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Effects of Repetitive Transcranial Magnetic Stimulation on Spike Pattern and Topography in Patients with Focal Epilepsy

Abstract

Repetitive Transcranial Magnetic Stimulation (rTMS) is a non-invasive method for brain stimulation. Group-studies applying rTMS in epilepsy patients aiming to decrease epileptic spike- or seizure-frequency have led to inconsistent results. Here we studied whether therapeutic trains of rTMS have detectable effects on individual spike pattern and/or frequency in patients suffering from focal epilepsy. Five patients with focal epilepsy underwent one session of rTMS online with EEG using a 6 Hz prime/1 Hz rTMS protocol (real and sham). The EEG was recorded continuously throughout the stimulation, and the epileptic spikes recorded immediately before (baseline) and after stimulation (sham and real) were subjected to further analysis. Number of spikes, spike-strength and spike-topography were examined. In two of the five patients, real TMS led to significant changes when compared to baseline and sham (decrease in spike-count in one patient, change in topography of the after-discharge in the other patient). Spike-count and topography remained unchanged the remaining patients. Overall, our results do not indicate a consistent effect of rTMS stimulation on interictal spike discharges, but speak in favor of a rather weak and individually variable immediate effect of rTMS on focal epileptic activity. The individuation of most effective stimulation patterns will be decisive for the future role of rTMS in epilepsies and needs to be determined in larger studies.

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References

  • Bae EH, Schrader LM, Machii K, Alonso-Alonso M, Riviello JJ Jr, Pascual-Leone A, Rotenberg A (2007) Safety and tolerability of repetitive transcranial magnetic stimulation in patients with epilepsy: a review of the literature. Epilepsy Behav 10(4):521–528

    Article  PubMed  Google Scholar 

  • Barker AT, Jalinous R, Freeston IL (1985) Non-invasive magnetic stimulation of human motor cortex. Lancet 1(8437):1106–1107

    Article  CAS  PubMed  Google Scholar 

  • Bohotin V, Fumal A, Vandenheede M, Gerard P, Bohotin C, Maertens de Noordhout A, Schoenen J (2002) Effects of repetitive transcranial magnetic stimulation on visual evoked potentials in migraine. Brain 125(Pt 4):912–922

    Article  CAS  PubMed  Google Scholar 

  • Cantello R, Rossi S, Varrasi C, Ulivelli M, Civardi C, Bartalini S, Vatti G, Cincotta M, Borgheresi A, Zaccara G, Quartarone A, Crupi D, Lagana A, Inghilleri M, Giallonardo AT, Berardelli A, Pacifici L, Ferreri F, Tombini M, Gilio F, Quarato P, Conte A, Manganotti P, Bongiovanni LG, Monaco F, Ferrante D, Rossini PM (2007) Slow repetitive TMS for drug-resistant epilepsy: clinical and EEG findings of a placebo-controlled trial. Epilepsia 48:366–374

    Article  PubMed  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(5):1398–1403

    CAS  PubMed  Google Scholar 

  • 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(1):140–142

    Article  PubMed  Google Scholar 

  • Daniele O, Brighina F, Piazza A, Giglia G, Scalia S, Fierro B (2003) Low-frequency transcranial magnetic stimulation in patients with cortical dysplasia––a preliminary study. J Neurol 250(6):761–762

    Article  PubMed  Google Scholar 

  • De Santis L, Clarke S, Murray MM (2007) Automatic and intrinsic auditory “what” and “where” processing in humans revealed by electrical neuroimaging. Cereb Cortex 17(1):9–17

    Article  PubMed  Google Scholar 

  • Enomoto H, Ugawa Y, Hanajima R, Yuasa K, Mochizuki H, Terao Y, Shiio Y, Furubayashi T, Iwata NK, Kanazawa I (2001) Decreased sensory cortical excitability after 1 Hz rTMS over the ipsilateral primary motor cortex. Clin Neurophysiol 112(11):2154–2158

    Article  CAS  PubMed  Google Scholar 

  • Esser SK, Huber R, Massimini M, Peterson MJ, Ferrarelli F, Tononi GA (2006) Direct demonstration of cortical LTP in humans: a combined TMS/EEG study. Brain Res Bull 69(1):86–94

    Article  CAS  PubMed  Google Scholar 

  • Fregni F, Schachter SC, Pascual-Leone A (2005a) Transcranial magnetic stimulation treatment for epilepsy: can it also improve depression and vice versa? Epilepsy Behav 7(2):182–189

    Article  PubMed  Google Scholar 

  • Fregni F, Thome-Souza S, Bermpohl F, Marcolin MA, Herzog A, Pascual-Leone A, Valente KD (2005b) Antiepileptic effects of repetitive transcranial magnetic stimulation in patients with cortical malformations: an EEG and clinical study. Stereotact Funct Neurosurg 83(2–3):57–62

    Article  PubMed  Google Scholar 

  • Fregni F, Boggio PS, Valle AC, Otachi P, Thut G, Rigonatti SP, Marcolin MA, Fecteau S, Pascual-Leone A, Fiore L, Valente K (2006a) Homeostatic effects of plasma valproate levels on corticospinal excitability changes induced by 1 Hz rTMS in patients with juvenile myoclonic epilepsy. Clin Neurophysiol 117(6):1217–1227

    Article  CAS  PubMed  Google Scholar 

  • Fregni F, Otachi PT, Do Valle A, Boggio PS, Thut G, Rigonatti SP, Pascual-Leone A, Valente KD (2006b) A randomized clinical trial of repetitive transcranial magnetic stimulation in patients with refractory epilepsy. Ann Neurol 60(4):447–455

    Article  PubMed  Google Scholar 

  • Fumal A, Bohotin V, Vandenheede M, Seidel L, de Pasqua V, de Noordhout J, Schoenen AM (2003) Effects of repetitive transcranial magnetic stimulation on visual evoked potentials: new insights in healthy subjects. Exp Brain Res 150(3):332–340

    PubMed  Google Scholar 

  • Guthrie D, Buchwald JS (1991) Significance testing of difference potentials. Psychophysiology 28(2):240–244

    Article  CAS  PubMed  Google Scholar 

  • Hallett M (2000) Transcranial magnetic stimulation and the human brain. Nature 406(6792):147–150

    Article  CAS  PubMed  Google Scholar 

  • Huang YZ, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC (2005) Theta burst stimulation of the human motor cortex. Neuron 45(2):201–206

    Article  CAS  PubMed  Google Scholar 

  • Iyer MB, Schleper N, Wassermann EM (2003) Priming stimulation enhances the depressant effect of low-frequency repetitive transcranial magnetic stimulation. J Neurosci 23(34):10867–10872

    CAS  PubMed  Google Scholar 

  • 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(3):702–708

    Article  PubMed  Google Scholar 

  • Kahkonen S, Komssi S, Wilenius J, Ilmoniemi RJ (2005) Prefrontal transcranial magnetic stimulation produces intensity-dependent EEG responses in humans. Neuroimage 24(4):955–960

    Article  CAS  PubMed  Google Scholar 

  • Kinoshita M, Ikeda A, Begum T, Yamamoto J, Hitomi T, Shibasaki H (2005) Low-frequency repetitive transcranial magnetic stimulation for seizure suppression in patients with extratemporal lobe epilepsy-a pilot study. Seizure 14(6):387–392

    PubMed  Google Scholar 

  • Kobayashi M, Pascual-Leone A (2003) Transcranial magnetic stimulation in neurology. Lancet Neurol 2(3):145–156

    Article  PubMed  Google Scholar 

  • Koenig T, Gianotti LRR (2009) Scalp field maps and their characterization. In: Michel CM, Koenig T, Brandeis D, Gianotti LRR, Wackermann J (eds) Electrical neuroimaging. Cambridge University Press, Cambridge, pp 25–48

  • Komssi S, Aronen HJ, Huttunen J, Kesaniemi M, Soinne L, Nikouline VV, Ollikainen M, Roine RO, Karhu J, Savolainen S, Ilmoniemi RJ (2002) Ipsi- and contralateral EEG reactions to transcranial magnetic stimulation. Clin Neurophysiol 113(2):175–184

    Article  PubMed  Google Scholar 

  • Lang N, Siebner HR, Ernst D, Nitsche MA, Paulus W, Lemon RN, Rothwell JC (2004) 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(9):634–639

    Article  PubMed  Google Scholar 

  • Lantz G, Michel CM, Seeck M, Blanke O, Spinelli L, Thut G, Landis T, Rosen I (2001) Space-oriented segmentation and 3-dimensional source reconstruction of ictal EEG patterns. Clin Neurophysiol 112(4):688–697

    Article  CAS  PubMed  Google Scholar 

  • Lantz G, Spinelli L, Seeck M, de Peralta Menendez RG, Sottas CC, Michel CM (2003) Propagation of interictal epileptiform activity can lead to erroneous source localizations: a 128-channel EEG mapping study. J Clin Neurophysiol 20(5):311–319

    Article  PubMed  Google Scholar 

  • Lehmann D, Skrandies W (1980) Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephalogr Clin Neurophysiol 48(6):609–621

    Article  CAS  PubMed  Google Scholar 

  • Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A (2000) Modulation of corticospinal excitability by repetitive transcranial magnetic stimulation. Clin Neurophysiol 111(5):800–805

    Article  CAS  PubMed  Google Scholar 

  • Menkes DL, Gruenthal M (2000) Slow-frequency repetitive transcranial magnetic stimulation in a patient with focal cortical dysplasia. Epilepsia 41(2):240–242

    Article  CAS  PubMed  Google Scholar 

  • Michel CM, Thut G, Morand S, Khateb A, Pegna AJ, de Grave Peralta R, de Gonzalez S, Seeck M, Landis T (2001) Electric source imaging of human brain functions. Brain Res Brain Res Rev 36(2–3):108–118

    Article  CAS  PubMed  Google Scholar 

  • Michel CM, Murray MM, Lantz G, Gonzalez S, Spinelli L, Grave de Peralta R (2004) EEG source imaging. Clin Neurophysiol 115(10):2195–2222

    Article  PubMed  Google Scholar 

  • Michel CM, Brandeis D, Koenig T (2009) Electrical neuroimaging in the time domain. In Michel CM, Koenig T, Brandeis D, Gianotti LRR, Wackermann J (eds) Electrical neuroimaging. Cambridge University Press, Cambridge

  • Misawa S, Kuwabara S, Shibuya K, Mamada K, Hattori T (2005) Low-frequency transcranial magnetic stimulation for epilepsia partialis continua due to cortical dysplasia. J Neurol Sci 234(1–2):37–39

    Article  PubMed  Google Scholar 

  • Murray MM, Brunet D, Michel CM (2008) Topographic ERP analyses: a step-by-step tutorial review. Brain Topogr 20(4):249–264

    Article  PubMed  Google Scholar 

  • Nyffeler T, Cazzoli D, Wurtz P, Luthi M, von Wartburg R, Chaves S, Deruaz A, Hess CW, Muri RM (2008) Neglect-like visual exploration behaviour after theta burst transcranial magnetic stimulation of the right posterior parietal cortex. Eur J Neurosci 27(7):1809–1813

    Article  PubMed  Google Scholar 

  • Pascual-Leone A, Valls-Sole J, Wassermann EM, Hallett M (1994) Responses to rapid-rate transcranial magnetic stimulation of the human motor cortex. Brain 117(4):847–858

    Article  PubMed  Google Scholar 

  • Pascual-Marqui RD, Michel CM, Lehmann D (1995) Segmentation of brain electrical activity into microstates: model estimation and validation. IEEE Trans Biomed Eng 42(7):658–665

    Article  CAS  PubMed  Google Scholar 

  • Pourtois G, Thut G, Grave de Peralta R, Michel C, Vuilleumier P (2005) Two electrophysiological stages of spatial orienting towards fearful faces: early temporo-parietal activation preceding gain control in extrastriate visual cortex. Neuroimage 26(1):149–163

    Article  PubMed  Google Scholar 

  • Santiago-Rodriguez E, Cardenas-Morales L, Harmony T, Fernandez-Bouzas A, Porras-Kattz E, Hernandez A (2008) Repetitive transcranial magnetic stimulation decreases the number of seizures in patients with focal neocortical epilepsy. Seizure

  • Schutter DJ, van Honk J (2003) Reductions in CI amplitude after repetitive transcranial magnetic stimulation(rTMS) over the striate cortex. Brain Res Cogn Brain Res 16(3):488–491

    Article  PubMed  Google Scholar 

  • 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(13):3379–3385

    Article  CAS  PubMed  Google Scholar 

  • Silvanto J, Pascual-Leone A (2008) State-dependency of transcranial magnetic stimulation. Brain Topogr 21(1):1–10

    Article  PubMed  Google Scholar 

  • Tergau F, Naumann U, Paulus W, Steinhoff BJ (1999) Low-frequency repetitive transcranial magnetic stimulation improves intractable epilepsy. Lancet 353(9171):2209

    Article  CAS  PubMed  Google Scholar 

  • Tergau F, Neumann D, Rosenow F, Nitsche MA, Paulus W, Steinhoff B (2003) Can epilepsies be improved by repetitive transcranial magnetic stimulation?––interim analysis of a controlled study. Suppl Clin Neurophysiol 56:400–405

    Article  PubMed  Google Scholar 

  • Theodore WH (2003) Transcranial magnetic stimulation in epilepsy. Epilepsy Curr 3(6):191–197

    Article  PubMed  Google Scholar 

  • Theodore WH, Hunter K, Chen R, Vega-Bermudez F, Boroojerdi B, Reeves-Tyer P, Werhahn K, Kelley KR, Cohen L (2002) Transcranial magnetic stimulation for the treatment of seizures: a controlled study. Neurology 59(4):560–562

    CAS  PubMed  Google Scholar 

  • Thut G, Theoret H, Pfennig A, Ives J, Kampmann F, Northoff G, Pascual-Leone A (2003) Differential effects of low-frequency rTMS at the occipital pole on visual-induced alpha desynchronization and visual-evoked potentials. Neuroimage 18(2):334–347

    Article  CAS  PubMed  Google Scholar 

  • Valentin A, Arunachalam R, Mesquita-Rodrigues A, Garcia Seoane JJ, Richardson MP, Mills KR, Alarcon G (2008) Late EEG responses triggered by transcranial magnetic stimulation(TMS) in the evaluation of focal epilepsy. Epilepsia 49(3):470–480

    Article  PubMed  Google Scholar 

  • Wagner T, Eden U, Fregni F, Valero-Cabre A, Ramos-Estebanez C, Pronio-Stelluto V, Grodzinsky A, Zahn M, Pascual-Leone A (2008) Transcranial magnetic stimulation and brain atrophy: a computer-based human brain model study. Exp Brain Res 186(4):539–550

    Article  PubMed  Google Scholar 

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Acknowledgments

The work was supported by the Swiss National Science Foundation by the grant No 320030-122073, No. 3200-113766 (M.S.), No. 3200-111783 (C.M.) and SPUM 33CM30-124089. The data were analyzed with the Cartool software (http://brainmapping.unige.ch/Cartool.htm) which is developed by Denis Brunet, from the Functional Brain Mapping Laboratory, Geneva, supported by the Center for Biomedical Imaging (CIBM), Geneva and Lausanne, Switzerland.

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Correspondence to Verena Brodbeck or Margitta Seeck.

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This is one of several papers published together in Brain Topography on the “Special Topic: TMS and EEG”

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Brodbeck, V., Thut, G., Spinelli, L. et al. Effects of Repetitive Transcranial Magnetic Stimulation on Spike Pattern and Topography in Patients with Focal Epilepsy. Brain Topogr 22, 267 (2010). https://doi.org/10.1007/s10548-009-0125-2

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  • DOI: https://doi.org/10.1007/s10548-009-0125-2

Keywords

  • Repetitive TMS
  • Epilepsy
  • Spike Pattern