Neuromuscular DiseasesNeuromuscular DiseasesНервно-мышечные болезни2222-87212413-0443Publishing House ABV Press23610.17650/2222-8721-2017-7-4-20-32LECTURES AND REVIEWSЛЕКЦИИ И ОБЗОРЫTranscranial magnetic stimulation with electroencephalography: methodology, applications for research and cilinicsТранскраниальная магнитная стимуляция с электроэнцефалографией: методология, экспериментальные и клинические возможностиNazarovaM. A.НазароваМ. А.
Russian Federation

Build. 1, 3a Krivokolennyy Pereulok, Moscow 101000, Russia

Россия, 101000 Москва, Кривоколенный переулок, 3а, корп. 1

chantante@gmail.comBlagoveschenskiyE. D.БлаговещенскийЕ. Д.
Russian Federation

Build. 1, 3a Krivokolennyy Pereulok, Moscow 101000, Russia

Россия, 101000 Москва, Кривоколенный переулок, 3а, корп. 1

NikulinV. V.НикулинВ. В.
Russian Federation

Build. 1, 3a Krivokolennyy Pereulok, Moscow 101000, Russia

Leipzig, Germany

Россия, 101000 Москва, Кривоколенный переулок, 3а, корп. 1

Германия, Лейпциг

MitinaM. V.МитинаМ. В.
Russian Federation

Build. 1, 3a Krivokolennyy Pereulok, Moscow 101000, Russia

Россия, 101000 Москва, Кривоколенный переулок, 3а, корп. 1

Centre for Cognition and Decision Making of the National Research University “Higher School of Economics”Центр нейроэкономики и когнитивных исследований Национального исследовательского университета «Высшая школа экономики»Centre for Cognition and Decision Making of the National Research University “Higher School of Economics” Max Planck Institute for Human Cognitive and Brain SciencesЦентр нейроэкономики и когнитивных исследований Национального исследовательского университета «Высшая школа экономики» Max Planck Institute for Human Cognitive and Brain Sciences110120187420321101201811012018Copyright ©; 2018, Nazarova M.A., Blagoveschenskiy E.D., Nikulin V.V., Mitina M.V.Copyright ©; 2018, Назарова М.А., Благовещенский Е.Д., Никулин В.В., Митина М.В.2018Nazarova M.A., Blagoveschenskiy E.D., Nikulin V.V., Mitina M.V.Назарова М.А., Благовещенский Е.Д., Никулин В.В., Митина М.В.https://creativecommons.org/licenses/by/4.0https://nmb.abvpress.ru/jour/article/view/236

Combined use of transcranial magnetic stimulation and electroencephalography (TMS-EEG) is a highly informative cutting edge technology which is relevant for fundamental, clinical and  translational research. Unique capabilities of TMS-EEG approach  allow to assess the functional state and connectivity of brain regions  thus opening new prospects for the evaluation of the TMS effects in  non-motor cortical areas. TMS-EEG responses have diagnostic and  prognostic potential for many neurological and mental illnesses.  Simultaneous co-registration of TMS with EEG remains a technically  sophisticated procedure and requires specialized equipment in  conjunction with application of complex data analysis techniques.  This review describes the details of TMS-EEG technique, principles of the experiment design, the shape and the reproducibility of TMS- evoked responses and applications of this promising approach both  in research and in clinics. 

Комбинированное использование транскраниальной магнитной стимуляции и электроэнцефалографии (ТМС-ЭЭГ) является современным высокоинформативным  экспериментальным подходом, который находит применение как в фундаментальных, так и  в клинических и трансляционных исследованиях. Уникальные возможности ТМС-ЭЭГ  позволяют оценивать функциональное состояние и связность областей мозга, а также  открывают новые перспективы оценки эффектов ТМС недвигательных областей коры.  Маркеры ТМС-ЭЭГ обладают диагностическим и прогностическим потенциалом в отношении  многих неврологических и психических болезней. Регистрация ЭЭГ одновременно с ТМС  остается технически сложной процедурой и требует наличия как специального  оборудования, так и примения сложных методов анализа данных. В настоящем обзоре  описаны технические особенности ТМС-ЭЭГ, принцип построения дизайна исследований, вид и  стабильность ТМС вызванного ответа на ЭЭГ, а также область применения метода ТМС-ЭЭГ.

transcranial magnetic stimulation with electroencephalographyfunctional stateconnectivity of brain regionsnon-motor cortical areasevoked motor responseтранскраниальная магнитная стимуляция с электроэнцефалографиейфункциональное состояниесвязность между областями мозганедвигательные области корывызванный моторный ответ1. Siebner H.R., Bergmann T.O., Bestmann S. et al. Consensus paper: combining transcranial stimulation with neuroimaging. Brain Stimul 2009;2(2):58–80. DOI: 10.1016/j.brs.2008.11.002. PMID: 20633405.Siebner H.R., Bergmann T.O., Bestmann S. et al. Consensus paper: combining transcranial stimulation with neuroimaging. Brain Stimul 2009;2(2):58–80. DOI: 10.1016/j.brs.2008.11.002. PMID: 20633405.2. Farzan F., Vernet M., Shafi M.M. et al. Characterizing and modulating brain circuitry through transcranial magnetic stimulation combined with electroencephalography. Front Neural Circuits 2016;10:73. DOI: 10.3389/fncir.2016.00073. PMID: 27713691.Farzan F., Vernet M., Shafi M.M. et al. Characterizing and modulating brain circuitry through transcranial magnetic stimulation combined with electroencephalography. Front Neural Circuits 2016;10:73. DOI: 10.3389/fncir.2016.00073. PMID: 27713691.3. Ilmoniemi R.J., Kicić D. Methodology for combined TMS and EEG. Brain Topogr 2010;22(4):233–48. DOI: 10.1007/s10548-009-0123-4. PMID: 20012350.Ilmoniemi R.J., Kicić D. Methodology for combined TMS and EEG. Brain Topogr 2010;22(4):233–48. DOI: 10.1007/s10548-009-0123-4. PMID: 20012350.4. Veniero D., Bortoletto M., Miniussi C. TMS-EEG co-registration: on TMS-induced artifact. Clin Neurophysiol 2009;120(7):1392–9. DOI: 10.1016/j.clinph.2009.04.023. PMID: 19535291.Veniero D., Bortoletto M., Miniussi C. TMS-EEG co-registration: on TMS-induced artifact. Clin Neurophysiol 2009;120(7):1392–9. DOI: 10.1016/j.clinph.2009.04.023. PMID: 19535291.5. Ives J.R., Rotenberg A., Poma R. et al. Electroencephalographic recording during transcranial magnetic stimulation in humans and animals. Clin Neurophysiol 2006;117(8):1870–5. DOI: 10.1016/j.clinph.2006.04.010. PMID: 16793336.Ives J.R., Rotenberg A., Poma R. et al. Electroencephalographic recording during transcranial magnetic stimulation in humans and animals. Clin Neurophysiol 2006;117(8):1870–5. DOI: 10.1016/j.clinph.2006.04.010. PMID: 16793336.6. Komssi S., Aronen H.J., Huttunen J. et al. Ipsi- and contralateral EEG reactions to transcranial magnetic stimulation. Clin Neurophysiol 2002;113(2):175–84. DOI: 10.1016/S1388-2457(01)00721-0. PMID: 11856623.Komssi S., Aronen H.J., Huttunen J. et al. Ipsi- and contralateral EEG reactions to transcranial magnetic stimulation. Clin Neurophysiol 2002;113(2):175–84. DOI: 10.1016/S1388-2457(01)00721-0. PMID: 11856623.7. Pascual-Leone A., Dhuna A., Roth B.J. et al. Risk of burns during rapid-rate magnetic stimulation in presence of electrodes. Lancet 1990;336(8724):1195–6. PMID: 1978057.Pascual-Leone A., Dhuna A., Roth B.J. et al. Risk of burns during rapid-rate magnetic stimulation in presence of electrodes. Lancet 1990;336(8724):1195–6. PMID: 1978057.8. Thut G., Ives J.R., Kampmann F. et al. A new device and protocol for combining TMS and online recordings of EEG and evoked potentials. J Neurosci Methods 2005;141(2):207–17. DOI: 10.1016/j.jneumeth.2004.06.016. PMID: 15661302.Thut G., Ives J.R., Kampmann F. et al. A new device and protocol for combining TMS and online recordings of EEG and evoked potentials. J Neurosci Methods 2005;141(2):207–17. DOI: 10.1016/j.jneumeth.2004.06.016. PMID: 15661302.9. Mäki H., Ilmoniemi R.J. EEG oscillations and magnetically evoked motor potentials reflect motor system excitability in overlapping neuronal populations. Clin Neurophysiol 2010;121(4):492–501. DOI: 10.1016/j.clinph.2009.11.078. PMID: 20093074.Mäki H., Ilmoniemi R.J. EEG oscillations and magnetically evoked motor potentials reflect motor system excitability in overlapping neuronal populations. Clin Neurophysiol 2010;121(4):492–501. DOI: 10.1016/j.clinph.2009.11.078. PMID: 20093074.10. Komssi S., Kähkönen S. The novelty value of the combined use of electroencephalography and transcranial magnetic stimulation for neuroscience research. Brain Res Rev 2006;52(1):183–92. DOI: 10.1016/j.brainresrev.2006.01.008. PMID: 16545462.Komssi S., Kähkönen S. The novelty value of the combined use of electroencephalography and transcranial magnetic stimulation for neuroscience research. Brain Res Rev 2006;52(1):183–92. DOI: 10.1016/j.brainresrev.2006.01.008. PMID: 16545462.11. Virtanen J., Ruohonen J., Näätänen R, Ilmoniemi R.J. Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation. Med Biol Eng Comput 1999;37(3):322–26. PMID: 10505382.Virtanen J., Ruohonen J., Näätänen R, Ilmoniemi R.J. Instrumentation for the measurement of electric brain responses to transcranial magnetic stimulation. Med Biol Eng Comput 1999;37(3):322–26. PMID: 10505382.12. Bonato C., Miniussi C., Rossini P.M. Transcranial magnetic stimulation and cortical evoked potentials: a TMS/EEG co-registration study. Clin Neurophysiol 2006;117(8):1699– 707. DOI: 10.1016/j.clinph.2006.05.006. PMID: 16797232.Bonato C., Miniussi C., Rossini P.M. Transcranial magnetic stimulation and cortical evoked potentials: a TMS/EEG co-registration study. Clin Neurophysiol 2006;117(8):1699– 707. DOI: 10.1016/j.clinph.2006.05.006. PMID: 16797232.13. Thut G., Northoff G., Ives J.R. et al. Effects of single-pulse transcranial magnetic stimulation (TMS) on functional brain activity: a combined event-related TMS and evoked potential study. Clin Neurophysiol 2003;114(11):2071–80. DOI: 10.1016/S1388-2457(03)00205-0. PMID: 14580605.Thut G., Northoff G., Ives J.R. et al. Effects of single-pulse transcranial magnetic stimulation (TMS) on functional brain activity: a combined event-related TMS and evoked potential study. Clin Neurophysiol 2003;114(11):2071–80. DOI: 10.1016/S1388-2457(03)00205-0. PMID: 14580605.14. Mutanen T.P., Mäki H., Ilmoniemi R.J. The effect of stimulus parameters on TMS-EEG muscle artifacts. Brain Stimul 2013;6(3):371–6. DOI: 10.1016/j.brs.2012.07.005. PMID: 22902312.Mutanen T.P., Mäki H., Ilmoniemi R.J. The effect of stimulus parameters on TMS-EEG muscle artifacts. Brain Stimul 2013;6(3):371–6. DOI: 10.1016/j.brs.2012.07.005. PMID: 22902312.15. Mutanen T.P., Kukkonen M., Nieminen J.O. et al. Recovering TMS-evoked EEG responses masked by muscle artifacts. Neuroimage 2016;139:157–66. DOI: 10.1016/j.neuroimage.2016.05.028. PMID: 27291496.Mutanen T.P., Kukkonen M., Nieminen J.O. et al. Recovering TMS-evoked EEG responses masked by muscle artifacts. Neuroimage 2016;139:157–66. DOI: 10.1016/j.neuroimage.2016.05.028. PMID: 27291496.16. Rossi S., Hallett M., Rossini P.M. et al. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 2009;120(12):2008–39. DOI: 10.1016/j.clinph.2009.08.016. PMID: 19833552.Rossi S., Hallett M., Rossini P.M. et al. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 2009;120(12):2008–39. DOI: 10.1016/j.clinph.2009.08.016. PMID: 19833552.17. Nikouline V., Ruohonen J., Ilmoniemi R.J. The role of the coil click in TMS assessed with simultaneous EEG. Clin Neurophysiol 1999;110(8):1325–8. PMID: 10454266.Nikouline V., Ruohonen J., Ilmoniemi R.J. The role of the coil click in TMS assessed with simultaneous EEG. Clin Neurophysiol 1999;110(8):1325–8. PMID: 10454266.18. Massimini M., Ferrarelli F., Huber R. et al. Breakdown of cortical effective connectivity during sleep. Science 2005;309(5744):2228–32. DOI: 10.1126/science.1117256. PMID: 16195466.Massimini M., Ferrarelli F., Huber R. et al. Breakdown of cortical effective connectivity during sleep. Science 2005;309(5744):2228–32. DOI: 10.1126/science.1117256. PMID: 16195466.19. Schlögl A., Keinrath C., Zimmermann D. et al. A fully automated correction method of EOG artifacts in EEG recordings. Clin Neurophysiol 2007;118(1):98–104. DOI: 10.1016/j.clinph.2006.09.003. PMID: 17088100.Schlögl A., Keinrath C., Zimmermann D. et al. A fully automated correction method of EOG artifacts in EEG recordings. Clin Neurophysiol 2007;118(1):98–104. DOI: 10.1016/j.clinph.2006.09.003. PMID: 17088100.20. Sekiguchi H., Takeuchi S., Kadota H. et al. TMS-induced artifacts on EEG can be reduced by rearrangement of the electrode’s lead wire before recording. Clin Neurophysiol 2011;122(5):984–90. DOI: 10.1016/j.clinph.2010.09.004. PMID: 20920887.Sekiguchi H., Takeuchi S., Kadota H. et al. TMS-induced artifacts on EEG can be reduced by rearrangement of the electrode’s lead wire before recording. Clin Neurophysiol 2011;122(5):984–90. DOI: 10.1016/j.clinph.2010.09.004. PMID: 20920887.21. Casarotto S., Romero Lauro L.J., Bellina V. et al. EEG responses to TMS are sensitive to changes in the perturbation parameters and repeatable over time. PLoS One 2010;5(4):102– 81. DOI: 10.1371/journal.pone.0010281. PMID: 20421968.Casarotto S., Romero Lauro L.J., Bellina V. et al. EEG responses to TMS are sensitive to changes in the perturbation parameters and repeatable over time. PLoS One 2010;5(4):102– 81. DOI: 10.1371/journal.pone.0010281. PMID: 20421968.22. Rossini P.M., Burke D., Chen R. et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 2015;126(6):1071–107. DOI: 10.1016/j.clinph.2015.02.001. PMID: 25797650.Rossini P.M., Burke D., Chen R. et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 2015;126(6):1071–107. DOI: 10.1016/j.clinph.2015.02.001. PMID: 25797650.23. Premoli I., Castellanos N., Rivolta D. et al. TMS-EEG signatures of GABAergic neurotransmission in the human cortex. J Neurosci 2014;34(16):5603–12. DOI: 10.1523/JNEUROSCI.5089-13.2014. PMID: 24741050.Premoli I., Castellanos N., Rivolta D. et al. TMS-EEG signatures of GABAergic neurotransmission in the human cortex. J Neurosci 2014;34(16):5603–12. DOI: 10.1523/JNEUROSCI.5089-13.2014. PMID: 24741050.24. Cavaleri R., Schabrun S.M., Chipchase L.S. The number of stimuli required to reliably assess corticomotor excitability and primary motor cortical representations using transcranial magnetic stimulation (TMS): a systematic review and meta-analysis. Syst Rev 2017;6(1):48. DOI: 10.1186/s13643-017-0440-8. PMID: 28264713.Cavaleri R., Schabrun S.M., Chipchase L.S. The number of stimuli required to reliably assess corticomotor excitability and primary motor cortical representations using transcranial magnetic stimulation (TMS): a systematic review and meta-analysis. Syst Rev 2017;6(1):48. DOI: 10.1186/s13643-017-0440-8. PMID: 28264713.25. Lioumis P., Kicić D., Savolainen P. et al. Reproducibility of TMS-Evoked EEG responses. Hum Brain Mapp 2009;30(4):1387–96. DOI: 10.1002/hbm.20608. PMID: 18537115.Lioumis P., Kicić D., Savolainen P. et al. Reproducibility of TMS-Evoked EEG responses. Hum Brain Mapp 2009;30(4):1387–96. DOI: 10.1002/hbm.20608. PMID: 18537115.26. Farzan F., Barr M.S., Levinson A.J. et al. Reliability of long-interval cortical inhibition in healthy human subjects: a TMS-EEG study. J Neurophysiol 2010;104(3):1339–46. DOI: 10.1152/jn.00279.2010. PMID: 20573972.Farzan F., Barr M.S., Levinson A.J. et al. Reliability of long-interval cortical inhibition in healthy human subjects: a TMS-EEG study. J Neurophysiol 2010;104(3):1339–46. DOI: 10.1152/jn.00279.2010. PMID: 20573972.27. Blankertz B., Lemm S., Treder M. et al. Single-trial analysis and classification of ERP components – a tutorial. Neuroimage 2011;56(2):814–25. DOI: 10.1016/j.neuroimage.2010.06.048. PMID: 20600976.Blankertz B., Lemm S., Treder M. et al. Single-trial analysis and classification of ERP components – a tutorial. Neuroimage 2011;56(2):814–25. DOI: 10.1016/j.neuroimage.2010.06.048. PMID: 20600976.28. Ilmoniemi R.J., Hernandez-Pavon J.C., Makela N.N. et al. Dealing with artifacts in TMS- evoked EEG. Conf Proc IEEE Eng Med Biol Soc 2015;2015:230–3. DOI: 10.1109/EMBC.2015.7318342. PMID: 26736242.Ilmoniemi R.J., Hernandez-Pavon J.C., Makela N.N. et al. Dealing with artifacts in TMS- evoked EEG. Conf Proc IEEE Eng Med Biol Soc 2015;2015:230–3. DOI: 10.1109/EMBC.2015.7318342. PMID: 26736242.29. Hernandez-Pavon J.C., Metsomaa J., Mutanen T. et al. Uncovering neural independent components from highly artifactual TMS-evoked EEG data. J Neurosci Methods 2012;209(1):144–57. DOI: 10.1016/j.jneumeth.2012.05.029. PMID: 22687937.Hernandez-Pavon J.C., Metsomaa J., Mutanen T. et al. Uncovering neural independent components from highly artifactual TMS-evoked EEG data. J Neurosci Methods 2012;209(1):144–57. DOI: 10.1016/j.jneumeth.2012.05.029. PMID: 22687937.30. Zrenner C., Belardinelli P., Müller-Dahlhaus F., Ziemann U. Closed-loop neuroscience and non-invasive brain stimulation: a tale of two loops. Front Cell Neurosci 2016;10:92. DOI: 10.3389/fncel.2016.00092. PMID: 27092055.Zrenner C., Belardinelli P., Müller-Dahlhaus F., Ziemann U. Closed-loop neuroscience and non-invasive brain stimulation: a tale of two loops. Front Cell Neurosci 2016;10:92. DOI: 10.3389/fncel.2016.00092. PMID: 27092055.31. Di Lazzaro V., Oliviero A., Pilato F. et al. The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol 2004;115(2):255–66. DOI: 10.3389/fncel.2016.00092. PMID: 14744565.Di Lazzaro V., Oliviero A., Pilato F. et al. The physiological basis of transcranial motor cortex stimulation in conscious humans. Clin Neurophysiol 2004;115(2):255–66. DOI: 10.3389/fncel.2016.00092. PMID: 14744565.32. Thielscher A., Kammer T. Electric field properties of two commercial figure-8 coils in TMS: calculation of focality and efficiency. Clin Neurophysiol 2004;115(7):1697–708. DOI: 10.1016/j.clinph.2004.02.019. PMID: 15203072.Thielscher A., Kammer T. Electric field properties of two commercial figure-8 coils in TMS: calculation of focality and efficiency. Clin Neurophysiol 2004;115(7):1697–708. DOI: 10.1016/j.clinph.2004.02.019. PMID: 15203072.33. Wagner T., Gangitano M., Romero R. et al. Intracranial measurement of current densities induced by transcranial magnetic stimulation in the human brain. Neurosci Lett 2004;354(2):91–4. DOI: 10.1016/S0304-3940(03)00861-9. PMID: 14698446.Wagner T., Gangitano M., Romero R. et al. Intracranial measurement of current densities induced by transcranial magnetic stimulation in the human brain. Neurosci Lett 2004;354(2):91–4. DOI: 10.1016/S0304-3940(03)00861-9. PMID: 14698446.34. Lazzaro V.D., Mazzone A., Saturno F. et al. Comparison of descending volleys evoked by monophasic and biphasic magnetic stimulation of the motor cortex in conscious humans. Exp Brain Res 2001;141(1):121–7. DOI: 10.1007/s002210100863. PMID: 11685416.Lazzaro V.D., Mazzone A., Saturno F. et al. Comparison of descending volleys evoked by monophasic and biphasic magnetic stimulation of the motor cortex in conscious humans. Exp Brain Res 2001;141(1):121–7. DOI: 10.1007/s002210100863. PMID: 11685416.35. Opitz A., Windhoff M., Heidemann R.M. et al. How the brain tissue shapes the electric field induced by transcranial magnetic stimulation. Neuroimage 2011;58(3):849– 59. DOI: 10.1016/j.neuroimage.2011.06.069. PMID: 21749927.Opitz A., Windhoff M., Heidemann R.M. et al. How the brain tissue shapes the electric field induced by transcranial magnetic stimulation. Neuroimage 2011;58(3):849– 59. DOI: 10.1016/j.neuroimage.2011.06.069. PMID: 21749927.36. Rosanova M., Casali A., Bellina V. et al. Natural frequencies of human corticothalamic circuits. J Neurosci 2009;29(24):7679–85. DOI: 10.1523/JNEUROSCI.0445-09.2009. PMID: 19535579.Rosanova M., Casali A., Bellina V. et al. Natural frequencies of human corticothalamic circuits. J Neurosci 2009;29(24):7679–85. DOI: 10.1523/JNEUROSCI.0445-09.2009. PMID: 19535579.37. Pfurtscheller G., Lopes da Silva F.H. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 1999;110(11):1842–57. PMID: 10576479.Pfurtscheller G., Lopes da Silva F.H. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol 1999;110(11):1842–57. PMID: 10576479.38. Romei V., Brodbeck V., Michel C. et al. Spontaneous fluctuations in posterior alpha- band EEG activity reflect variability in excitability of human visual areas. Cereb Cortex 2008;18(9):2010–8. DOI: 10.1093/cercor/bhm229. PMID: 18093905.Romei V., Brodbeck V., Michel C. et al. Spontaneous fluctuations in posterior alpha- band EEG activity reflect variability in excitability of human visual areas. Cereb Cortex 2008;18(9):2010–8. DOI: 10.1093/cercor/bhm229. PMID: 18093905.39. Nikulin V.V., Kicić D., Kähkönen S., Ilmoniemi R.J. Modulation of electroencephalographic responses to transcranial magnetic stimulation: evidence for changes in cortical excitability related to movement. Eur J Neurosci 2003;18(5):1206–12. DOI: 10.1046/j.1460- 9568.2003.02858.x. PMID: 12956719.Nikulin V.V., Kicić D., Kähkönen S., Ilmoniemi R.J. Modulation of electroencephalographic responses to transcranial magnetic stimulation: evidence for changes in cortical excitability related to movement. Eur J Neurosci 2003;18(5):1206–12. DOI: 10.1046/j.1460- 9568.2003.02858.x. PMID: 12956719.40. Premoli I., Biondi A., Carlesso S. et al. Lamotrigine and levetiracetam exert a similar modulation of TMS-evoked EEG potentials. Epilepsia 2017;58(1): 42–50. DOI: 10.1111/epi.13599. PMID: 27808418.Premoli I., Biondi A., Carlesso S. et al. Lamotrigine and levetiracetam exert a similar modulation of TMS-evoked EEG potentials. Epilepsia 2017;58(1): 42–50. DOI: 10.1111/epi.13599. PMID: 27808418.41. Ziemann U., Reis J., Schwenkreis P. et al. TMS and drugs revisited 2014. Clin Neurophysiol 2015;126(10):1847–68. DOI: 10.1016/j.clinph.2014.08.028. PMID: 25534482.Ziemann U., Reis J., Schwenkreis P. et al. TMS and drugs revisited 2014. Clin Neurophysiol 2015;126(10):1847–68. DOI: 10.1016/j.clinph.2014.08.028. PMID: 25534482.42. Vahabzadeh-Hagh A.M., Muller P.A., Pascual-leone A. et al. Measures of cortical inhibition by paired-pulse transcranial magnetic stimulation in anesthetized rats. J Neurophysiol 2011;105(2):615–24. DOI: 10.1152/jn.00660.2010. PMID: 21160011.Vahabzadeh-Hagh A.M., Muller P.A., Pascual-leone A. et al. Measures of cortical inhibition by paired-pulse transcranial magnetic stimulation in anesthetized rats. J Neurophysiol 2011;105(2):615–24. DOI: 10.1152/jn.00660.2010. PMID: 21160011.43. Muller P.A., Dhamne S.C. Vahabzadeh-Hagh A.M. et al. Suppression of motor cortical excitability in anesthetized rats by low frequency repetitive transcranial magnetic stimulation. PLoS One 2014;9(3):910–65. DOI: 10.1371/journal.pone.0091065. PMID: 24646791.Muller P.A., Dhamne S.C. Vahabzadeh-Hagh A.M. et al. Suppression of motor cortical excitability in anesthetized rats by low frequency repetitive transcranial magnetic stimulation. PLoS One 2014;9(3):910–65. DOI: 10.1371/journal.pone.0091065. PMID: 24646791.44. Rotenberg A., Muller P., Birnbaum D. et al. Seizure suppression by EEG-guided repetitive transcranial magnetic stimulation in the rat. Clin Neurophysiol 2008;119(12):2697–702. DOI: 10.1016/j.clinph.2008.09.003. PMID: 18977170.Rotenberg A., Muller P., Birnbaum D. et al. Seizure suppression by EEG-guided repetitive transcranial magnetic stimulation in the rat. Clin Neurophysiol 2008;119(12):2697–702. DOI: 10.1016/j.clinph.2008.09.003. PMID: 18977170.45. Komssi S., Kähkönen S., Ilmoniemi R.J. The effect of stimulus intensity on brain responses evoked by transcranial magnetic stimulation. Hum Brain Mapp 2004;21(3):154–4. DOI: 10.1002/hbm.10159. PMID: 14755835.Komssi S., Kähkönen S., Ilmoniemi R.J. The effect of stimulus intensity on brain responses evoked by transcranial magnetic stimulation. Hum Brain Mapp 2004;21(3):154–4. DOI: 10.1002/hbm.10159. PMID: 14755835.46. Frantseva M., Cui J., Farzan F. et al. Disrupted cortical conductivity in schizophrenia: TMS- EEG study. Cereb Cortex 2014;24(1):211–21. DOI: 10.1093/cercor/bhs304. PMID: 23042743.Frantseva M., Cui J., Farzan F. et al. Disrupted cortical conductivity in schizophrenia: TMS- EEG study. Cereb Cortex 2014;24(1):211–21. DOI: 10.1093/cercor/bhs304. PMID: 23042743.47. Voineskos A.N., Farzan F., Barr M.S. et al. The role of the corpus callosum in transcranial propagation. Biol Psychiatry 2010;68(9):825–31. DOI: 10.1016/j.biopsych.2010.06.021. PMID: 20708172.Voineskos A.N., Farzan F., Barr M.S. et al. The role of the corpus callosum in transcranial propagation. Biol Psychiatry 2010;68(9):825–31. DOI: 10.1016/j.biopsych.2010.06.021. PMID: 20708172.48. Schutter D., van Honk J. An electrophysiological link between the cerebellum, cognition and emotion: frontal theta EEG activity to single-pulse cerebellar TMS. Neuroimage 2006;33(4):1227–31. DOI: 10.1016/j.neuroimage.2006.06.055. PMID: 17023183.Schutter D., van Honk J. An electrophysiological link between the cerebellum, cognition and emotion: frontal theta EEG activity to single-pulse cerebellar TMS. Neuroimage 2006;33(4):1227–31. DOI: 10.1016/j.neuroimage.2006.06.055. PMID: 17023183.49. Ferrarelli F., Massimini M., Sarasso S. et al. Breakdown in cortical effective connectivity during midazolam-induced loss of consciousness. Proc Natl Acad Sci USA 2010;107(6):2681– 6. DOI: 10.1073/pnas.0913008107. PMID: 20133802.Ferrarelli F., Massimini M., Sarasso S. et al. Breakdown in cortical effective connectivity during midazolam-induced loss of consciousness. Proc Natl Acad Sci USA 2010;107(6):2681– 6. DOI: 10.1073/pnas.0913008107. PMID: 20133802.50. Iscan Z., Nazarova M., Fedele T. et al. Pre-stimulus alpha oscillations and intersubject variability of motor evoked potentials in single- and paired-pulse TMS paradigms. Front Hum Neurosci 2016;10:504. DOI: 10.3389/fnhum.2016.00504. PMID: 27774060.Iscan Z., Nazarova M., Fedele T. et al. Pre-stimulus alpha oscillations and intersubject variability of motor evoked potentials in single- and paired-pulse TMS paradigms. Front Hum Neurosci 2016;10:504. DOI: 10.3389/fnhum.2016.00504. PMID: 27774060.51. Dugué L., Marque P., VanRullen R. The phase of ongoing oscillations mediates the causal relation between brain excitation and visual perception. J Neurosci 2011;31(33):11889–93. DOI: 10.1523/JNEUROSCI.1161-11.2011. PMID: 21849549.Dugué L., Marque P., VanRullen R. The phase of ongoing oscillations mediates the causal relation between brain excitation and visual perception. J Neurosci 2011;31(33):11889–93. DOI: 10.1523/JNEUROSCI.1161-11.2011. PMID: 21849549.52. Farzan F., Barr M.S., Wong W. et al. Suppression of gamma-oscillations in the dorsolateral prefrontal cortex following long interval cortical inhibition: a TMS-EEG study. Neuropsychopharmacology 2009;34(6):1543–51. DOI: 10.1038/npp.2008.211. PMID: 19037204.Farzan F., Barr M.S., Wong W. et al. Suppression of gamma-oscillations in the dorsolateral prefrontal cortex following long interval cortical inhibition: a TMS-EEG study. Neuropsychopharmacology 2009;34(6):1543–51. DOI: 10.1038/npp.2008.211. PMID: 19037204.53. Casula E.P., Tarantino V., Basso D. et al. Low-frequency rTMS inhibitory effects in the primary motor cortex: insights from TMS-evoked potentials. Neuroimage 2014;98:225–32. DOI: 10.1016/j.neuroimage.2014.04.065. PMID: 24793831.Casula E.P., Tarantino V., Basso D. et al. Low-frequency rTMS inhibitory effects in the primary motor cortex: insights from TMS-evoked potentials. Neuroimage 2014;98:225–32. DOI: 10.1016/j.neuroimage.2014.04.065. PMID: 24793831.54. Fedele T., Blagovechtchenski E., Nazarova M. et al. Long-range temporal correlations in the amplitude of alpha oscillations predict and reflect strength of intracortical facilitation: combined TMS and EEG study. Neuroscience. 2016;331:109–19. DOI: 10.1016/j.neuroscience.2016.06.015. PMID: 27318302.Fedele T., Blagovechtchenski E., Nazarova M. et al. Long-range temporal correlations in the amplitude of alpha oscillations predict and reflect strength of intracortical facilitation: combined TMS and EEG study. Neuroscience. 2016;331:109–19. DOI: 10.1016/j.neuroscience.2016.06.015. PMID: 27318302.55. Kawasaki M., Uno Y., Mori J. et al. Transcranial magnetic stimulation-induced global propagation of transient phase resetting associated with directional information flow. Front Hum Neurosci 2014;8:1–13. DOI: 10.3389/fnhum.2014.00173. PMID: 24723875.Kawasaki M., Uno Y., Mori J. et al. Transcranial magnetic stimulation-induced global propagation of transient phase resetting associated with directional information flow. Front Hum Neurosci 2014;8:1–13. DOI: 10.3389/fnhum.2014.00173. PMID: 24723875.56. Sarasso S., Boly M., Napolitani M. et al. Consciousness and complexity during unresponsiveness induced by propofol, xenon, and ketamine. Curr Biol 2015;25(23):3099– 105. DOI: 10.1016/j.cub.2015.10.014. PMID: 26752078.Sarasso S., Boly M., Napolitani M. et al. Consciousness and complexity during unresponsiveness induced by propofol, xenon, and ketamine. Curr Biol 2015;25(23):3099– 105. DOI: 10.1016/j.cub.2015.10.014. PMID: 26752078.57. Massimini M., Ferrarelli F., Murphy M.J. et al. Cortical reactivity and effective connectivity during REM sleep in humans. Cogn Neurosci 2010;1(3):176–83. DOI: 10.1080/17588921003731578. PMID: 20823938.Massimini M., Ferrarelli F., Murphy M.J. et al. Cortical reactivity and effective connectivity during REM sleep in humans. Cogn Neurosci 2010;1(3):176–83. DOI: 10.1080/17588921003731578. PMID: 20823938.58. Sun Y., Farzan F., Mulsant B.H. et al. Indicators for remission of suicidal ideation following magnetic seizure therapy in patients with treatment- resistant depression. JAMA Psychiatry 2016;73(4):337–45. DOI: 10.1001/jamapsychiatry.2015.3097. PMID: 26981889.Sun Y., Farzan F., Mulsant B.H. et al. Indicators for remission of suicidal ideation following magnetic seizure therapy in patients with treatment- resistant depression. JAMA Psychiatry 2016;73(4):337–45. DOI: 10.1001/jamapsychiatry.2015.3097. PMID: 26981889.59. Kimiskidis V.K. Transcranial magnetic stimulation (TMS) coupled with electroencephalography (EEG): biomarker of the future. Rev Neurol (Paris) 2016;172(2):123–6. DOI: 10.1016/j.neurol.2015.11.004. PMID: 26857413.Kimiskidis V.K. Transcranial magnetic stimulation (TMS) coupled with electroencephalography (EEG): biomarker of the future. Rev Neurol (Paris) 2016;172(2):123–6. DOI: 10.1016/j.neurol.2015.11.004. PMID: 26857413.60. Ferreri F., Vecchio F., Vollero L. et al. Sensorimotor cortex excitability and connectivity in Alzheimer’s disease: a TMS-EEG co-registration study. Hum Brain Mapp 2016;37(6):2083–96. DOI: 10.1002/hbm.23158. PMID: 26945686.Ferreri F., Vecchio F., Vollero L. et al. Sensorimotor cortex excitability and connectivity in Alzheimer’s disease: a TMS-EEG co-registration study. Hum Brain Mapp 2016;37(6):2083–96. DOI: 10.1002/hbm.23158. PMID: 26945686.61. Barr M.S., Farzan F., Davis K.D. et al. Measuring GABAergic inhibitory activity with TMS- EEG and its potential clinical application for chronic pain. J Neuroimmune Pharmacol 2013;8(3):535–46. DOI: 10.1007/s11481-012-9383-y. PMID: 22744222.Barr M.S., Farzan F., Davis K.D. et al. Measuring GABAergic inhibitory activity with TMS- EEG and its potential clinical application for chronic pain. J Neuroimmune Pharmacol 2013;8(3):535–46. DOI: 10.1007/s11481-012-9383-y. PMID: 22744222.62. Casali A.G., Gosseries O., Rosanova M. et al. A theoretically based index of consciousness independent of sensory processing and behavior. Sci Transl Med 2013;5(198):105. DOI: 10.1126/scitranslmed.3006294. PMID: 23946194.Casali A.G., Gosseries O., Rosanova M. et al. A theoretically based index of consciousness independent of sensory processing and behavior. Sci Transl Med 2013;5(198):105. DOI: 10.1126/scitranslmed.3006294. PMID: 23946194.63. Conde V., Andreasen S.H., Petersen T.H. et al. Alterations in the brain’s connectome during recovery from severe traumatic brain injury: protocol for a longitudinal prospective study. BMJ Open 2017;7(6):e016286. DOI: 10.1136/bmjopen-2017-016286. PMID: 28615277.Conde V., Andreasen S.H., Petersen T.H. et al. Alterations in the brain’s connectome during recovery from severe traumatic brain injury: protocol for a longitudinal prospective study. BMJ Open 2017;7(6):e016286. DOI: 10.1136/bmjopen-2017-016286. PMID: 28615277.64. Radhu N., Garcia Dominguez L., Farzan F. et al. Evidence for inhibitory deficits in the prefrontal cortex in schizophrenia. Brain 2015;138(Pt 2):483–97. DOI: 10.1093/brain/awu360. PMID: 25524710.Radhu N., Garcia Dominguez L., Farzan F. et al. Evidence for inhibitory deficits in the prefrontal cortex in schizophrenia. Brain 2015;138(Pt 2):483–97. DOI: 10.1093/brain/awu360. PMID: 25524710.65. Bruckmann S., Hauk D., Roessner V. et al. Hyperactivity disorder: new insights from the electroencephalographic response to transcranial magnetic stimulation. Brain 2012;135(Pt 7):2215–30. DOI: 10.1093/brain/aws071. PMID: 22492560.Bruckmann S., Hauk D., Roessner V. et al. Hyperactivity disorder: new insights from the electroencephalographic response to transcranial magnetic stimulation. Brain 2012;135(Pt 7):2215–30. DOI: 10.1093/brain/aws071. PMID: 22492560.66. Shafi M.M., Vernet M., Klooster D. et al. Physiological consequences of abnormal connectivity in a developmental epilepsy. Ann Neurol 2015;77(3):487–503. DOI: 10.1002/ana.24343. PMID: 25858773.Shafi M.M., Vernet M., Klooster D. et al. Physiological consequences of abnormal connectivity in a developmental epilepsy. Ann Neurol 2015;77(3):487–503. DOI: 10.1002/ana.24343. PMID: 25858773.67. Kimiskidis V.K., Tsimpiris A., Ryvlin P. et al. TMS combined with EEG in genetic generalized epilepsy: a phase II diagnostic accuracy study. Clin Neurophysiol 2017;128(2):367–81. DOI: 10.1016/j.clinph.2016.11.013. PMID: 28007469.Kimiskidis V.K., Tsimpiris A., Ryvlin P. et al. TMS combined with EEG in genetic generalized epilepsy: a phase II diagnostic accuracy study. Clin Neurophysiol 2017;128(2):367–81. DOI: 10.1016/j.clinph.2016.11.013. PMID: 28007469.68. Rotenberg A. Prospects for clinical applications of transcranial magnetic stimulation and real-time EEG in epilepsy. Brain Topogr 2010;22(4):257–66. DOI: 10.1007/s10548-009-0116-3. PMID: 19921417.Rotenberg A. Prospects for clinical applications of transcranial magnetic stimulation and real-time EEG in epilepsy. Brain Topogr 2010;22(4):257–66. DOI: 10.1007/s10548-009-0116-3. PMID: 19921417.69. Helfrich C., Pierau S.S., Freitag C.M. et al. Monitoring cortical excitability during repetitive transcranial magnetic stimulation in children with ADHD: a single-blind, sham- controlled TMS-EEG study. PloS One 2012;7(11):500–73. DOI: 10.1371/journal.pone.0050073. PMID: 23185537.Helfrich C., Pierau S.S., Freitag C.M. et al. Monitoring cortical excitability during repetitive transcranial magnetic stimulation in children with ADHD: a single-blind, sham- controlled TMS-EEG study. PloS One 2012;7(11):500–73. DOI: 10.1371/journal.pone.0050073. PMID: 23185537.70. Farzan F., Barr M.S., Levinson A.J. et al. Evidence for gamma inhibition deficits in the dorsolateral prefrontal cortex of patients with schizophrenia. Brain 2010;133(Pt 5):1505–14. DOI: 10.1093/brain/awq046. PMID: 20350936.Farzan F., Barr M.S., Levinson A.J. et al. Evidence for gamma inhibition deficits in the dorsolateral prefrontal cortex of patients with schizophrenia. Brain 2010;133(Pt 5):1505–14. DOI: 10.1093/brain/awq046. PMID: 20350936.71. Thut G., Veniero D., Romei V. et al. Article rhythmic TMS causes local entrainment of natural oscillatory signatures. Curr Biol 2011;21(14):1176–85. DOI: 10.1016/j.cub.2011.05.049. PMID: 21723129.Thut G., Veniero D., Romei V. et al. Article rhythmic TMS causes local entrainment of natural oscillatory signatures. Curr Biol 2011;21(14):1176–85. DOI: 10.1016/j.cub.2011.05.049. PMID: 21723129.72. Lett T.A., Kennedy J.L., Radhu N. et al. Prefrontal white matter structure mediates the influence of GAD1 on working memory. Neuropsychopharmacology 2016;41(9):2224–31. DOI: 10.1038/npp.2016.14. PMID: 26822489.Lett T.A., Kennedy J.L., Radhu N. et al. Prefrontal white matter structure mediates the influence of GAD1 on working memory. Neuropsychopharmacology 2016;41(9):2224–31. DOI: 10.1038/npp.2016.14. PMID: 26822489.73. Buetefisch C., Heger R., Schicks W. et al. Hebbian-type stimulation during robot-assisted training in patients with stroke. Neurorehabil Neural Repair 2011;25(7): 645–55. DOI: 10.1177/1545968311402507. PMID: 21606211.Buetefisch C., Heger R., Schicks W. et al. Hebbian-type stimulation during robot-assisted training in patients with stroke. Neurorehabil Neural Repair 2011;25(7): 645–55. DOI: 10.1177/1545968311402507. PMID: 21606211.