Stereotactic EEG-based cortical electrical stimulation in the preoperative evaluation of epilepsy_Journal of Epilepsy

Authors：

HE Xinru ,  SUN Meizhen

Department of Neurology, the First Hospital of Shanxi Medical University, Taiyuan 030000, China;

Corresponding author：

SUN Meizhen, Email: sunmeizhen213@126.com

Keywords：

Electrical cortical stimulation; Stereotactic electroencephalography; Epilepsy; Preoperative evaluation

DOI：

10.7507/2096-0247.202503009

Video：

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Epilepsy is one of the most common neurological disorders, and surgical intervention is usually used for drug-resistant focal epilepsy. Cortical electrical stimulation is widely used in preoperative evaluation of epilepsy to explore the anatomical-clinical electrical correlations between epileptogenic and functional networks through electrical stimulation, and the functional brain maps produced by cortical electrical stimulation depict areas of the functional cortex at an individual level, identifying the functional cortex with greater precision, as well as helping to establish epilepsy network, enabling more precise localization of seizure zones and providing a more accurate localization for surgical resection. Electrical cortical stimulation has become a standard technique for the preoperative assessment of brain region function in brain surgery. It is an indispensable part of preoperative evaluation.The main types of functional mapping by electrical stimulation include stereoelectroencephalography (SEEG) and subdural electrode (SDE), SEEG-guided cortical electrical stimulation is gradually becoming more mainstream compared to subdural electrodes, and is increasingly valuable and important as a preoperative evaluation of epilepsy. It is increasingly demonstrating its value and importance because it avoids craniotomy, takes less time for surgery, has fewer associated complications and infections, and can explore deep lesions, increasing the understanding of human functional neuroanatomy and enabling more precise localization of seizure zones.This article reviews the history of the development of cortical electrical stimulation technology, the intrinsic mechanisms, the value of the application of SEEG, and also provides a comprehensive comparison between SEEG and SDE, despite the irreplaceable advantages of SEEG, attention should be paid to the unresolved clinical and scientific issues of SEEG, and the establishment of a consensus-based clinical guideline, as the application of this technology will be more widely used in both clinical and scientific work.

1.	Beghi E. The Epidemiology of epilepsy. Neuroepidemiology, 2020, 54(2): 185-191.
2.	Tang F, Hartz AMS, Bauer B. Drug-resistant epilepsy: multiple hypotheses, few answers. Frontiers in Neurology, 2017, 8: 301.
3.	Thijs R D, Surges R, O’Brien T J, et al. Epilepsy in adults. The Lancet, 2019, 393(10172): 689-701.
4.	Arya R, Ervin B, Holloway T, et al. Electrical stimulation sensorimotor mapping with stereo-EEG. Clinical Neurophysiology, 2020, 131(8): 1691-1701.
5.	Isitan C, Yan Q, Spencer DD, et al. Brief history of electrical cortical stimulation: a journey in time from Volta to Penfield. Epilepsy Research, 2020, 166: 106363.
6.	Eadie M. Cortical epileptogenesis and David Ferrier. Journal of the History of the Neurosciences, 2018, 27(2): 107-116.
7.	Pearce JMS. Sir David Ferrier MD, FRS. Journal of Neurology, Neurosurgery, and Psychiatry, 2003, 74(6): 787.
8.	Feindel W, Leblanc R, De Almeida AN. Epilepsy surgery: historical highlights 1909–2009. Epilepsia, 2009, 50(s3): 131-151.
9.	Bancaud J, Talairach J, Morel P, et al. “Generalized” epileptic seizures elicited by electrical stimulation of the frontal lobe in man. Electroencephalography and Clinical Neurophysiology, 1974, 37(3): 275-282.
10.	Rattay F. The basic mechanism for the electrical stimulation of the nervous system. Neuroscience, 1999, 89(2): 335-346.
11.	Ranck JB. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Research, 1975, 98(3): 417-440.
12.	Nowak L G, Bullier J. Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. Experimental Brain Research, 1998, 118(4): 477-488.
13.	Kole MHP, Stuart GJ. Signal processing in the axon initial segment. Neuron, 2012, 73(2): 235-247.
14.	Jankowska E, Padel Y, Tanaka R. The mode of activation of pyramidal tract cells by intracortical stimuli. The Journal of Physiology, 1975, 249(3): 617-636.
15.	Canals S, Beyerlein M, Murayama Y, et al. Electric stimulation fMRI of the perforant pathway to the rat hippocampus. Magnetic Resonance Imaging, 2008, 26(7): 978-986.
16.	David O, Bastin J, Chabardès S, et al. Studying network mechanisms using intracranial stimulation in epileptic patients. Frontiers in Systems Neuroscience, 2010, 4: 15.
17.	Ezure K, Oshima T. Lateral spread of neuronal activity within the motor cortex investigated with intracellular responses to distant epicortical stimulation. The Japanese Journal of Physiology, 1985, 35(2): 223-249.
18.	Keller CJ, Honey CJ, Mégevand P, et al. Mapping human brain networks with cortico-cortical evoked potentials. Philosophical Transactions of the Royal Society B: Biological Sciences, 2014, 369(1653): 20130528.
19.	Li L, Kriukova K, Engel J, et al. Seizure development in the acute intrahippocampal epileptic focus. Scientific Reports, 2018, 8(1): 1423.
20.	Brodovskaya A, Shiono S, Kapur J. Activation of the basal ganglia and indirect pathway neurons during frontal lobe seizures. Brain, 2021, 144(7): 2074-2091.
21.	Jehi L, Morita-Sherman M, Love TE, et al. Comparative effectiveness of stereotactic electroencephalography versus subdural grids in epilepsy surgery. Annals of Neurology, 2021, 90(6): 927-939.
22.	Zijlmans M, Zweiphenning W, van Klink N. Changing concepts in presurgical assessment for epilepsy surgery. Neurology, 2019, 15(10): 594-606.
23.	Trébuchon A, Chauvel P. Electrical stimulation for seizure induction and functional mapping in stereoelectroencephalography. Journal of Clinical Neurophysiology, 2016, 33(6): 511-521.
24.	Perrone‐Bertolotti M, Alexandre S, Jobb A, et al. Probabilistic mapping of language networks from high frequency activity induced by direct electrical stimulation. Human Brain Mapping, 2020, 41(14): 4113-4126.
25.	Cuisenier P, Testud B, Minotti L, et al. Relationship between direct cortical stimulation and induced high-frequency activity for language mapping during SEEG recording. Journal of Neurosurgery, 2021, 134(3): 1251-1261.
26.	Arya R, Ervin B, Dudley J, et al. Electrical stimulation mapping of language with stereo-EEG. Epilepsy & Behavior, 2019, 99: 106395.
27.	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 Neurology, 2019, 76(9): 1070-1078.
28.	Sanchez-Larsen A, Principe A, Ley M, et al. Characterization of the insular role in cardiac function through intracranial electrical stimulation of the human insula. Annals of Neurology, 2021, 89(6): 1172-1180.
29.	Mariani V, Balestrini S, Gozzo F, et al. Intracerebral electrical stimulations of the temporal lobe: a stereoelectroencephalography study. European Journal of Neuroscience, 2021, 54(4): 5368-5383.
30.	Chassoux F, Navarro V, Catenoix H, et al. Planning and management of SEEG. Clinical Neurophysiology, 2018, 48(1): 25-37.
31.	Nathan SS, Sinha SR, Gordon B, et al. Determination of current density distributions generated by electrical stimulation of the human cerebral cortex. Electroencephalography and Clinical Neurophysiology, 1993, 86(3): 183-192.
32.	Arya R. Electrical stimulation mapping of brain function: a comparison of subdural electrodes and stereo-EEG. Frontiers in Human Neuroscience, 2020, 14: 102.
33.	Joshi S, Stephens E, Bleasel A, et al. Successful stereoelectroencephalography re-evaluation in epilepsy patients after failed initial subdural grid evaluation. Epileptic Disorders, 2023, 25(4): 534-544.
34.	Taussig D, Chipaux M, Fohlen M, et al. Invasive evaluation in children (SEEG vs subdural grids). Seizure, 2020, 77: 43-51.
35.	Jha R, Liu DD, Gerstl JVE, et al. Comparative effectiveness of stereotactic, subdural, or hybrid intracranial EEG monitoring in epilepsy surgery. Journal of Neurosurgery, 2024, 141(2): 372-380.
36.	Tandon N, Tong BA, Friedman ER, et al. Analysis of morbidity and outcomes associated with use of subdural grids vs stereoelectroencephalography in patients with intractable epilepsy. JAMA Neurology, 2019, 76(6): 672-681.
37.	Hu W H, Zhao B T, Zhang C, et al. Focal cortical dysplasia II-related seizures originate from the bottom of the dysplastic sulcus: a stereoelectroencephalography study. Clinical Neurophysiology, 2019, 130(9): 1596-1603.
38.	Macdonald-Laurs E, Maixner WJ, Bailey CA, et al. One-stage, limited-resection epilepsy surgery for bottom-of-sulcus dysplasia. Neurology, 2021, 97(2): e178-e190.
39.	Young JJ, Coulehan K, Fields MC, et al. Language mapping using electrocorticography versus stereoelectroencephalography: a case series. Epilepsy & Behavior, 2018, 84: 148-151.
40.	Männlin J, San Antonio-Arce V, Reinacher PC, et al. Safety profile of subdural and depth electrode implantations in invasive EEG exploration of drug-resistant focal epilepsy. Seizure, 2023, 110: 21-27.
41.	Talai A, Eschbach K, Stence NV, et al. Comparison of subdural grid and stereoelectroencephalography in a cohort of pediatric patients. Epilepsy Research, 2021, 177: 106758.
42.	Gomes FC, Larcipretti ALL, Udoma-Udofa OC, et al. Stereoelectroencephalography versus subdural electrodes for invasive monitoring of drug-resistant epilepsy patients: a systematic review and meta-analysis. Seizure, 2025, 129: 33-41.
43.	Cockle E, Rayner G, Malpas C, et al. An international survey of SEEG cortical stimulation practices. Epilepsia Open, 2023, 8(3): 1084-1095.

1. Beghi E. The Epidemiology of epilepsy. Neuroepidemiology, 2020, 54(2): 185-191.
2. Tang F, Hartz AMS, Bauer B. Drug-resistant epilepsy: multiple hypotheses, few answers. Frontiers in Neurology, 2017, 8: 301.
3. Thijs R D, Surges R, O’Brien T J, et al. Epilepsy in adults. The Lancet, 2019, 393(10172): 689-701.
4. Arya R, Ervin B, Holloway T, et al. Electrical stimulation sensorimotor mapping with stereo-EEG. Clinical Neurophysiology, 2020, 131(8): 1691-1701.
5. Isitan C, Yan Q, Spencer DD, et al. Brief history of electrical cortical stimulation: a journey in time from Volta to Penfield. Epilepsy Research, 2020, 166: 106363.
6. Eadie M. Cortical epileptogenesis and David Ferrier. Journal of the History of the Neurosciences, 2018, 27(2): 107-116.
7. Pearce JMS. Sir David Ferrier MD, FRS. Journal of Neurology, Neurosurgery, and Psychiatry, 2003, 74(6): 787.
8. Feindel W, Leblanc R, De Almeida AN. Epilepsy surgery: historical highlights 1909–2009. Epilepsia, 2009, 50(s3): 131-151.
9. Bancaud J, Talairach J, Morel P, et al. “Generalized” epileptic seizures elicited by electrical stimulation of the frontal lobe in man. Electroencephalography and Clinical Neurophysiology, 1974, 37(3): 275-282.
10. Rattay F. The basic mechanism for the electrical stimulation of the nervous system. Neuroscience, 1999, 89(2): 335-346.
11. Ranck JB. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Research, 1975, 98(3): 417-440.
12. Nowak L G, Bullier J. Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. Experimental Brain Research, 1998, 118(4): 477-488.
13. Kole MHP, Stuart GJ. Signal processing in the axon initial segment. Neuron, 2012, 73(2): 235-247.
14. Jankowska E, Padel Y, Tanaka R. The mode of activation of pyramidal tract cells by intracortical stimuli. The Journal of Physiology, 1975, 249(3): 617-636.
15. Canals S, Beyerlein M, Murayama Y, et al. Electric stimulation fMRI of the perforant pathway to the rat hippocampus. Magnetic Resonance Imaging, 2008, 26(7): 978-986.
16. David O, Bastin J, Chabardès S, et al. Studying network mechanisms using intracranial stimulation in epileptic patients. Frontiers in Systems Neuroscience, 2010, 4: 15.
17. Ezure K, Oshima T. Lateral spread of neuronal activity within the motor cortex investigated with intracellular responses to distant epicortical stimulation. The Japanese Journal of Physiology, 1985, 35(2): 223-249.
18. Keller CJ, Honey CJ, Mégevand P, et al. Mapping human brain networks with cortico-cortical evoked potentials. Philosophical Transactions of the Royal Society B: Biological Sciences, 2014, 369(1653): 20130528.
19. Li L, Kriukova K, Engel J, et al. Seizure development in the acute intrahippocampal epileptic focus. Scientific Reports, 2018, 8(1): 1423.
20. Brodovskaya A, Shiono S, Kapur J. Activation of the basal ganglia and indirect pathway neurons during frontal lobe seizures. Brain, 2021, 144(7): 2074-2091.
21. Jehi L, Morita-Sherman M, Love TE, et al. Comparative effectiveness of stereotactic electroencephalography versus subdural grids in epilepsy surgery. Annals of Neurology, 2021, 90(6): 927-939.
22. Zijlmans M, Zweiphenning W, van Klink N. Changing concepts in presurgical assessment for epilepsy surgery. Neurology, 2019, 15(10): 594-606.
23. Trébuchon A, Chauvel P. Electrical stimulation for seizure induction and functional mapping in stereoelectroencephalography. Journal of Clinical Neurophysiology, 2016, 33(6): 511-521.
24. Perrone‐Bertolotti M, Alexandre S, Jobb A, et al. Probabilistic mapping of language networks from high frequency activity induced by direct electrical stimulation. Human Brain Mapping, 2020, 41(14): 4113-4126.
25. Cuisenier P, Testud B, Minotti L, et al. Relationship between direct cortical stimulation and induced high-frequency activity for language mapping during SEEG recording. Journal of Neurosurgery, 2021, 134(3): 1251-1261.
26. Arya R, Ervin B, Dudley J, et al. Electrical stimulation mapping of language with stereo-EEG. Epilepsy & Behavior, 2019, 99: 106395.
27. 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 Neurology, 2019, 76(9): 1070-1078.
28. Sanchez-Larsen A, Principe A, Ley M, et al. Characterization of the insular role in cardiac function through intracranial electrical stimulation of the human insula. Annals of Neurology, 2021, 89(6): 1172-1180.
29. Mariani V, Balestrini S, Gozzo F, et al. Intracerebral electrical stimulations of the temporal lobe: a stereoelectroencephalography study. European Journal of Neuroscience, 2021, 54(4): 5368-5383.
30. Chassoux F, Navarro V, Catenoix H, et al. Planning and management of SEEG. Clinical Neurophysiology, 2018, 48(1): 25-37.
31. Nathan SS, Sinha SR, Gordon B, et al. Determination of current density distributions generated by electrical stimulation of the human cerebral cortex. Electroencephalography and Clinical Neurophysiology, 1993, 86(3): 183-192.
32. Arya R. Electrical stimulation mapping of brain function: a comparison of subdural electrodes and stereo-EEG. Frontiers in Human Neuroscience, 2020, 14: 102.
33. Joshi S, Stephens E, Bleasel A, et al. Successful stereoelectroencephalography re-evaluation in epilepsy patients after failed initial subdural grid evaluation. Epileptic Disorders, 2023, 25(4): 534-544.
34. Taussig D, Chipaux M, Fohlen M, et al. Invasive evaluation in children (SEEG vs subdural grids). Seizure, 2020, 77: 43-51.
35. Jha R, Liu DD, Gerstl JVE, et al. Comparative effectiveness of stereotactic, subdural, or hybrid intracranial EEG monitoring in epilepsy surgery. Journal of Neurosurgery, 2024, 141(2): 372-380.
36. Tandon N, Tong BA, Friedman ER, et al. Analysis of morbidity and outcomes associated with use of subdural grids vs stereoelectroencephalography in patients with intractable epilepsy. JAMA Neurology, 2019, 76(6): 672-681.
37. Hu W H, Zhao B T, Zhang C, et al. Focal cortical dysplasia II-related seizures originate from the bottom of the dysplastic sulcus: a stereoelectroencephalography study. Clinical Neurophysiology, 2019, 130(9): 1596-1603.
38. Macdonald-Laurs E, Maixner WJ, Bailey CA, et al. One-stage, limited-resection epilepsy surgery for bottom-of-sulcus dysplasia. Neurology, 2021, 97(2): e178-e190.
39. Young JJ, Coulehan K, Fields MC, et al. Language mapping using electrocorticography versus stereoelectroencephalography: a case series. Epilepsy & Behavior, 2018, 84: 148-151.
40. Männlin J, San Antonio-Arce V, Reinacher PC, et al. Safety profile of subdural and depth electrode implantations in invasive EEG exploration of drug-resistant focal epilepsy. Seizure, 2023, 110: 21-27.
41. Talai A, Eschbach K, Stence NV, et al. Comparison of subdural grid and stereoelectroencephalography in a cohort of pediatric patients. Epilepsy Research, 2021, 177: 106758.
42. Gomes FC, Larcipretti ALL, Udoma-Udofa OC, et al. Stereoelectroencephalography versus subdural electrodes for invasive monitoring of drug-resistant epilepsy patients: a systematic review and meta-analysis. Seizure, 2025, 129: 33-41.
43. Cockle E, Rayner G, Malpas C, et al. An international survey of SEEG cortical stimulation practices. Epilepsia Open, 2023, 8(3): 1084-1095.

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