Physiological correlates of neuro- and magnetic stimulation in therapy of epilepsy

Abstract

In the literature survey, non-pharmaceutical methods of therapy of epilepsy are considered including electrostimulation of vagus nerve, exposure to magnetic field and transcranial magnetic stimulation (TMS). Correlates of the effectiveness of electro- and magnetic stimulation are electrophysiological parameters, clinical data and influence on the mental and cognitive functions. Use of repetitive transcranial magnetic stimulation in addition to antiepileptic drugs has a certain ground. According to modern understanding and the results of experimental studies, the mechanism of modulator inhibitory alterations is associated with a potential of TMS to cause long-term synaptic depression or long-term potentiation. These long-lasting phenomena probably underlie anticonvulsant effects of low frequency magnetic stimulation. Inclusion of physiologists and neurophysiologists into the research will permit to solve such an important problem as a study of physiological mechanisms of the effectiveness of non-pharmacological electro- and magnetic action in epilepsy.

Keywords

vagus and trigeminal nerves stimulation / transcranial magnetic stimulation / magnetic field / epilepsy

References

[1] Shon YM., Lim SC, Lim SH. Therapeutic effect of repetitive transcranial magnetic stimulation on non-lesional focal refractory epilepsy. Journal of Clinical Neuroscience. 2019;63:130-3. doi:10.1016/j.jocn. 2019.01.025

[2] Shon Y.M., Lim S.C., Lim S.H. Therapeutic effect of repetitive transcranial magnetic stimulation on non-lesional focal refractory epilepsy // Journal of Clinical Neuroscience. 2019. Vol. 63. P. 130-133. doi:10.1016/j.jocn.2019.01.025

[3] Nardone R, Versace V, Höller Y, et al. Transcranial magnetic stimulation in myoclonus of different etiologies. Brain Research Bulletin. 2018;140:258-69. doi:10.1016/j.brainresbull.2018.05.016

[4] Nardone R., Versace V., Höller Y., et al. Trans-cranial magnetic stimulation in myoclonus of different etiologies // Brain Research Bulletin. 2018. Vol. 140. P. 258-269. doi:10.1016/j.brainresbull. 2018.05.016

[5] Dibué-Adjei M, Kamp MA, Vonck K. 30 years of vagus nerve stimulation trials in epilepsy: Do we need neuro-modulation-specific trial designs? Epilepsy Research. 2019;153:71-5. doi:10.1016/j.eple-psyres.2019.02.004

[6] Dibué-Adjei M., Kamp M.A., Vonck K. 30 years of vagus nerve stimulation trials in epilepsy: Do we need neu-romodulation-specific trial designs? // Epilepsy Research. 2019. Vol. 153. P. 71-75. doi:10. 1016/j.eplepsyres.2019.02.004

[7] González HFJ., Yengo-Kahn A, Englot DJ. Vagus Nerve Stimulation for the Treatment of Epilepsy. Neurosur-gery Clinics of North America. 2019;30 (2):219-30. doi:10.1016/j.nec.2018.12.005

[8] González H.F.J., Yengo-Kahn A., Englot D.J. Vagus Nerve Stimulation for the Treatment of Epilepsy // Neuro-surgery Clinics of North America. 2019. Vol. 30, №2. P. 219-230. doi:10.1016/j.nec. 2018.12.005

[9] Selitskiy GV, Karlov VA, Sorokina ND. Mekha-nizmy vospriyatiya mozgom cheloveka magnitnogo polya. Fizi-ologiya Cheloveka. 1996;22(4):66-72. (In Russ).

[10] Селицкий Г.В., Карлов В.А., Сорокина Н.Д. Механизмы восприятия мозгом человека магнитного поля // Физиология человека. 1996. Т. 22, №4. С. 66-72.

[11] Ulashchik VS, Pletnev AS, Voychenko NV, et al. Magnitoterapiya: Teoreticheskiye osnovy i prakti-cheskoye primeneniye. Minsk: Belaruskaya navuka; 2015. (In Russ).

[12] Улащик В.С., Плетнев А.С., Войченко Н.В., и др. Магнитотерапия: Теоретические основы и практическое примене-ние. Минск: Беларуская навука; 2015.

[13] Rivadulla C, Aguilar J, Coletti M, et al. Static magnetic fields reduce epileptiform activity in anesthetized rat and monkey. Scientific Reports. 2018; 8(1):15985. doi:10.1038/s41598-018-33808-x

[14] Rivadulla C., Aguilar J., Coletti M., et al. Static magnetic fields reduce epileptiform activity in anesthetized rat and monkey // Scientific Reports. 2018. Vol. 8, №1. P. 15985. doi:10.1038/s41598-018-33808-x

[15] Fokin VF, Ponomareva NV., Kuntsevich GI. Electrophysiological Markers of Middle Cerebral Artery Blood Flow Velocity in Healthy Subjects. Annals of the Russian Academy of Medical Sciences. 2013;(10):57-60. (In Russ).

[16] Фокин В.Ф., Пономарёва Н.В., Кунцевич Г.И. Электрофизиологические корреляты скорости движения крови по средней мозговой артерии здорового человека // Вестник РАМН. 2013. №10. С. 57-60.

[17] Selitskiy GV, Karlov VA, Sorokina ND. Vliyaniye ponizhennogo geomagnitnogo polya na bioelektri-cheskuyu aktivnost’ mozga pri epilepsii. Zhurnal Nevrologii i Psikhiatrii imeni C.C. Korsakova. 1999; 99(4):48-50. (In Russ).

[18] Селицкий Г.В., Карлов В.А., Сорокина Н.Д. Влияние пониженного геомагнитного поля на биоэлектриче-скую активность мозга при эпилепсии // Журнал неврологии и психиатрии им. C.C. Корсакова. 1999. Т. 99, №4. С. 48-50.

[19] Karlov VA, ZHidkova IA, Karakhan GV, et al. Pre-frontal’naya epilepsiya. Zhurnal Nevrologii i Psihi-atrii im. C.C. Korsakova. 1997;97(7):8-12. (In Russ).

[20] Карлов В.А., Жидкова И.А., Карахан Г.В., и др. Префронтальная эпилепсия // Журнал неврологии и пси-хиатрии им. C.C. Корсакова. 1997. Т. 97, №7. С. 8-12.

[21] Shabalov VA, Isagulyan ED. Khronicheskaya elektro-stimulyatsiya v lechenii nevropaticheskikh bolevykh sin-dromov. Kriterii dlitel’noy effektivnosti. Atmosfera. Nervnyye bolezni. 2010;(4):2-10. (In Russ).

[22] Шабалов В.А., Исагулян Э.Д. Хроническая электростимуляция в лечении невропатических болевых син-дромов. Критерии длительной эффективности // Атмосфера. Нервные болезни. 2010. №4. C. 2-10.

[23] DeGiorgio CM, Shewmon A, Murray D, et al. Pilot study of trigeminal nerve stimulation (TNS) for epilepsy: a proof-of concept trial. Epilepsia. 2006; 47(7):1213-5. doi:10.1111/j.1528-1167.2006.00594.x

[24] DeGiorgio C.M., Shewmon A., Murray D., et al. Pilot study of trigeminal nerve stimulation (TNS) for epilepsy: a proof-of concept trial // Epilepsia. 2006. Vol. 47, №7. Р. 1213-1215. doi:10.1111/ j.1528-1167.2006.00594.x

[25] Balabanova AI, Bavdurnuy AA, Bolba MV, et al. Life style and non-medication treatment methods of epilepsy. Meditsinskaya Nauka i Obrazovaniye Urala. 2015;1(2):139-45. (In Russ).

[26] Балабанова А.И., Бавдурный А.А., Больба М.В., и др. Образ жизни и немедикаментозные методы лечения при эпилепсии // Медицинская наука и образование Урала. 2015. Т. 16, №2-1. C. 139-145.

[27] Eldaief M, Press DZ, Pascual-Leone A. Transcranial magnetic stimulation in neurology: A review of established and prospective applications. Neurology. Clinical Practice. 2013;3(6):519-26. doi:10.1212/01. CPJ.0000436213.11132.8e

[28] Eldaief M., Press D.Z., Pascual-Leone A. Trans-cranial magnetic stimulation in neurology: A review of estab-lished and prospective applications // Neurology. Clinical Practice. 2013. Vol. 3, №6. P. 519-526. doi:10.1212/01.CPJ.0000436213.11132.8e

[29] Chervyakov AV, Poydasheva AG, Korzhova YuE, et al. Sovremennyye terapevticheskiye vozmozhnosti rit-micheskoy transkranial'noy magnitnoy stimulyatsii v lechenii zabolevaniy nervnoy sistemy. Russkiy Med-itsinskiy Zhurnal. 2014;(22):1567-72. (In Russ).

[30] Червяков А.В., Пойдашева А.Г., Коржова Ю.Е., и др. Современные терапевтические возможности ритми-ческой транскраниальной магнитной стимуляции в лечении заболеваний нервной системы // Русский ме-дицинский журнал. 2014. №22. P. 1567-1572.

[31] Pati S, Alexopoulos AV. Pharmacoresistant epilepsy: from pathogenesis to current and emerging therapies. Cleveland Clinical Journal of Medicine. 2010;77(7): 457-67. doi:10.3949/ccjm.77a.09061

[32] Pati S., Alexopoulos A.V. Pharmacoresistant epilepsy: from pathogenesis to current and emerging therapies // Cleveland Clinical Journal of Medicine. 2010. Vol. 77, №7. P. 457-467. doi:10.3949/ccjm.77a.09061

[33] Fregni F, Otachi PT, Do Valle A, et al. A randomized clinical trial of repetitive transcranial magnetic stimulation in patients with refractory epilepsy. Annals of Neurology. 2006;60(4):447-55. doi:10.1002/ ana.20950

[34] Fregni F., Otachi P.T., Do Valle A., et al. A randomized clinical trial of repetitive transcranial magnetic stimula-tion in patients with refractory epilepsy // Annals of Neurology. 2006. Vol. 60, №4. P. 447-455. doi:10.1002/ana.20950

[35] Sun W, Mao W, Meng X, et al. Low-frequency repetitive transcranial magnetic stimulation for the treatment of refractory partial epilepsy: a controlled clinical study. Epilepsia. 2012;53(10):1782-9. doi:10. 1111/j.1528-1167.2012.03626.x

[36] Sun W., Mao W., Meng X., et al. Low-frequency repetitive transcranial magnetic stimulation for the treatment of refractory partial epilepsy: a controlled clinical study // Epilepsia. 2012. Vol. 53, №10. P. 1782-1789. doi:10.1111/j.1528-1167.2012.03626.x

[37] Hsu WY, Cheng CH, Lin MW, et al. Antiepileptic effects of low frequency repetitive transcranial magnetic stimulation: a meta-analysis. Epilepsy Research. 2011;96(3):231-40. doi:10.1016/j.eplepsy-res.2011.06.002

[38] Hsu W.Y., Cheng C.H., Lin M.W., et al. Antiepileptic effects of low frequency repetitive trans-cranial magnetic stimulation: A meta-analysis // Epilepsy Research. 2011. Vol. 96, №3. P. 231-240. doi:10.1016/j.eplepsyres.2011.06.002

[39] Dokukina TV, Misyuk NN, Hlebokazov FP, et al. Primenenie transkranial'noj magnitoterapii v kompleksnom lechenii epilepsii. In: Covremennye metody diagnostiki, lecheniya i profilaktiki zabolevanij. Minsk; 2018. (In Russ).

[40] Докукина Т.В., Мисюк Н.Н., Хлебоказов Ф.П., и др. Применение транскраниальной магнитотерапии в комплексном лечении эпилепсии. В сб.: Современные методы диагностики, лечения и профилактики за-болеваний. Минск; 2018.

[41] Rotenberg A. Prospects for clinical applications of transcranial magnetic stimulation and real-time EEG in epi-lepsy. Brain Topography. 2010;22(4): 257-66. doi:10.1007/s10548-009-0116-3

[42] Rotenberg A. Prospects for clinical applications of transcranial magnetic stimulation and real-time EEG in epi-lepsy // Brain Topography. 2010. Vol. 22, №4. P. 257-266. doi:10.1007/s10548-009-0116-3

[43] Rotenberg A, Bae EH, Takeoka M, et al. Repetitive transcranial magnetic stimulation in the treatment of epilep-sia partialis continua. Epilepsy Behavior. 2009;14(1):253-7. doi:10.1016/j.yebeh.2008.09.007

[44] Rotenberg A., Bae E.H., Takeoka M., et al. Repetitive transcranial magnetic stimulation in the treatment of epi-lepsia partialis continua // Epilepsy & Behavior. 2009. Vol. 14, №1. P. 253-257. doi:10. 1016/j.yebeh.2008.09.007

[45] Santiago-Rodriguez E, Cardenas-Morales L, Harmony T, et al. Repetitive transcranial magnetic stimulation de-creases the number of seizures in patients with focal neocortical epilepsy. Seizure. 2008;17 (8): 677-683.

[46] Santiago-Rodríguez E., Cárdenas-Morales L., Harmony T., et al. Repetitive transcranial magnetic stimulation decreases the number of seizures in patients with focal neocortical epilepsy // Seizure. 2008. Vol. 17, №8. P. 677-683. doi:10.1016/j.seizure.2008.04.005

[47] Najib U, Bashir Sh, Edwards D, et al. Transcranial Brain Stimulation: Clinical Applications and Future Direc-tions. Neurosurgery Clinics of North America. 2011;22(2):233-58. doi:10.1016/j.nec.2011.01.002

[48] Najib U., Bashir Sh., Edwards D., et al. Transcranial Brain Stimulation: Clinical Applications and Future Direc-tions // Neurosurgery Clinics of North America. 2011. Vol. 22, №2. P. 233-258. doi:10.1016/j.nec.2011.01.002

[49] Chen R, Spencer DC, Weston J, et al. Transcranial magnetic stimulation for the treatment of epilepsy (Review). The Cochrane Database of Systematic Reviews. 2016;(8):CD011025. doi:10.1002/14651858. CD011025.pub2

[50] Chen R., Spencer D.C., Weston J., et al. Transcranial magnetic stimulation for the treatment of epilepsy (Review) // The Cochrane Database of Systematic Reviews. 2016. №8. P. CD011025. doi:10.1002/14651858.CD011025.pub2

[51] Evstigneev VV, Kisten' OV. Transcranial magnetic stimulation in complex therapy of epilepsy. Annals of Clini-cal and Experimental Neurology. 2013;7(2): 20-6. (In Russ).

[52] Евстигнеев В.В., Кистень О.В. Транскраниальная магнитная стимуляция в комплексной терапии эпилеп-сии // Анналы клинической и экспериментальной неврологии. 2013. Т. 7, №2. C. 20-26.

[53] Pereira LS, Müller VT, Gomes M, et al. Safety of repetitive transcranial magnetic stimulation in patients with epi-lepsy: A systematic review. Epilepsy & Behavior. 2016;57(Pt A):167-76. doi:10.1016/j. yebeh.2016.01.015

[54] Pereira L.S., Müller V.T., Gomes M., et al. Safety of repetitive transcranial magnetic stimulation in patients with epilepsy: A systematic review// Epilepsy & Behavior. 2016. Vol. 57, Pt A. P. 167-176. doi:10.1016/j.yebeh.2016.01.015

[55] Rossi S, Hallett M, Rossini P, et al. Safety of TMS Consensus Group. Clinical safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical Neurophysiology. 2009; 120(12):2008-39. doi:10.1016/j.clinph.2009.08.016

[56] Rossi S., Hallett M., Rossini P., et al. Safety of TMS Consensus Group. Clinical safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research // Clinical Neurophysiology. 2009. Vol. 120, №12. P. 2008-2039. doi:10.1016/ j.clinph.2009.08.016

[57] Kisten’ OV, Evstigneyev VV. Vozmozhnosti ritmi-cheskoy transkranial’noy magnitnoy stimulyatsii v optimi-zatsii blokady epileptogeneza. Lechebnoye Delo. 2014;4(38):19-28. (In Russ).

[58] Кистень О.В., Евстигнеев В.В. Возможности ритмической транскраниальной магнитной стимуляции в оп-тимизации блокады эпилептогенеза // Лечебное дело. 2014. №4(38). C. 19-28.

[59] Funke K, Benali А. Modulation of cortical inhibition by rTMS – findings obtained from animal models. Journal of Physiology. 2011;589(Pt 18): 4423-35. doi:10.1113/jphysiol.2011.206573

[60] Funke K., Benali А. Modulation of cortical inhibition by rTMS – findings obtained from animal models // Jour-nal of Physiology. 2011. Vol. 589, Pt 18. P. 4423-4435. doi:10.1113/jphysiol.2011.206573

[61] Hoffmann RE, Cavus I. Slow transcranial magnetic stimulation, long-term depotentiation, and brain hyperex-citability disorders. The American Journal of Psychiatry. 2002;159(7):1093-102. doi:10.1176/ ap-pi.ajp.159.7.1093

[62] Hoffmann R.E., Cavus I. Slow transcranial magnetic stimulation, long-term depotentiation, and brain hyperex-citability disorders // The American Journal of Psychiatry. 2002. Vol. 159, №7. P. 1093-1102. doi:10.1176/appi.ajp.159.7.1093

[63] Pettorruso M, Di Giuda D., Martinotti G, et al. Dopaminergic and clinical correlates of high-frequ-ency repetitive transcranial magnetic stimulation in gam-bling addiction: a SPECT case study. Addictive Behaviors. 2019;93:246-9. doi:10.1016/j.ad-dbeh.2019.02.013

[64] Pettorruso M., Di Giuda, D., Martinotti G., et al. Dopaminergic and clinical correlates of high-frequency repetitive transcranial magnetic stimulation in gambling addiction: a SPECT case study // Addictive Behaviors. 2019. Vol. 93. P. 246-249. doi:10.1016/j.addbeh.2019.02.013

[65] Zhang JQ, Yu JM, Wang XM, et al. The Effects of Pretreatment with Low-Frequency Repetitive Tran-seranial mMagnetic Stimulation on Expressions of Hippocampns GAD65 and NMDAR1 in Rats with Pilocarpine-lnduced Seizures. Chinese Journal of Neuroimmunology and Neurology. 2008;(6):430-3.

[66] Zhang J.Q., Yu J.M., Wang X.M., et al. The Effects of Pretreatment with Low-Frequency Repetitive Transeranial mMagnetic Stimulation on Expressions of Hippocampns GAD65 and NMDAR1 in Rats with Pilocarpine-lnduced Seizures // Chinese Journal of Neuroimmunology and Neurology. 2008. №6. P. 430-433.

[67] Conway CR, Udaiyar A, Schachter SC. Neurosti-mulation for depression in epilepsy. Epilepsy & Behavior. 2018;88S:25-32. doi:10.1016/j.yebeh.2018. 06.007

[68] Conway C.R., Udaiyar A., Schachter S.C. Neuro-stimulation for depression in epilepsy // Epilepsy & Behavior. 2018. Vol. 88S. P. 25-32. doi:10.1016/ j.yebeh.2018.06.007

[69] Kinoshita M, Ikeda A, Begum T, et al. Low-frequency repetitive transcranial magnetic stimulation for seizure suppression in patients with extra-temporal lobe epilepsy: a pilot study. Seizure. 2005; 14(6):387-92. doi:10.1016/j.seizure.2005.05.002

[70] Kinoshita M., Ikeda A., Begum T., et al. Low-frequency repetitive transcranial magnetic stimulation for seizure suppression in patients with extra-temporal lobe epilepsy: a pilot study // Seizure. 2005. Vol. 14, №6. P. 387-392. doi:10.1016/j.seizure. 2005.05.002

[71] Cantello R, Rossi S, Varrasi C, et al. Slow repetitive TMS for drug-resistant epilepsy: clinical and EEG findings of a placebo-controlledtrial. Epilepsia. 2007;48(2):366-74. doi:10.1111/j.1528-1167.2006. 00938.x

[72] Cantello R., Rossi S., Varrasi C., et al. Slow repetitive TMS for drug-resistant epilepsy: clinical and EEG findings of a placebo-controlled trial // Epilepsia. 2007. Vol. 48, №2. P. 366-374. doi:10.1111/ j.1528-1167.2006.00938.x

[73] Kisten' OV, Evstigneev VV. Probable anticonvulsive mechanisms of repetitive transcranial magnetic stimulation and predictors of its effectivity. Epilepsy and Paroxysmal Conditions. 2014;6(1): 19-26. (In Russ).

[74] Кистень О.В., Евстигнеев В.В. Возможные противосудорожные механизмы ритмической транскраниаль-ной магнитной стимуляции и предикторы ее эффективности // Эпилепсия и пароксизмальные состояния. 2014. T. 6, №1. C. 19-26.

[75] Gimranov RF, Kurdyukova EN. Transcranial Magnetic Stimulation in Research of Emotion in the Healthy and Patients with Epilepsy. I.P. Pavlov Journal of Higher Nervous Activity. 2005;55(2): 202-6. (In Russ).

[76] Гимранов Р.Ф., Курдюкова Е.Н. Транскраниальная магнитная стимуляция в исследовании эмоции у здо-ровых испытуемых и больных эпилепсией // Журнал высшей нервной деятельности им. И.П. Павлова. 2005. Т. 55, №2. C. 202-206.

[77] Yang J, Phi JH. The Present and Future of Vagus Nerve Stimulation. Journal of Korean Neurosurgical Society. 2019;62(3):344-52. doi:10.3340/jkns. 2019.0037

[78] Yang J., Phi J.H. The Present and Future of Vagus Nerve Stimulation // Journal of Korean Neurosurgical Society. 2019. Vol. 62, №3. P. 344-352. doi:10. 3340/jkns.2019.0037

RIGHTS & PERMISSIONS

Sorokina N.D., Pertsov S.S., Selitskiy G.V.