Brain Topography

, Volume 22, Issue 4, pp 294–306

Mechanisms and Applications of Theta-burst rTMS on the Human Motor Cortex

  • Lizbeth Cárdenas-Morales
  • Dennis A. Nowak
  • Thomas Kammer
  • Robert C. Wolf
  • Carlos Schönfeldt-Lecuona
Review

Abstract

Theta-burst Stimulation (TBS) is a novel form of repetitive transcranial magnetic stimulation (rTMS). Applied over the primary motor cortex it has been successfully used to induce changes in cortical excitability. The advantage of this stimulation paradigm is that it is able to induce strong and long lasting effects using a lower stimulation intensity and a shorter time of stimulation compared to conventional rTMS protocols. Since its first description, TBS has been used in both basic and clinical research in the last years and more recently it has been expanded to other domains than the motor system. Its capacity to induce synaptic plasticity could lead to therapeutic implications for neuropsychiatric disorders. The neurobiological mechanisms of TBS are not fully understood at present; they may involve long-term potentiation (LTP)- and depression (LTD)-like processes, as well as inhibitory mechanisms modulated by GABAergic activity. This article highlights current hypotheses regarding the mechanisms of action of TBS and some central factors which may influence cortical responses to TBS. Furthermore, previous and ongoing research performed in the field of TBS on the motor cortex is summarized.

Keywords

Cortical excitability Synaptic plasticity Long-term potentiation Depression 

References

  1. Abraham WC, Bear MF (1996) Metaplasticity: the plasticity of synaptic plasticity. Trends Neurosci 19:126–130CrossRefPubMedGoogle Scholar
  2. Aleman A, Sommer IE, Kahn RS (2007) Efficacy of slow repetitive transcranial magnetic stimulation in the treatment of resistant auditory hallucinations in schizophrenia: a meta-analysis. J Clin Psychiatry 68:416–421CrossRefPubMedGoogle Scholar
  3. Allen SJ, Dawbarn D (2006) Clinical relevance of the neurotrophins and their receptors. Clin Sci (Lond) 110:175–191CrossRefGoogle Scholar
  4. Angelucci F, Oliviero A, Pilato F, Saturno E, Dileone M, Versace V, Musumeci G, Batocchi AP, Tonali PA, Di Lazzaro V (2004) Transcranial magnetic stimulation and BDNF plasma levels in amyotrophic lateral sclerosis. Neuroreport 15:717–720CrossRefPubMedGoogle Scholar
  5. Artola A, Singer W (1993) Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci 16:480–487CrossRefPubMedGoogle Scholar
  6. Aydin-Abidin S, Trippe J, Funke K, Eysel UT, Benali A (2008) High- and low-frequency repetitive transcranial magnetic stimulation differentially activates c-Fos and zif268 protein expression in the rat brain. Exp Brain Res 188:249–261Google Scholar
  7. Bliss TV, Gardner-Medwin AR (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J Physiol 232:357–374PubMedGoogle Scholar
  8. Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J Physiol 232:331–356PubMedGoogle Scholar
  9. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313:1626–1628CrossRefPubMedGoogle Scholar
  10. Cárdenas-Morales L, Grön G, Kammer T (2008) Exploring the effects of theta burst stimulation: an off-line combination of transcranial magnetic stimulation and functional magnetic resonance imaging. In: George MS (ed) Third international conference on TMS and tDCS October 1–4. Brain Stimulation, Göttingen, Germany, p 248Google Scholar
  11. Centonze D, Koch G, Versace V, Mori F, Rossi S, Brusa L, Grossi K, Torelli F, Prosperetti C, Cervellino A, Marfia GA, Stanzione P, Marciani MG, Boffa L, Bernardi G (2007) Repetitive transcranial magnetic stimulation of the motor cortex ameliorates spasticity in multiple sclerosis. Neurology 68:1045–1050CrossRefPubMedGoogle Scholar
  12. Cheeran B, Talelli P, Mori F, Koch G, Suppa A, Edwards MJ, Houlden H, Bhatia K, Greenwood R, Rothwell JC (2008) A common polymorphism in the brain derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. J Physiol 586:5717–5725Google Scholar
  13. 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 48:1398–1403PubMedGoogle Scholar
  14. Codecà C, Mori F, Kusayanagi H, Monteleone F, Centonze D, Koch G (2008) iTBS of Primary motor cortex improves spasticity in MS patients. In: George MS (ed) Third international conference on TMS and tDCS, October 1–4. Brain Stimulation, Göttingen, Germany, p 267Google Scholar
  15. Conte A, Gilio F, Iacovelli E, Bettolo CM, Di Bonaventura C, Frasca V, Carbone A, Prencipe M, Berardelli A, Inghilleri M (2007) Effects of repetitive transcranial magnetic stimulation on spike-and-wave discharges. Neurosci Res 57:140–142CrossRefPubMedGoogle Scholar
  16. Cordes J, Arends M, Mobascher A, Brinkmeyer J, Kornischka J, Eichhammer P, Klimke A, Winterer G, Agelink MW (2006) Potential clinical targets of repetitive transcranial magnetic stimulation treatment in schizophrenia. Neuropsychobiol 54:87–99CrossRefGoogle Scholar
  17. Corona JC, Tovar-y-Romo LB, Tapia R (2007) Glutamate excitotoxicity and therapeutic targets for amyotrophic lateral sclerosis. Exp Opin Therap Targets 11:1415–1428CrossRefGoogle Scholar
  18. Dafotakis M, Grefkes C, Eickhoff SB, Karbe H, Fink GR, Nowak DA (2008) Effects of rTMS on grip force control following subcortical stroke. Exp Neurol 211:407–412CrossRefPubMedGoogle Scholar
  19. Daskalakis ZJ, Möller B, Christensen BK, Fitzgerald PB, Gunraj C, Chen R (2006) The effects of repetitive transcranial magnetic stimulation on cortical inhibition in healthy human subjects. Exp Brain Res 174:403–412CrossRefPubMedGoogle Scholar
  20. Davies CH, Starkey SJ, Pozza MF, Collingridge GL (1991) GABA autoreceptors regulate the induction of LTP. Nature 349:609–611CrossRefPubMedGoogle Scholar
  21. Di Lazzaro V, Oliviero A, Saturno E, Pilato F, Dileone M, Sabatelli M, Tonali P (2004) Motor cortex stimulation for amyotrophic lateral sclerosis. Time for a therapeutic trial? Clin Neurophysiol 115:1479–1485CrossRefPubMedGoogle Scholar
  22. Di Lazzaro V, Pilato F, Saturno E, Oliviero A, Dileone M, Mazzone P, Insola A, Tonali PA, Ranieri F, Huang YZ, Rothwell JC (2005) Theta-burst repetitive transcranial magnetic stimulation suppresses specific excitatory circuits in the human motor cortex. J Physiol 565:945–950CrossRefPubMedGoogle Scholar
  23. Di Lazzaro V, Dileone M, Pilato F, Profice P, Ranieri F, Musumeci G, Angelucci F, Sabatelli M, Tonali PA (2006a) Repetitive transcranial magnetic stimulation for ALS—a preliminary controlled study. Neurosci Lett 408:135–140CrossRefPubMedGoogle Scholar
  24. Di Lazzaro V, Dileone M, Pilato F, Tonali PA, Rothwell JC (2006b) Repetitive transcranial magnetic stimulation of the motor cortex for hemichorea. J Neurol Neurosurg Psychiatry 77:1095–1097CrossRefPubMedGoogle Scholar
  25. Di Lazzaro V, Pilato F, Dileone M, Profice P, Capone F, Ranieri F, Musumeci G, Cianfoni A, Pasqualetti P, Tonali PA (2008a) Modulating cortical excitability in acute stroke: a repetitive TMS study. Clin Neurophysiol 119:715–723CrossRefPubMedGoogle Scholar
  26. Di Lazzaro V, Pilato F, Dileone M, Profice P, Oliviero A, Mazzone P, Insola A, Ranieri F, Meglio M, Tonali PA, Rothwell JC (2008b) The physiological basis of the effects of intermittent theta burst stimulation of the human motor cortex. J Physiol 586:3871–3879Google Scholar
  27. Diamond DM, Dunwiddie TV, Rose GM (1988) Characteristics of hippocampal primed burst potentiation in vitro and in the awake rat. J Neurosci 8:4079–4088PubMedGoogle Scholar
  28. Edwards MJ, Huang YZ, Mir P, Rothwell JC, Bhatia KP (2006) Abnormalities in motor cortical plasticity differentiate manifesting and nonmanifesting DYT1 carriers. Mov Dis 21:2181–2186CrossRefGoogle Scholar
  29. Fitzgerald PB, Brown TL, Daskalakis ZJ (2002) The application of transcranial magnetic stimulation in psychiatry and neurosciences research. Acta Psychiatr Scand 105:324–340CrossRefPubMedGoogle Scholar
  30. Fitzgerald PB, Fountain S, Daskalakis ZJ (2006) A comprehensive review of the effects of rTMS on motor cortical excitability and inhibition. Clin Neurophysiol 117:2584–2596CrossRefPubMedGoogle Scholar
  31. Franca M, Koch G, Mochizuki H, Huang YZ, Rothwell JC (2006) Effects of theta burst stimulation protocols on phosphene threshold. Clin Neurophysiol 117:1808–1813CrossRefPubMedGoogle Scholar
  32. Gentner R, Wankerl K, Reinsberger C, Zeller D, Classen J (2008) Depression of human corticospinal excitability induced by magnetic theta-burst stimulation: evidence of rapid polarity-reversing metaplasticity. Cereb Cortex 18:2046–2053CrossRefPubMedGoogle Scholar
  33. Gerschlager W, Siebner HR, Rothwell JC (2001) Decreased corticospinal excitability after subthreshold 1 Hz rTMS over lateral premotor cortex. Neurology 57:449–455PubMedGoogle Scholar
  34. Gottschalk W, Pozzo-Miller LD, Figurov A, Lu B (1998) Presynaptic modulation of synaptic transmission and plasticity by brain-derived neurotrophic factor in the developing hippocampus. J Neurosci 18:6830–6839PubMedGoogle Scholar
  35. Grossheinrich N, Rau A, Pogarell O, Hennig-Fast K, Reinl MKS., Dieler A, Leicht G, Mulert C, Sterr A, Padberg F (2008) Theta burst stimulation of the prefrontal cortex: safety and impact on cognition, mood, and resting electroencephalogram. Biol Psychiatry (in press)Google Scholar
  36. Hausmann A, Weis C, Marksteiner J, Hinterhuber H, Humpel C (2000) Chronic repetitive transcranial magnetic stimulation enhances c-fos in the parietal cortex and hippocampus. Mol Brain Res 76:355–362CrossRefPubMedGoogle Scholar
  37. Herwig U, Fallgatter AJ, Höppner J, Eschweiler GW, Kron MHG, Padberg F, Naderi-Heiden A, Abler B, Eichhammer P, Grossheinrich N, Hay B, Kammer T, Langguth B, Laske C, Plewnia C, Richter MM, Schulz M, Unterecker S, Zinke A, Spitzer M, Schönfeldt-Lecuona C (2008) Antidepressant effects of augmentative transcranial magnetic stimulation: randomised multicentre trial. Br J Psychiatry 191:441–448CrossRefGoogle Scholar
  38. Hess G, Aizenman CD, Donoghue JP (1996) Conditions for the induction of long-term potentiation in layer II/III horizontal connections of the rat motor cortex. J Neurophysiol 75:1765–1778PubMedGoogle Scholar
  39. Hrabetova S, Sacktor TC (1997) Long-term potentiation and long-term depression are induced through pharmacologically distinct NMDA receptors. Neurosci Lett 226:107–110CrossRefPubMedGoogle Scholar
  40. Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45:201–206CrossRefPubMedGoogle Scholar
  41. Huang YZ, Chen RS, Rothwell JC, Wen HY (2007) The after-effect of human theta burst stimulation is NMDA receptor dependent. Clin Neurophysiol 118:1028–1032CrossRefPubMedGoogle Scholar
  42. Huang YZ, Rothwell JC, Edwards MJ, Chen RS (2008) Effect of physiological activity on an NMDA-dependent form of cortical plasticity in human. Cereb Cortex 18:563–570CrossRefPubMedGoogle Scholar
  43. Hubl D, Nyffeler T, Wurtz P, Chaves S, Pflugshaupt T, Lüthi M, von Wartburg R, Wiest R, Dierks T, Strik WK, Hess CW, Müri RM (2008) Time course of blood oxygenation level-dependent signal response after theta burst transcranial magnetic stimulation of the frontal eye field. Neuroscience 151:921–928CrossRefPubMedGoogle Scholar
  44. Hummel FC, Cohen LG (2006) Non-invasive brain stimulation: a new strategy to improve neurorehabilitation after stroke. Lancet Neurol 5:708–712CrossRefPubMedGoogle Scholar
  45. Iezzi E, Conte A, Suppa A, Agostino R, Dinapoli L, Scontrini A, Berardelli A (2008) Phasic voluntary movements reverse the after-effects of subsequent theta-burst stimulation in humans. J Neurophysiol 100:2070–2076Google Scholar
  46. Ishikawa S, Matsunaga K, Nakanishi R, Kawahira K, Murayama N, Tsuji S, Huang YZ, Rothwell JC (2007) Effect of theta burst stimulation over the human sensorimotor cortex on motor and somatosensory evoked potentials. Clin Neurophysiol 118:1033–1043CrossRefPubMedGoogle Scholar
  47. Joo EY, Han SJ, Chung SH, Cho JW, Seo DW, Hong SB (2007) Antiepileptic effects of low-frequency repetitive transcranial magnetic stimulation by different stimulation durations and locations. Clin Neurophysiol 118:702–708CrossRefPubMedGoogle Scholar
  48. Kahana MJ (2006) The cognitive correlates of human brain oscillations. J Neurosci 26:1669–1672CrossRefPubMedGoogle Scholar
  49. Kammer T, Beck S, Thielscher A, Laubis-Herrmann U, Topka H (2001) Motor thresholds in humans: a transcranial magnetic stimulation study comparing different pulse waveforms, current directions and stimulator types. Clin Neurophysiol 112:250–258CrossRefPubMedGoogle Scholar
  50. Karege F, Perret G, Bondolfi G, Schwald M, Bertschy G, Aubry JM (2002) Decreased serum brain-derived neurotrophic factor levels in major depressed patients. Psychiatry Res 109:143–148CrossRefPubMedGoogle Scholar
  51. Khedr EM, Rothwell JC, Shawky OA, Ahmed MA, Foly N, Hamdy A (2007) Dopamine levels after repetitive transcranial magnetic stimulation of motor cortex in patients with Parkinson’s disease: preliminary results. Mov Dis 22:1046–1050CrossRefGoogle Scholar
  52. Kleim JA, Chan S, Pringle E, Schallert K, Procaccio V, Jimenez R, Cramer SC (2006) BDNF val66met polymorphism is associated with modified experience-dependent plasticity in human motor cortex. Nat Neurosci 9:735–737CrossRefPubMedGoogle Scholar
  53. Klein E, Chistyakov A (2008) Antidepressant effect of theta-burst rTMS. ClinicalTrialsgov. http://clinicaltrials.gov/ct2/show/NCT00515658
  54. Klintsova AY, Dickson E, Yoshida R, Greenough WT (2004) Altered expression of BDNF and its high-affinity receptor TrkB in response to complex motor learning and moderate exercise. Brain Res 1028:92–104CrossRefPubMedGoogle Scholar
  55. 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 471:501–519PubMedGoogle Scholar
  56. Lang UE, Hellweg R, Gallinat J, Bajbouj M (2007) Acute prefrontal cortex transcranial magnetic stimulation in healthy volunteers: no effects on brain-derived neurotrophic factor (BDNF) concentrations in serum. J Affect Disord 107:255–258CrossRefPubMedGoogle Scholar
  57. Lange R, Lee L, Weiller C, Siebner HR (2008) Theta burst stimulation triggers functional compensation within the primary motor and premotor cortex during motor skill acquisition. In: George MS (ed) Third international conference on TMS and tDCS October 1–4. Brain Stimulation, Göttingen, Germany, p 280Google Scholar
  58. Larson J, Wong D, Lynch G (1986) Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res Bull 368:347–350Google Scholar
  59. Laske C, Eschweiler GW (2006) Brain-derived neurotrophic factor: from nerve growth factor to modulator of brain plasticity in cognitive processes and psychiatric diseases. Nervenarzt 77:523–537CrossRefPubMedGoogle Scholar
  60. Lee SH, Kim W, Chung YC, Jung KH, Bahk WM, Jun TY, Kim KS, George MS, Chae JH (2005) A double blind study showing that two weeks of daily repetitive TMS over the left or right temporoparietal cortex reduces symptoms in patients with schizophrenia who are having treatment-refractory auditory hallucinations. Neurosci Lett 376:177–181CrossRefPubMedGoogle Scholar
  61. Lefaucheur J, Drouot X, Ménard-Lefaucheur I, Keravel Y, Nguyen J (2006) Motor cortex rTMS restores defective intracortical inhibition in chronic neuropathic pain. Neurology 67:1568–1574CrossRefPubMedGoogle Scholar
  62. Lisman JE, Idiart MA (1995) Storage of 7 ± 2 short-term memories in oscillatory subcycles. Science 267:1512–1515CrossRefPubMedGoogle Scholar
  63. Lomarev MP, Kim DY, Richardson SP, Voller B, Hallett M (2007) Safety study of high-frequency transcranial magnetic stimulation in patients with chronic stroke. Clin Neurophysiol 118:2072–2075CrossRefPubMedGoogle Scholar
  64. Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000) Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp Brain Res 133:125–130CrossRefGoogle Scholar
  65. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5–21CrossRefPubMedGoogle Scholar
  66. Mansur CG, Fregni F, Boggio PS, Riberto M, Gallucci-Neto J, Santos CM, Wagner T, Rigonatti SP, Marcolin MA, Pascual-Leone A (2005) A sham stimulation-controlled trial of rTMS of the unaffected hemisphere in stroke patients. Neurology 64:1802–1804CrossRefPubMedGoogle Scholar
  67. Mix A, Benali A, Eysel UT, Funke K (2008) The effect of chronic transcranial theta burst magnetic stimulation on an associative tactile learning rat in tha rat. In: George MS (ed) Third international conference on TMS ans tDCS October 1–4. Brain Stimulation, Göttingen, Germany, p 282Google Scholar
  68. 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 111:1002–1007CrossRefPubMedGoogle Scholar
  69. Mulkey RM, Malenka RC (1992) Mechanisms underlying induction of homosynaptic long-term depression in area CA1 of the hippocampus. Neuron 5:967–975CrossRefGoogle Scholar
  70. Müller MB, Toschi N, Kresse AE, Post A, Keck ME (2000) Long-term repetitive transcranial magnetic stimulation increases the expression of brain-derived neurotrophic factor and cholecystokinin mRNA, but not neuropeptide tyrosine mRNA in specific areas of rat brain. Neuropsychopharmacology 23:205–215CrossRefPubMedGoogle Scholar
  71. Nowak D, Berner J, Herrnberger B, Kammer T, Grön G, Schönfeldt-Lecuona C (2008a) Continuous theta-burst stimulation over the dorsal premotor cortex interferes with associative learning during object lifting. Cortex 45:473–482Google Scholar
  72. Nowak DA, Grefkes C, Dafotakis M, Eickhoff S, Küst J, Karbe H, Fink GR (2008b) Effects of low-frequency repetitive transcranial magnetic stimulation of the contralesional primary motor cortex on movement kinematics and neural activity in subcortical stroke. Arch Neurol 65:741–747CrossRefPubMedGoogle Scholar
  73. Nyffeler T, Wurtz P, Lüscher H, Hess C, Senn W, Pflugshaupt T, von Wartburg R, Lüthi M, Müri R (2006) Extending lifetime of plastic changes in the human brain. Eur J Neurosci 24:2961–2966CrossRefPubMedGoogle Scholar
  74. O’Reardon JP, Solvason HB, Janicak PG, Sampson S, Isenberg KE, Nahas Z, McDonald W, Avery D, Fitzgerald PB, Loo C, Demitrack MA, George MS, Sackeim HA (2007) Efficacy and safety of transcranial magnetic stimulation in the acute treatment of major depression: a multisite randomized controlled trial. Biol Psychiatry 62:1208–1216CrossRefPubMedGoogle Scholar
  75. Pascual-Leone A, Valls-Solé J, Wassermann EM, Hallett M (1994) Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117:847–858CrossRefPubMedGoogle Scholar
  76. Pascual-Leone A, Tormos JM, Keenan J, Tarazona F, Cañete C, Catalá MD (1998) Study and modulation of human cortical excitability with transcranial magnetic stimulation. J Clin Neurophysiol 15:333–343CrossRefPubMedGoogle Scholar
  77. Paulus W (2005) Toward establishing a therapeutic window for rTMS by theta burst stimulation [comment]. Neuron 45:181–183CrossRefPubMedGoogle Scholar
  78. Peinemann A, Lehner C, Mentschel C, Munchau A, Conrad B, Siebner HR (2000) Subthreshold 5-Hz repetitive transcranial magnetic stimulation of the human primary motor cortex reduces intracortical paired-pulse inhibition. Neurosci Lett 296:21–24CrossRefPubMedGoogle Scholar
  79. Plewnia C, Reimold M, Najib A, Reischl G, Plontke SK, Gerloff C (2007) Moderate therapeutic efficacy of positron emission tomography-navigated repetitive transcranial magnetic stimulation for chronic tinnitus: a randomised, controlled pilot study. J Neurol Neurosurg Psychiatry 78:152–156CrossRefPubMedGoogle Scholar
  80. Plewnia C, Rilk AJ, Soekadar SR, Arfeller C (2008) Safety and effectiveness of repetitive transcranial magnetic stimulation in the treatment of tinnitus. ClinicalTrialsgov. http://clinicaltrials.gov/ct2/show/NCT00518024
  81. Poreisz C, Csifcsák G, Antal A, Levold M, Hillers F, Paulus W (2008) Theta burst stimulation of the motor cortex reduces laser-evoked pain perception. Neuroreport 19:193–196CrossRefPubMedGoogle Scholar
  82. Quartarone A, Siebner HR, Rothwell JC (2006) Task-specific hand dystonia: can too much plasticity be bad for you? Trends Neurosci 29:192–199CrossRefPubMedGoogle Scholar
  83. Ridding MC, Rothwell JC (2007) Perspectives—opinion—is there a future for therapeutic use of transcranial magnetic stimulation? Nat Rev Neurosci 8:559–567CrossRefPubMedGoogle Scholar
  84. Rossi S, De Capua A, Ulivelli M, Bartalini S, Falzarano V, Filippone G, Passero S (2007) Effects of repetitive transcranial magnetic stimulation on chronic tinnitus: a randomised, crossover, double blind, placebo controlled study. J Neurol Neurosurg Psychiatry 78:857–863CrossRefPubMedGoogle Scholar
  85. Rossini PM, Rossi S (2007) Transcranial magnetic stimulation—diagnostic, therapeutic, and research potential. Neurology 68:484–488CrossRefPubMedGoogle Scholar
  86. Rothwell JC, Thompson PD, Day BL, Boyd S, Marsden CD (1991) Stimulation of the human motor cortex through the scalp. Exp Physiol 76:159–200PubMedGoogle Scholar
  87. Schindler K, Nyffeler T, Wiest R, Hauf M, Mathis J, Hess C, Müri R (2008) Theta burst transcranial magnetic stimulation is associated with increased EEG synchronization in the stimulated relative to unstimulated cerebral hemisphere. Neurosci Lett 436:31–34CrossRefPubMedGoogle Scholar
  88. Schönfeldt-Lecuona C, Connemann BJ, Viviani R, Spitzer M, Herwig U (2006) Transcranial magnetic stimulation in motor conversion disorder: a short case series. J Clin Neurophysiol 23:472–475PubMedGoogle Scholar
  89. Schwenkreis P, Witscher K, Pleger B, Malin JP, Tegenthoff M (2005) The NMDA antagonist memantine affects training induced motor cortex plasticity—a study using transcranial magnetic stimulation. BMC Neurosci 6:35CrossRefPubMedGoogle Scholar
  90. Siebner HR, Filipovic SR, Rowe JB, Cordivari C, Gerschlager W, Rothwell J, Frackowiak RS, Bhatia KP (2003) Patients with focal arm dystonia have increased sensitivity to slow-frequency repetitive TMS of the dorsal premotor cortex. Brain 126:2710–2725CrossRefPubMedGoogle Scholar
  91. Siebner HR, Lang N, Rizzo V, Nitsche MA, Paulus W, Lemon RN, Rothwell JC (2004) Preconditioning of low-frequency repetitive transcranial magnetic stimulation with transcranial direct current stimulation: evidence for homeostatic plasticity in the human motor cortex. J Neurosci 24:3379–3385CrossRefPubMedGoogle Scholar
  92. Smith JA, Mennemeier M, Bartel T, Chelette KC, Kimbrell T, Triggs W, Dornhoffer JL (2007) Repetitive transcranial magnetic stimulation for tinnitus: a pilot study. Laryngoscope 117:529–534CrossRefPubMedGoogle Scholar
  93. Stefan K, Gentner R, Zeller D, Dang S, Classen J (2008) Theta-burst stimulation: remote physiological and local behavioral after-effects. Neuroimage 40:265–274CrossRefPubMedGoogle Scholar
  94. Suppa A, Ortu E, Zafar N, Deriu F, Paulus W, Berardelli A, Rothwell JC (2008) Theta burst stimulation induces after-effects on contralateral primary motor cortex excitability in humans. J Physiol 586:4489–4500CrossRefPubMedGoogle Scholar
  95. Talelli P, Cheeran BJ, Teo JTH, Rothwell JC (2007a) Pattern-specific role of the current orientation used to deliver Theta Burst Stimulation. Clin Neurophysiol 118:1815–1823CrossRefPubMedGoogle Scholar
  96. Talelli P, Greenwood RJ, Rothwell JC (2007b) Exploring Theta Burst Stimulation as an intervention to improve motor recovery in chronic stroke. Clin Neurophysiol 118:333–342CrossRefPubMedGoogle Scholar
  97. Teo JTH, Swayne OB, Rothwell JC (2007) Further evidence for NMDA-dependence of the after-effects of human theta burst stimulation. Clin Neurophysiol 118:1649–1651CrossRefPubMedGoogle Scholar
  98. Tergau F, Naumann U, Paulus W, Steinhoff BJ (1999) Low-frequency repetitive transcranial magnetic stimulation improves intractable epilepsy. Lancet 353:2209CrossRefPubMedGoogle Scholar
  99. Thickbroom GW (2007) Transcranial magnetic stimulation and synaptic plasticity: experimental framework and human models. Exp Brain Res 180:583–593CrossRefPubMedGoogle Scholar
  100. 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 112:2138–2145CrossRefPubMedGoogle Scholar
  101. Turrigiano GG, Leslie KR, Desai NS, Rutherford LC, Nelson SB (1998) Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391:845–846CrossRefGoogle Scholar
  102. Wassermann, EM, Grafman J, Berry C, Hollnagel C, Wild K, Clark K, Hallet M (1996) Use and safety of a new repetitive transcranial magnetic stimulator. Electroencephalogr Clin Neurophysiol 101:412–417Google Scholar
  103. Wu T, Sommer M, Tergau F, Paulus W (2000) Lasting influence of repetitive transcranial magnetic stimulation on intracortical excitability in human subjects. Neurosci Lett 287:37–40CrossRefPubMedGoogle Scholar
  104. Zafar N, Paulus W, Sommer M (2008) Comparative assessment of best conventional with best theta burst repetitive transcranial magnetic stimulation protocols on human motor cortex excitability. Clin Neurophysiol 119:1393–1399CrossRefPubMedGoogle Scholar
  105. Ziemann U (1999) Intracortical inhibition and facilitation in the conventional paired TMS paradigm. Electroenceph Clin Neurophysiol Suppl 51:127–136Google Scholar
  106. Ziemann U, Lönnecker S, Steinhoff BJ, Paulus W (1996) Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 40:344–345CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Lizbeth Cárdenas-Morales
    • 1
  • Dennis A. Nowak
    • 2
  • Thomas Kammer
    • 1
  • Robert C. Wolf
    • 1
  • Carlos Schönfeldt-Lecuona
    • 1
  1. 1.Department of Psychiatry and Psychotherapy IIIUniversity Clinic UlmUlmGermany
  2. 2.Department of NeurologyUniversity of CologneCologneGermany

Personalised recommendations