Электрическая стимуляция с использованием электродов для стереоэлектроэнцефалографии
https://doi.org/10.17650/1683-3295-2024-26-3-144-155
Аннотация
Электрическая стимуляция (ЭС) с использованием электродов для стереоэлектроэнцефалографии – важный компонент предхирургического обследования пациентов со структурной фармакорезистентной эпилепсией. ЭС помогает в решении 2 наиболее сложных проблем в хирургии эпилепсии – тотального удаления эпилептогенного участка коры головного мозга и минимизации постоперационного неврологического дефицита. ЭС позволяет осуществлять провокацию типичных эпилептических приступов у пациентов с целью уточнения нейрофизиологических особенностей и границ эпилептогенной зоны, а также картировать функционально значимые зоны для уменьшения площади резекции с прогнозированием постоперационного неврологического дефицита. Результаты исследований, проведенных с использованием ЭС, вносят огромный вклад не только в практическую медицину, но и в фундаментальную науку, позволяя более детально изучить функции отдельных участков головного мозга и понять элементы патогенеза различных заболеваний нервной системы.
Об авторах
В. О. РусскинРоссия
Вадим Олегович Русскин
119435 Москва, Абрикосовский пер., 2
А. А. Кузнецова
Россия
119049 Москва, 4-й Добрынинский пер., 1/9;
115419 Москва, ул. Донская, 43
В. Б. Соловьев
Россия
119049 Москва, 4-й Добрынинский пер., 1/9
А. В. Левов
Россия
119049 Москва, 4-й Добрынинский пер., 1/9
Ф. Б. Бердинов
Россия
119049 Москва, 4-й Добрынинский пер., 1/9;
117198, Москва, ул. МиклухоМаклая, 6
М. И. Лившиц
Россия
119049 Москва, 4-й Добрынинский пер., 1/9;
117997 Москва, ул. Островитянова, 1
В. А. Сандриков
Россия
119435 Москва, Абрикосовский пер., 2
Список литературы
1. Beghi E. The Epidemiology of еpilepsy. Neuroepidemiology 2020;54(2):185–91. DOI: 10.1159/000503831
2. Эпилепсия и эпилептический статус у взрослых и детей. Клинические рекомендации Минздрава России. 2022. Доступно по: https://cr.minzdrav.gov.ru/schema/741_6?ysclid=lytt0xchgq539764487
3. Крылов В.В., Гехт А.Б., Трифонов И.С. и др. Исходы хирургического лечения пациентов с фармакорезистентными формами эпилепсии. Журнал неврологии и психиатрии им. С.С. Корсакова. Спецвыпуски 2016;116(9–2):13–8. DOI: 10.17116/jnevro20161169213-18
4. Kwan P., Arzimanoglou A., Berg A.T. et al. Definition of drug resistant epilepsy: consensus proposal by the ad hoc Task Force of the ILAE Commission on Therapeutic Strategies. Epilepsia 2010;51(6):1069–77. DOI: 10.1111/j.1528-1167.2009.02397.x
5. Scheffer I.E., Berkovic S., Capovilla G. et al. ILAE classification of the epilepsies: position paper of the ILAE Commission for Classification and Terminology. Epilepsia 2017;58(4):512–21. DOI: 10.1111/epi.13709
6. Зуев А.А., Головтеев А.Л., Педяш Н.В. и др. Возможности хирургического лечения фармакорезистентной эпилепсии с использованием робот-ассистированной имплантации глубинных электродов для проведения инвазивной стереоэлектроэнцефалографии. Нейрохирургия 2020;22(1):12–20. DOI: 10.17650/1683-3295-2020-22-1-12-20
7. Bartholow R. Experimental investigations into the functions of the human brain. Am J Med Sci 1874;66:305–13.
8. Leblanc R. Cushing, Penfield, and cortical stimulation. J Neurosurg 2018;130(1):76–83. DOI: 10.3171/2017.7.JNS171256
9. Foerster O., Penfield W. The structural basis of traumatic epilepsy and results of radical operation. Brain 1930;53(2):99–119. DOI: 10.1093/brain/53.2.99
10. Penfield W., Boldrey E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 1937;60(4):389–443. DOI: 10.1093/brain/60.4.389
11. Reif P.S., Strzelczyk A., Rosenow F. The history of invasive EEG evaluation in epilepsy patients. Seizure 2016;41:191–5. DOI: 10.1016/j.seizure.2016.04.006
12. Talairach J., Bancaud J., Geier S. et al. The cingulate gyrus and human behaviour. Electroencephalogr Clin Neurophysiol 1973;34(1):45–52. DOI: 10.1016/0013-4694(73)90149-1
13. Bancaud J., Talairach J., Morel P. et al. “Generalized” epileptic seizures elicited by electrical stimulation of the frontal lobe in man. Electroencephalogr Clin Neurophysiol 1974;37(3):275–82. DOI: 10.1016/0013-4694(74)90031-5
14. Kovac S., Vakharia V.N., Scott C., Diehl B. Invasive epilepsy surgery evaluation. Seizure 2017;44:125–36. DOI: 10.1016/j.seizure.2016.10.016
15. Балацкая А.С., Педяш Н.В., Головтеев А.Л. и др. Стереоэлектроэнцефалография в прехирургическом обследовании пациентов с фармакорезистентной фокальной эпилепсией. Эпилепсия и пароксизмальные состояния 2022;14(2):183–94. DOI: 10.17749/2077-8333/epi.par.con.2022.090
16. Sheng J., Liu S., Qin H. et al. Drug-resistant epilepsy and surgery. Curr Neuropharmacol 2018;16(1):17–28. DOI: 10.2174/1570159X15666170504123316
17. Pfurtscheller G., Cooper R. Frequency dependence of the transmission of the EEG from cortex to scalp. Electroencephalogr Clin Neurophysiol 1975;38(1):93–6. DOI: 10.1016/0013-4694(75)90215-1
18. Grinenko O., Li J., Mosher J.C. et al. A fingerprint of the epileptogenic zone in human epilepsies. Brain 2018;141(1):117–31. DOI: 10.1093/brain/awx306
19. David O., Blauwblomme T., Job A.S. et al. Imaging the seizure onset zone with stereo-electroencephalography. Brain 2011; 134(Pt 10):2898–911. DOI: 10.1093/brain/awr238
20. Alarcon G., Binnie C.D., Elwes R.D., Polkey C.E. Power spectrum and intracranial EEG patterns at seizure onset in partial epilepsy. Electroencephalogr Clin Neurophysiol 1995;94(5):326–37. DOI: 10.1016/0013-4694(94)00286-t
21. Höller Y., Kutil R., Klaffenböck L. et al. High-frequency oscillations in epilepsy and surgical outcome. A meta-analysis. Front Hum Neurosci 2015;9:574. DOI: 10.3389/fnhum.2015.00574
22. Kovac S., Scott C.A., Maglajlija V. et al. Extraoperative electrical cortical stimulation: characteristics of motor responses and correlation with precentral gyrus. J Clin Neurophysiol 2011;28(6):618–24. DOI: 10.1097/WNP.0b013e31823cc0f9
23. Chaudhary U.J., Duncan J.S. Applications of blood-oxygen-leveldependent functional magnetic resonance imaging and diffusion tensor imaging in epilepsy. Neuroimaging Clin N Am 2014;24(4):671–94. DOI: 10.1016/j.nic.2014.07.001
24. Ni B., Wang X., Yu T. et al. Pre-surgical language mapping in epilepsy: using fMRI in Chinese-speaking patients. Front Hum Neurosci 2019;13:183. DOI: 10.3389/fnhum.2019.00183
25. Sarubbo S., Tate M., De Benedictis A. et al. Mapping critical cortical hubs and white matter pathways by direct electrical stimulation: an original functional atlas of the human brain. Neuroimage 2020;205:116237. DOI: 10.1016/j.neuroimage.2019.116237
26. Rattay F. The basic mechanism for the electrical stimulation of the nervous system. Neuroscience 1999;89(2):335–46. DOI: 10.1016/s0306-4522(98)00330-3
27. Kovac S., Kahane P., Diehl B. Seizures induced by direct electrical cortical stimulation – mechanisms and clinical considerations. Clin Neurophysiol 2016;127(1):31–9. DOI: 10.1016/j.clinph.2014.12.009
28. Shindhelm A.C., Thio B.J., Sinha S.R. Modeling the impact of electrode/tissue geometry on electrical stimulation in stereo-EEG. J Clin Neurophysiol 2023;40(4):339–49. DOI: 10.1097/WNP.0000000000000892
29. Suh M., Bahar S., Mehta A.D., Schwartz T.H. Blood volume and hemoglobin oxygenation response following electrical stimulation of human cortex. Neuroimage 2006;31(1):66–75. DOI: 10.1016/j.neuroimage.2005.11.030
30. Isnard J., Taussig D., Bartolomei F. et al. French guidelines on stereoelectroencephalography (SEEG). Neurophysiol Clin 2018;48(1):5–13. DOI: 10.1016/j.neucli.2017.11.005
31. Trébuchon A., Chauvel P. Electrical stimulation for seizure induction and functional mapping in stereoelectroencephalography. J Clin Neurophysiol 2016;33(6):511–21. DOI:10.1097/WNP.0000000000000313
32. Arya R., Aungaroon G., Zea Vera A. et al. Fosphenytoin premedication for pediatric extra-operative electrical stimulation brain mapping. Epilepsy Res 2018;140:171–6. DOI: 10.1016/j.eplepsyres.2018.01.017
33. Landazuri P., Minotti L. Electrical stimulation for mapping of the epileptogenic zone. In: Invasive studies of the human epileptic brain: Principles and practice. Ed. by S.D. Lhatoo, P. Kahane, H.O. Luders. Oxford: Oxford University Press, 2019. Pp. 161–172. DOI: 10.1093/med/9780198714668.003.0013
34. Kovac S., Scott C.A., Maglajlija V. et al. Comparison of bipolar versus monopolar extraoperative electrical cortical stimulation mapping in patients with focal epilepsy. Clin Neurophysiol 2014;125(4):667–74. DOI: 10.1016/j.clinph.2013.09.026
35. Grande K.M., Ihnen S.K.Z., Arya R. Electrical stimulation mapping of brain function: a comparison of subdural electrodes and stereo-EEG. Front Hum Neurosci 2020;14:611291. DOI: 10.3389/fnhum.2020.611291
36. Giovannelli G., Pelliccia V., Abarrategui B. et al. Intermediate stimulation frequencies for language mapping using Stereo-EEG. Clin Neurophysiol 2022;144:91–7. DOI: 10.1016/j.clinph.2022.10.003
37. Arya R., Ervin B., Dudley J. et al. Electrical stimulation mapping of language with stereo-EEG. Epilepsy Behav 2019;99:106395. DOI: 10.1016/j.yebeh.2019.06.038
38. Arya R., Ervin B., Holloway T. et al. Electrical stimulation sensorimotor mapping with stereo-EEG. Clin Neurophysiol 2020;131(8):1691–701. DOI: 10.1016/j.clinph.2020.04.159
39. Hamberger M.J., Williams A.C., Schevon C.A. Extraoperative neurostimulation mapping: results from an international survey of epilepsy surgery programs. Epilepsia 2014;55(6):933–9. DOI: 10.1111/epi.12644
40. Bartolomei F., Nica A., Valenti-Hirsch M.P. et al. Interpretation of SEEG recordings. Neurophysiol Clin 2018;48(1):53–7. DOI: 10.1016/j.neucli.2017.11.010
41. Wyler A.R., Ward A.A. Jr. Neurons in human epileptic cortex. Response to direct cortical stimulation. J Neurosurg 1981;55(6):904–8. DOI: 10.3171/jns.1981.55.6.0904
42. Mormann F., Jefferys J.G. Neuronal firing in human epileptic cortex: the ins and outs of synchrony during seizures. Epilepsy Curr 2013;13(2):100–2. DOI: 10.5698/1535-7597-13.2.100
43. Gollwitzer S., Hopfengärtner R., Rössler K. et al. Afterdischarges elicited by cortical electric stimulation in humans: when do they occur and what do they mean? Epilepsy Behav 2018:87:173–9. DOI: 10.1016/j.yebeh.2018.09.007
44. Rosenow F., Lüders H. Presurgical evaluation of epilepsy. Brain 2001;124(Pt 9):1683–700. DOI: 10.1093/brain/124.9.1683
45. Kahane P., Landré E., Minotti L. et al. The Bancaud and Talairach view on the epileptogenic zone: a working hypothesis. Epileptic Disord 2006;8(Suppl 2):S16–26.
46. Cuello Oderiz C., von Ellenrieder N., Dubeau F. et al. Association of cortical stimulation-induced seizure with surgical outcome in patients with focal drug-resistant epilepsy. JAMA Neurol 2019;76(9):1070–8. DOI: 10.1001/jamaneurol.2019.1464
47. Trebuchon A., Racila R., Cardinale F. Electrical stimulation for seizure induction during SEEG exploration: a useful predictor of postoperative seizure recurrence? J Neurol Neurosurg Psychiatry 2020;jnnp-2019-322469. DOI: 10.1136/jnnp-2019-322469
48. Bernier G.P., Richer F., Giard N. et al. Electrical stimulation of the human brain in epilepsy. Epilepsia 1990;31(5):513–20. DOI: 10.1111/j.1528-1157.1990.tb06099.x
49. Jacobs J., Zijlmans M., Zelmann R et al. Value of electrical stimulation and high frequency oscillations (80–500 Hz) in identifying epileptogenic areas during intracranial EEG recordings. Epilepsia 2010;51(4):573–82. DOI: 10.1111/j.1528-1167.2009.02389.x
50. Halgren E., Walter R.D., Cherlow D.G., Crandall P.H. Mental phenomena evoked by electrical stimulation of the human hippocampal formation and amygdala. Brain 1978;10(1)1:83–117. DOI: 10.1093/brain/101.1.83
51. Wieser H.G., Bancaud J., Talairach J. et al. Comparative value of spontaneous and chemically and electrically induced seizures in establishing the lateralization of temporal lobe seizures. Epilepsia 1979;20(1):47–59. DOI: 10.1111/j.1528-1157.1979.tb04775.x
52. Munari C., Kahane P., Tassi .L et al. Intracerebral low frequency electrical stimulation: a new tool for the definition of the “epileptogenic area”? Acta Neurochir Suppl (Wien) 1993;58: 181–5. DOI: 10.1007/978-3-7091-9297-9_42
53. Kahane P., Tassi L., Francione S. et al. [Electroclinical manifestations elicited by intracerebral electric stimulation “shocks” in temporal lobe epilepsy (In French)]. Neurophysiol Clin 1993;23(4):305–26. DOI: 10.1016/s0987-7053(05)80123-6
54. Chassoux F., Devaux B., Landré E. et al. Stereoelectroencephalography in focal cortical dysplasia: a 3D approach to delineating the dysplastic cortex. Brain 2000;123(Pt 8):1733–51. DOI: 10.1093/brain/123.8.1733
55. Landré E., Turak B., Toussaint D., Trottier S. Intérêt des stimulations électriques intracérébrales en stéréoélectroencéphalographie dans les épilepsies partielles. Epilepsies 2004;16:213–25. (In French).
56. McGonigal A., Lagarde S., Trébuchon-Dafonseca A. et al. Early onset motor semiology in seizures triggered by cortical stimulation during SEEG. Epilepsy Behav 2018;88:262–7. DOI: 10.1016/j.yebeh.2018.09.017
57. Singh R., Principe A., Tadel F. et al. Mapping the insula with stereo-electroencephalography: the emergence of semiology in insula lobe seizures. Ann Neurol 2020;88(3):477–88. DOI: 10.1002/ana.25817
58. Spilioti M., Winston J.S., Centeno M. et al. The nature, frequency and value of stimulation induced seizures during extraoperative cortical stimulation for functional mapping. Seizure 2020;81:71–5. DOI: 10.1016/j.seizure.2020.07.027
59. So E.L., Alwaki A. A guide for cortical electrical stimulation mapping. J Clin Neurophysiol 2018;35(2):98–105. DOI: 10.1097/WNP.0000000000000435
60. Nii Y., Uematsu S., Lesser R.P., Gordon B. Does the central sulcus divide motor and sensory functions? Cortical mapping of human hand areas as revealed by electrical stimulation through subdural grid electrodes. Neurology 1996;46(2):360–7. DOI: 10.1212/wnl.46.2.360
61. Nachev P., Kennard C., Husain M. Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 2008;9(11):856–69. DOI: 10.1038/nrn2478
62. Aron O., Jonas J., Colnat-Coulbois S., Maillard L. Language mapping using stereo electroencephalography: a review and expert opinion. Front Hum Neurosci 2021;15:619521. DOI: 10.3389/fnhum.2021.619521
63. Hamberger M.J. Cortical language mapping in epilepsy: a critical review. Neuropsychol Rev 2007;17(4):477–89. DOI: 10.1007/s11065-007-9046-6
64. Alonso F., Sweet J., Miller J. Speech mapping using depth electrodes: the “electric Wada”. Clin Neurol Neurosurg 2016;144:88–90. DOI: 10.1016/j.clineuro.2016.03.017
65. Young J.J., Coulehan K., Fields M.C. et al. Language mapping using electrocorticography versus stereoelectroencephalography: a case series. Epilepsy Behav 2018;84:148–51. DOI: 10.1016/j.yebeh.2018.04.032
66. Holloway T., Leach J.L., Tenney J.R. et al. Functional MRI and electrical stimulation mapping for language localization: a comparative meta-analysis. Clin Neurol Neurosurg 2022;222:107417. DOI: 10.1016/j.clineuro.2022.107417
67. Parvizi J., Veit M.J., Barbosa D.A.N. et al. Complex negative emotions induced by electrical stimulation of the human hypothalamus. Brain Stimul 2022;15(3):615–23. DOI: 10.1016/j.brs.2022.04.008
68. Fausto C. The integration of emotional expression and experience: a pragmatist review of recent evidence from brain stimulation. Emotion Rev 2019;11(1):27–38. DOI: 10.1177/1754073917723461
69. Long Q., Li W., Zhang W. et al. Electrical stimulation mapping in the medial prefrontal cortex induced auditory hallucinations of episodic memory: a case report. Front Hum Neurosci 2022;16:815232. DOI: 10.3389/fnhum.2022.815232
70. Caruana F., Avanzini P., Gozzo F. et al. Mirth and laughter elicited by electrical stimulation of the human anterior cingulate cortex. Cortex 2015;71:323–31. DOI: 10.1016/j.cortex.2015.07.024
71. Bartolomei F., Lagarde S., Villalon S.M. et al. The “Proust phenomenon”: odor-evoked autobiographical memories triggered by direct amygdala stimulation in human. Cortex 2017;90:173–5. DOI: 10.1016/j.cortex.2016.12.005
72. Popa I., Donos C., Barborica A. et al. Intrusive thoughts elicited by direct electrical stimulation during stereoelectroencephalography. Front Neurol 2016;7:114. DOI: 10.3389/fneur.2016.00114
73. Gumnit R.J., Labiner D.M., Fountain N.B. et al. Data on Specialized Epilepsy Centers: report to the Institute of Medicine’s Committee on the Public Health Dimensions of the Epilepsies. In: Epilepsy across the spectrum: promoting health and understanding. Ed. by M.J. England, C.T. Liverman, A.M. Schultz et al. Washington (DC): National Academies Press (US), 2012. C. Available at: https://www.ncbi.nlm.nih.gov/books/NBK100603/
74. Gaillard W.D., Jette N., Arnold S.T. et al. Task force for pediatric epilepsy surgery, commission for pediatrics, and the surgical commission of the international league against epilepsy. Establishing criteria for pediatric epilepsy surgery center levels of care: report from the ILAE Pediatric Epilepsy Surgery Task Force. Epilepsia 2020;61(12):2629–42. DOI: 10.1111/epi.16698
75. Katz J., Armstrong C., Kvint S. et al. Stereoelectroencephalography in the very young: case report. Epilepsy Behav Rep 2022;19:100552. DOI: 10.1016/j.ebr.2022.100552
76. Jayakar P., Lesser R.P. Extraoperative functional mapping. In: Epilepsy: A comprehensive textbook. Ed. by J.J. Engel, T.A. Pedley. 2nd edn. Philadelphia, PA: Lippincott Williams & Wilkins, 2008.
77. Aungaroon G., Zea Vera A., Horn P.S. et al. After-discharges and seizures during pediatric extra-operative electrical cortical stimulation functional brain mapping: incidence, thresholds, and determinants. Clini Neurophysiol 2017;128(10):2078–86. DOI: 10.1016/j.clinph.2017.06.259
78. Signorelli F., Guyotat J., Mottolese C. et al. Intraoperative electrical stimulation mapping as an aid for surgery of intracranial lesions involving motor areas in children. Childs Nerv Syst 2004;20(6):420–6. DOI: 10.1007/s00381-004-0961-z
79. Cossu M., Schiariti M., Francione S. et al. Stereoelectroencephalography in the presurgical evaluation of focal epilepsy in infancy and early childhood. J Neurosurg Pediatr 2012;9(3):290–300. DOI: 10.3171/2011.12.PEDS11216
80. Taussig D., Chipaux M., Lebas A. et al. Stereoelectroencephalography (SEEG) in 65 children: an effective and safe diagnostic method for pre-surgical diagnosis, independent of age. Epileptic Disord 2014;16(3):280–95. DOI: 10.1684/epd.2014.0679
Рецензия
Для цитирования:
Русскин В.О., Кузнецова А.А., Соловьев В.Б., Левов А.В., Бердинов Ф.Б., Лившиц М.И., Сандриков В.А. Электрическая стимуляция с использованием электродов для стереоэлектроэнцефалографии. Нейрохирургия. 2024;26(3):144-155. https://doi.org/10.17650/1683-3295-2024-26-3-144-155
For citation:
Russkin V.O., Kuznetsova A.A., Solovyev V.B., Levov A.V., Berdinov F.B., Livshits M.I., Sandrikov V.A. Electric stimulation using stereoelectroencephalography electrodes. Russian journal of neurosurgery. 2024;26(3):144-155. (In Russ.) https://doi.org/10.17650/1683-3295-2024-26-3-144-155