Транскраниальная магнитная стимуляция с электроэнцефалографией: методология, экспериментальные и клинические возможности

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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.

Об авторах

М. А. Назарова

Центр нейроэкономики и когнитивных исследований Национального исследовательского университета «Высшая школа экономики»

Автор, ответственный за переписку.
Email: chantante@gmail.com
Россия, 101000 Москва, Кривоколенный переулок, 3а, корп. 1 Россия

Е. Д. Благовещенский

Центр нейроэкономики и когнитивных исследований Национального исследовательского университета «Высшая школа экономики»

Email: fake@neicon.ru
Россия, 101000 Москва, Кривоколенный переулок, 3а, корп. 1 Россия

В. В. Никулин

Центр нейроэкономики и когнитивных исследований Национального исследовательского университета «Высшая школа экономики»

Max Planck Institute for Human Cognitive and Brain Sciences

Email: fake@neicon.ru

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

Германия, Лейпциг

Россия

М. В. Митина

Центр нейроэкономики и когнитивных исследований Национального исследовательского университета «Высшая школа экономики»

Email: fake@neicon.ru
Россия, 101000 Москва, Кривоколенный переулок, 3а, корп. 1 Россия

Список литературы

  1. 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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.
  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.

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© Назарова М.А., Благовещенский Е.Д., Никулин В.В., Митина М.В., 2018

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