. Pascual-Leone A., Catalá M.D., and Pascual-Leone Pascual A. Lateralized effect of rapid-rate transcranial magnetic stimulation of the prefrontal cortex on mood. Neurology 46 (1996) 499-502
85. Pascual-Leone A., Rubio B., Pallardó F., and Catalá M.D. Rapid-rate transcranial magnetic stimulation of left dorsolateral prefrontal cortex in drug-resistant depression. Lancet 348 (1996) 233-237
86. Pascual-Leone A., Tormos J.M., Keenan J., Tarazona F., Canete C., and Catala M.D. Study and modulation of human cortical excitability with transcranial magnetic stimulation. J Clin Neurophysiol 15 (1998) 333-343
87. Patton H.D., and Amassian V.E. Single and multiple-unit analysis of cortical stage of pyramidal tract activation. J Neurophysiol 17 (1954) 345-363
88. Post R.M., Kimbrell T.A., McCann U.D., Dunn R.T., Osuch E.A., Speer A.M., et al. Repetitive transcranial magnetic stimulation as a neuropsychiatric tool: present status and future potential. J ECT 15 (1999) 39-59
89. Priori A. Brain polarization in humans: a reappraisal of an old tool for prolonged non-invasive modulation of brain excitability. Clin Neurophysiol 114 (2003) 589-595
90. Priori A., Berardelli A., Rona S., Accornero N., and Manfredi M. Polarization of the human motor cortex through the scalp. Neuroreport 9 (1998) 2257-2260
91. Quartarone A., Bagnato S., Rizzo V., Siebner H.R., Dattola V., Scalfari A., et al. Abnormal associative plasticity of the human motor cortex in writer's cramp. Brain 126 (2003) 2586-2596
92. Rachid F., and Bertschy G. Safety and efficacy of repetitive transcranial magnetic stimulation in the treatment of depression: a critical appraisal of the last 10 years. Neurophysiol Clin 36 (2006) 157-183
93. Ranck Jr. J.B. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98 (1975) 417-440
94. Ridding M.C., and Rothwell J.C. Is there a future for therapeutic use of transcranial magnetic stimulation?. Nat Rev Neurosci 8 (2007) 559-567
95. Rizzo V., Siebner H.R., Modugno N., Pesenti A., Munchau A., Gerschlager W., et al. Shaping the excitability of human motor cortex with premotor rTMS. J Physiol (London) 554 (2004) 483-495
96. Rosenthal J., Waller H.J., and Amassian V.E. An analysis of the activation of motor cortical neurons by surface stimulation. J Neurophysiol 30 (1967) 844-858
97. Rounis E., Lee L., Siebner H.R., Rowe J.B., Friston K.J., Rothwell J.C., et al. Frequency specific changes in regional cerebral blood flow and motor system connectivity following rTMS to the primary motor cortex. Neuroimage 26 (2005) 164-176
98. Rumi D.O., Gattaz W.F., Rigonatti S.P., Rosa M.A., Fregni F., Rosa M.O., et al. Transcranial magnetic stimulation accelerates the antidepressant effect of amitriptyline in severe depression: a double-blind placebo-controlled study. Biol Psychiatry 57 (2005) 162-166
99. Siebner H.R., Mentschel C., Auer C., and Conrad B. Repetitive transcranial magnetic stimulation has a beneficial effect on bradykinesia in Parkinson's disease. Neuroreport 10 (1999) 589-594
100. Siebner H.R., Tormos J.M., Ceballos-Baumann A.O., Auer C., Catala M.D., Conrad B., et al. Low-frequency repetitive transcranial magnetic stimulation of the motor cortex in writer's cramp. Neurology 52 (1999) 529-537
101. Siebner H.R., Filipovic S.R., Rowe J.B., Cordivari C., Gerschlager W., Rothwell J.C., et al. Patients with focal arm dystonia have increased sensitivity to slow-frequency repetitive TMS of the dorsal premotor cortex. Brain 126 (2003) 2710-2725
102. Siebner H.R., Lang N., Rizzo V., Nitsche M.A., Paulus W., Lemon R.N., et al. Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J Neurosci 24 (2004) 3379-3385
103. Sommer M., Tergau F., Wischer S., and Paulus W. Paired-pulse repetitive transcranial magnetic stimulation of the human motor cortex. Exp Brain Res 139 (2001) 465-472
104. Stefan K., Kunesch E., Cohen L.G., Benecke R., and Classen J. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 123 (2000) 572-584
105. Stefan K., Wycislo M., and Classen J. Modulation of associative human motor cortical plasticity by attention. J Neurophysiol 92 (2004) 66-72
106. Tergau F., Naumann U., Paulus W., and Steinhoff B.J. Low-frequency repetitive transcranial magnetic stimulation improves intractable epilepsy. Lancet 353 (1999) 2209
107. Thickbroom G.W., Byrnes M.L., Edwards D.J., and Mastaglia F.L. Repetitive paired-pulse TMS at I-wave periodicity markedly increases corticospinal excitability: a new technique for modulating synaptic plasticity. Clin Neurophysiol 117 (2006) 61-66
108. Tsubokawa T., Katayama Y., Yamamoto T., Hirayama T., and Koyama S. Chronic motor cortex stimulation for the treatment of central pain. Acta Neurochir Suppl (Wien) 52 (1991) 137-139
109. Turrigiano G.G., and Nelson S.B. Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5 (2004) 97-107
110. Ueki Y., Mima T., Kotb M.A., Sawada H., Saiki H., Ikeda A., et al. Altered plasticity of the human motor cortex in Parkinson's disease. Ann Neurol 59 (2006) 60-71
111. Ziemann U., Hallett M., and Cohen L.G. Mechanisms of deafferentation-induced plasticity in human motor cortex. J Neurosci 18 (1998) 7000-7007
112. Ziemann U., Tam A., Butefisch C., and Cohen L.G. Dual modulating effects of amphetamine on neuronal excitability and stimulation-induced plasticity in human motor cortex. Clin Neurophysiol 113 (2002) 1308-1315
113. Ziemann U., Ilic T.V., Pauli C., Meintzschel F., and Ruge D. Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J Neurosci 24 (2004) 1666-1672