Epilepsy surgery is the therapy of choice for many patients with drug-resistant focal epilepsy. Recognizing and describing ictal and interictal patterns with intracranial electroencephalography (EEG) recordings is important in order to most efficiently leverage advantages of this technique to accurately delineate the seizure-onset zone before undergoing surgery. In this seminar in epileptology, we address learning objective "1.4.11 Recognize and describe ictal and interictal patterns with intracranial recordings" of the International League against Epilepsy curriculum for epileptologists. We will review principal considerations of the implantation planning, summarize the literature for the most relevant ictal and interictal EEG patterns within and beyond the Berger frequency spectrum, review invasive stimulation for seizure and functional mapping, discuss caveats in the interpretation of intracranial EEG findings, provide an overview on special considerations in children and in subdural grids/strips, and review available quantitative/signal analysis approaches. To be as practically oriented as possible, we will provide a mini atlas of the most frequent EEG patterns, highlight pearls for its not infrequently challenging interpretation, and conclude with two illustrative case examples. This article shall serve as a useful learning resource for trainees in clinical neurophysiology/epileptology by providing a basic understanding on the concepts of invasive intracranial EEG.

Aarhus University Aarhus Denmark

Analytical Neurophysiology Lab Montreal Neurological Institute and Hospital Montreal Québec Canada

Behavioral and Social Neuroscience Research Group Central European Institute of Technology Masaryk University Brno Czechia

Bladin Berkovic Comprehensive Epilepsy Program Department of Neurology Austin Health Melbourne Victoria Australia

Brno Epilepsy Center Department of Neurology St Anne's University Hospital and Medical Faculty of Masaryk University Member of the ERN EpiCARE Brno Czechia

Danish Epilepsy Centre Dianalund Denmark

Department of Clinical Neurosciences CHUV Lausanne University Hospital Lausanne Switzerland

Department of Epileptology University Hospital Bonn Bonn Germany

Department of Neurology Alfred Health Melbourne Victoria Australia

Department of Neurology and Neurosurgery UMC Utrecht Brain Center University Medical Center Utrecht Utrecht the Netherlands

Department of Neurology Duke University Medical Center and Department of Biomedical Engineering Duke Pratt School of Engineering Durham North Carolina USA

Department of Neurology Feinberg School of Medicine Northwestern Memorial Hospital Chicago Illinois USA

Department of Neurology Medical University of Innsbruck Innsbruck Austria

Department of Neurology Royal Melbourne Hospital Melbourne Victoria Australia

Department of Neurology The University of Chicago Chicago Illinois USA

Department of Neurology University of Florida Gainesville Florida USA

Department of Neuroscience Central Clinical School Monash University Melbourne Victoria Australia

Department of Neurosciences Mater Misericordiae Hospital Brisbane Queensland Australia

Department of Paediatrics and Department of Neuroscience Cumming School of Medicine University of Calgary Calgary Alberta Canada

Epilepsy Research Centre Department of Medicine University of Melbourne Melbourne Victoria Australia

Hotchkiss Brain Institute and Alberta Children's Hospital Research Institute University of Calgary Calgary Alberta Canada

Mater Research Institute Faculty of Medicine University of Queensland St Lucia Queensland Australia

Neurophysiology Unit Institute of Neurosurgery Dr Asenjo Santiago Chile

Stichting Epilepsie Instellingen Nederland Heemstede The Netherlands

Wilder Center for Epilepsy Research University of Florida Gainesville Florida USA

See more in PubMed

Engel J. What can we do for people with drug-resistant epilepsy? The 2016 Wartenberg lecture. Neurology. 2016;87:2483-2489. https://doi.org/10.1212/WNL.0000000000003407

Vakharia VN, Duncan JS, Witt JA, Elger CE, Staba R, Engel J. Getting the best outcomes from epilepsy surgery. Ann Neurol. 2018;83:676-690. https://doi.org/10.1002/ANA.25205

Jayakar P, Gotman J, Harvey AS, Palmini A, Tassi L, Schomer D, et al. Diagnostic utility of invasive EEG for epilepsy surgery: indications, modalities, and techniques. Epilepsia. 2016;57:1735-1747. https://doi.org/10.1111/EPI.13515

Gavvala J, Zafar M, Sinha SR, Kalamangalam G, Schuele S. Stereotactic EEG practices: a survey of United States tertiary referral epilepsy centers. J Clin Neurophysiol. 2022;39:474-480. https://doi.org/10.1097/WNP.0000000000000794

Jehi L, Morita-Sherman M, Love TE, Bartolomei F, Bingaman W, Braun K, et al. Comparative effectiveness of stereotactic electroencephalography versus subdural grids in epilepsy surgery. Ann Neurol. 2021;90:927-939. https://doi.org/10.1002/ANA.26238

McGonigal A, Bartolomei F, Chauvel P. On seizure semiology. Epilepsia. 2021;62:2019-2035. https://doi.org/10.1111/EPI.16994

Bancaud J, Talairach J, Bonis A. La stéréo-électroencéphalographie dans l'épilepsie: informations neurophysiopathologiques apportées par l'investigation fonctionnelle stéréotaxique. Paris: Masson; 1965.

Rosenow F, Lüders H. Presurgical evaluation of epilepsy. Brain. 2001;124:1683-1700. https://doi.org/10.1093/BRAIN/124.9.1683

Kahane P, Landré E, Minotti L, Francione S, Ryvlin P. The Bancaud and Talairach view on the epileptogenic zone: a working hypothesis. Epileptic Disord. 2006;8(Suppl 2):S16-S26.

Chauvel P, Gonzalez-Martinez J, Bulacio J. Presurgical intracranial investigations in epilepsy surgery. Handb Clin Neurol. 2019;161:45-71. https://doi.org/10.1016/B978-0-444-64142-7.00040-0

Isnard J, Taussig D, Bartolomei F, Bourdillon P, Catenoix H, Chassoux F, et al. French guidelines on stereoelectroencephalography (SEEG). Neurophysiol Clin. 2018;48:5-13. https://doi.org/10.1016/J.NEUCLI.2017.11.005

Englot DJ. A modern epilepsy surgery treatment algorithm: incorporating traditional and emerging technologies. Epilepsy Behav. 2018;80:68-74. https://doi.org/10.1016/J.YEBEH.2017.12.041

Mirandola L, Mai RF, Francione S, Pelliccia V, Gozzo F, Sartori I, et al. Stereo-EEG: diagnostic and therapeutic tool for periventricular nodular heterotopia epilepsies. Epilepsia. 2017;58:1962-1971. https://doi.org/10.1111/EPI.13895

Bourdillon P, Cucherat M, Isnard J, Ostrowsky-Coste K, Catenoix H, Guénot M, et al. Stereo-electroencephalography-guided radiofrequency thermocoagulation in patients with focal epilepsy: a systematic review and meta-analysis. Epilepsia. 2018;59:2296-2304. https://doi.org/10.1111/EPI.14584

Gonzalez-Martinez J, Bulacio J, Alexopoulos A, Jehi L, Bingaman W, Najm I. Stereoelectroencephalography in the “difficult to localize” refractory focal epilepsy: early experience from a north American epilepsy center. Epilepsia. 2013;54:323-330. https://doi.org/10.1111/J.1528-1167.2012.03672.X

Hall JA, Khoo HM. Robotic-assisted and image-guided MRI-compatible Stereoelectroencephalography. Can J Neurol Sci. 2018;45:35-43. https://doi.org/10.1017/CJN.2017.240

Cardinale F, Rizzi M, Vignati E, Cossu M, Castana L, d'Orio P, et al. Stereoelectroencephalography: retrospective analysis of 742 procedures in a single centre. Brain. 2019;142:2688-2704. https://doi.org/10.1093/BRAIN/AWZ196

Astner-Rohracher A, Zimmermann G, Avigdor T, Abdallah C, Barot N, Brázdil M, et al. Development and validation of the 5-SENSE score to predict focality of the seizure-onset zone as assessed by Stereoelectroencephalography. JAMA Neurol. 2022;79:70-79. https://doi.org/10.1001/JAMANEUROL.2021.4405

Bartolomei F, Trébuchon A, Bonini F, Lambert I, Gavaret M, Woodman M, et al. What is the concordance between the seizure onset zone and the irritative zone? A SEEG quantified study. Clin Neurophysiol. 2016;127:1157-1162. https://doi.org/10.1016/J.CLINPH.2015.10.029

Lagarde S, Buzori S, Trebuchon A, Carron R, Scavarda D, Milh M, et al. The repertoire of seizure onset patterns in human focal epilepsies: determinants and prognostic values. Epilepsia. 2019;60:85-95. https://doi.org/10.1111/EPI.14604

Henkel A, Noachtar S, Pfänder M, Lüders HO. The localizing value of the abdominal aura and its evolution: a study in focal epilepsies. Neurology. 2002;58:271-276. https://doi.org/10.1212/WNL.58.2.271

Epstein CM. Digital EEG: trouble in paradise? J Clin Neurophysiol. 2006;23:190-193. https://doi.org/10.1097/01.WNP.0000220083.90279.22

Zelmann R, Frauscher B, Phellan Aro R, Gueziri H-E, Collins DL. SEEGAtlas: a framework for the identification and classification of depth electrodes using clinical images. J Neural Eng. 2023;20:20. https://doi.org/10.1088/1741-2552/ACD6BD

Kahane P, Minotti L, Hoffmann D, Lachaux JP, Ryvlin P. Invasive EEG in the definition of the seizure onset zone: depth electrodes. In: Rosenow F, Lüders HO, editors. Handbook of Clinical Neurophysiology, Vol. 3. Presurgical assessment of the epilepsies with clinical neurophysiology and functional imaging. Elsevier BV: Amsterdam; 2003. p. 109-133.

Sperling MR. Intracranial electroencephalography. In: Ebersole JS, Pedley TA, editors. Current Practice of Clinical Electroencephalography. 3rd ed. Philadelphia: Lippincott Williams & Wilkins; 2003.

Frauscher B, Von Ellenrieder N, Zelmann R, Doležalová I, Minotti L, Olivier A, et al. Atlas of the normal intracranial electroencephalogram: neurophysiological awake activity in different cortical areas. Brain. 2018;141:1130-1144. https://doi.org/10.1093/BRAIN/AWY035

Jasper H, Penfield W. Electrocorticograms in man: effect of voluntary movement upon the electrical activity of the precentral gyrus. Arch Psychiatr Nervenkr. 1949;183:163-174. https://doi.org/10.1007/BF01062488

Kural MA, Duez L, Sejer Hansen V, Larsson PG, Rampp S, Schulz R, et al. Criteria for defining interictal epileptiform discharges in EEG: a clinical validation study. Neurology. 2020;94:E2139-E2147. https://doi.org/10.1212/WNL.0000000000009439

Gloor P. Neuronal generators and the problem of localization in electroencephalography: application of volume conductor theory to electroencephalography. J Clin Neurophysiol. 1985;2:327-354. https://doi.org/10.1097/00004691-198510000-00002

Paredes-Aragon E, AlKhaldi NA, Ballesteros-Herrera D, Mirsattari SM. Stereo-encephalographic Presurgical evaluation of temporal lobe epilepsy: an evolving science. Front Neurol. 2022;13:867458. https://doi.org/10.3389/FNEUR.2022.867458

Palmini A, Gambardella A, Andermann F, Dubeau F, da Costa JC, Olivier A, et al. Intrinsic epileptogenicity of human dysplastic cortex as suggested by corticography and surgical results. Ann Neurol. 1995;37:476-487. https://doi.org/10.1002/ANA.410370410

Ferrier CH, Alarcon G, Engelsman J, Binnie CD, Koutroumanidis M, Polkey CE, et al. Relevance of residual histologic and electrocorticographic abnormalities for surgical outcome in frontal lobe epilepsy. Epilepsia. 2001;42:363-371. https://doi.org/10.1046/J.1528-1157.2001.06900.X

Shakhatreh L, Janmohamed M, Baker AA, Willard A, Laing J, Rychkova M, et al. Interictal and seizure-onset EEG patterns in malformations of cortical development: a systematic review. Neurobiol Dis. 2022;174:105863. https://doi.org/10.1016/J.NBD.2022.105863

Cuello-Oderiz C, von Ellenrieder N, Sankhe R, Olivier A, Hall J, Dubeau F, et al. Value of ictal and interictal epileptiform discharges and high frequency oscillations for delineating the epileptogenic zone in patients with focal cortical dysplasia. Clin Neurophysiol. 2018;129:1311-1319. https://doi.org/10.1016/J.CLINPH.2018.02.003

Francione S, Nobili L, Cardinale F, Citterio A, Galli C, Tassi L. Intra-lesional stereo-EEG activity in Taylor's focal cortical dysplasia. Epileptic Disord. 2003;5(Suppl 2):S105-S114.

Di Giacomo R, Uribe-San-Martin R, Mai R, Francione S, Nobili L, Sartori I, et al. Stereo-EEG ictal/interictal patterns and underlying pathologies. Seizure. 2019;72:54-60. https://doi.org/10.1016/J.SEIZURE.2019.10.001

Mohamed AR, Bailey CA, Freeman JL, Maixner W, Jackson GD, Harvey AS. Intrinsic epileptogenicity of cortical tubers revealed by intracranial EEG monitoring. Neurology. 2012;79:2249-2257. https://doi.org/10.1212/WNL.0B013E3182768923

Kannan L, Vogrin S, Bailey C, Maixner W, Harvey AS. Centre of epileptogenic tubers generate and propagate seizures in tuberous sclerosis. Brain. 2016;139:2653-2667. https://doi.org/10.1093/BRAIN/AWW192

Sklenarova B, Zatloukalova E, Cimbalnik J, Klimes P, Dolezalova I, Pail M, et al. Interictal High-Frequency Oscillations, Spikes, and Connectivity profiles: a Fingerprint of Epileptogenic Brain Pathologies. 2023.

Gnatkovsky V, Pelliccia V, de Curtis M, Tassi L. Two main focal seizure patterns revealed by intracerebral electroencephalographic biomarker analysis. Epilepsia. 2019;60:96-106. https://doi.org/10.1111/EPI.14610

Lee SA, Spencer DD, Spencer SS. Intracranial EEG seizure-onset patterns in neocortical epilepsy. Epilepsia. 2000;41:297-307. https://doi.org/10.1111/J.1528-1157.2000.TB00159.X

Kane N, Acharya J, Benickzy S, Caboclo L, Finnigan S, Kaplan PW, et al. A revised glossary of terms most commonly used by clinical electroencephalographers and updated proposal for the report format of the EEG findings. Revision 2017. Clin Neurophysiol Pract. 2017;2:170-185. https://doi.org/10.1016/J.CNP.2017.07.002

Perucca P, Dubeau F, Gotman J. Intracranial electroencephalographic seizure-onset patterns: effect of underlying pathology. Brain. 2014;137:183-196. https://doi.org/10.1093/BRAIN/AWT299

Faught E, Kuzniecky RI, Hurst DC. Ictal EEG wave forms from epidural electrodes predictive of seizure control after temporal lobectomy. Electroencephalogr Clin Neurophysiol. 1992;83:229-235. https://doi.org/10.1016/0013-4694(92)90116-Y

Spanedda F, Cendes F, Gotman J. Relations between EEG seizure morphology, interhemispheric spread, and mesial temporal atrophy in bitemporal epilepsy. Epilepsia. 1997;38:1300-1314. https://doi.org/10.1111/J.1528-1157.1997.TB00068.X

Wennberg R, Arruda F, Quesney LF, Olivier A. Preeminence of extrahippocampal structures in the generation of mesial temporal seizures: evidence from human depth electrode recordings. Epilepsia. 2002;43:716-726. https://doi.org/10.1046/J.1528-1157.2002.31101.X

Spencer SS, Guimaraes P, Katz A, Kim J, Spencer D. Morphological patterns of seizures recorded intracranially. Epilepsia. 1992;33:537-545. https://doi.org/10.1111/J.1528-1157.1992.TB01706.X

Velasco AL, Wilson CL, Babb TL, Engel J. Functional and anatomic correlates of two frequently observed temporal lobe seizure-onset patterns. Neural Plast. 2000;7:49-63. https://doi.org/10.1155/NP.2000.49

Schiller Y, Cascino GD, Busacker NE, Sharbrough FW. Characterization and comparison of local onset and remote propagated electrographic seizures recorded with intracranial electrodes. Epilepsia. 1998;39:380-388. https://doi.org/10.1111/J.1528-1157.1998.TB01390.X

Grinenko O, Li J, Mosher JC, Wang IZ, Bulacio JC, Gonzalez-Martinez J, et al. A fingerprint of the epileptogenic zone in human epilepsies. Brain. 2018;141:117-131. https://doi.org/10.1093/BRAIN/AWX306

Salami P, Peled N, Nadalin JK, Martinet LE, Kramer MA, Lee JW, et al. Seizure onset location shapes dynamics of initiation. Clin Neurophysiol. 2020;131:1782-1797. https://doi.org/10.1016/J.CLINPH.2020.04.168

Singh S, Sandy S, Wiebe S. Ictal onset on intracranial EEG: do we know it when we see it? State of the evidence. Epilepsia. 2015;56:1629-1638. https://doi.org/10.1111/EPI.13120

Alter AS, Dhamija R, McDonough TL, Shen S, McBrian DK, Mandel AM, et al. Ictal onset patterns of subdural intracranial electroencephalogram in children: how helpful for predicting epilepsy surgery outcome? Epilepsy Res. 2019;149:44-52. https://doi.org/10.1016/J.EPLEPSYRES.2018.10.008

Frauscher B, von Ellenrieder N, Dubeau F, Gotman J. Different seizure-onset patterns in mesiotemporal lobe epilepsy have a distinct interictal signature. Clin Neurophysiol. 2017;128:1282-1289. https://doi.org/10.1016/J.CLINPH.2017.04.020

Gastaut H, Broughton RJ. Epileptic Seizures: Clinical and Electrographic Features, Diagnosis and Treatment. Springfield, Illinois, USA: Charles C. Thomas Publisher; 1972.

Bartolomei F, Lagarde S, Wendling F, McGonigal A, Jirsa V, Guye M, et al. Defining epileptogenic networks: contribution of SEEG and signal analysis. Epilepsia. 2017;58:1131-1147. https://doi.org/10.1111/EPI.13791

Chauvel P, McGonigal A. Emergence of semiology in epileptic seizures. Epilepsy Behav. 2014;38:94-103. https://doi.org/10.1016/J.YEBEH.2013.12.003

Bartolomei F, Trébuchon A, Gavaret M, Régis J, Wendling F, Chauvel P. Acute alteration of emotional behaviour in epileptic seizures is related to transient desynchrony in emotion-regulation networks. Clin Neurophysiol. 2005;116:2473-2479. https://doi.org/10.1016/J.CLINPH.2005.05.013

Aupy J, Noviawaty I, Krishnan B, Suwankpakdee P, Bulacio J, Gonzalez-Martinez J, et al. Insulo-opercular cortex generates oroalimentary automatisms in temporal seizures. Epilepsia. 2018;59:583-594. https://doi.org/10.1111/EPI.14011

Zalta A, Hou JC, Thonnat M, Bartolomei F, Morillon B, McGonigal A. Neural correlates of rhythmic rocking in prefrontal seizures. Neurophysiol Clin. 2020;50:331-338. https://doi.org/10.1016/J.NEUCLI.2020.07.003

Bragin A, Engel J, Wilson CL, Fried I, Buzsáki G. High-frequency oscillations in human brain. Hippocampus. 1999;9:137-142. https://doi.org/10.1002/(sici)1098-1063(1999)9:2<137::aid-hipo5>3.0.co;2-0

van't Klooster MA, Van Klink NEC, Leijten FSS, Zelmann R, Gebbink TA, Gosselaar PH, et al. Residual fast ripples in the intraoperative corticogram predict epilepsy surgery outcome. Neurology. 2015;85:120-128. https://doi.org/10.1212/WNL.0000000000001727

Akiyama T, Otsubo H, Ochi A, Galicia EZ, Weiss SK, Donner EJ, et al. Topographic movie of ictal high-frequency oscillations on the brain surface using subdural EEG in neocortical epilepsy. Epilepsia. 2006;47:1953-1957. https://doi.org/10.1111/j.1528-1167.2006.00823.x

Zelmann R, Lina JM, Schulze-Bonhage A, Gotman J, Jacobs J. Scalp EEG is not a blur: it can see high frequency oscillations although their generators are small. Brain Topogr. 2014;27:683-704. https://doi.org/10.1007/S10548-013-0321-Y

RamachandranNair R, Ochi A, Imai K, Benifla M, Akiyama T, Holowka S, et al. Epileptic spasms in older pediatric patients: MEG and ictal high-frequency oscillations suggest focal-onset seizures in a subset of epileptic spasms. Epilepsy Res. 2008;78:216-224. https://doi.org/10.1016/J.EPLEPSYRES.2007.12.007

Foffani G, Uzcategui YG, Gal B, Menendez de la Prida L. Reduced spike-timing reliability correlates with the emergence of fast ripples in the rat epileptic hippocampus. Neuron. 2007;55:930-941. https://doi.org/10.1016/J.NEURON.2007.07.040

Jacobs J, LeVan P, Chander R, Hall J, Dubeau F, Gotman J. Interictal high-frequency oscillations (80-500 Hz) are an indicator of seizure onset areas independent of spikes in the human epileptic brain. Epilepsia. 2008;49:1893-1907. https://doi.org/10.1111/J.1528-1167.2008.01656.X

Brázdil M, Pail M, Halámek J, Plešinger F, Cimbálník J, Roman R, et al. Very high-frequency oscillations: novel biomarkers of the epileptogenic zone. Ann Neurol. 2017;82:299-310. https://doi.org/10.1002/ANA.25006

Fedele T, Burnos S, Boran E, Krayenbühl N, Hilfiker P, Grunwald T, et al. Resection of high frequency oscillations predicts seizure outcome in the individual patient. Sci Rep. 2017;7:13836. https://doi.org/10.1038/S41598-017-13064-1

Zhang Y, Chung H, Ngo JP, Monsoor T, Hussain SA, Matsumoto JH, et al. Characterizing physiological high-frequency oscillations using deep learning. J Neural Eng. 2022;19(6). https://doi.org/10.1088/1741-2552/aca4fa

Frauscher B, von Ellenrieder N, Zelmann R, Rogers C, Nguyen DK, Kahane P, et al. High-frequency oscillations in the Normal human brain. Ann Neurol. 2018;84:374-385. https://doi.org/10.1002/ANA.25304

Van Klink NEC, Van't Klooster MA, Zelmann R, Leijten FSS, Ferrier CH, Braun KPJ, et al. High frequency oscillations in intra-operative electrocorticography before and after epilepsy surgery. Clin Neurophysiol. 2014;125:2212-2219. https://doi.org/10.1016/J.CLINPH.2014.03.004

Alkawadri R, Gaspard N, Goncharova II, Spencer DD, Gerrard JL, Zaveri H, et al. The spatial and signal characteristics of physiologic high frequency oscillations. Epilepsia. 2014;55:1986-1995. https://doi.org/10.1111/EPI.12851

Pail M, Cimbálník J, Roman R, Daniel P, Shaw DJ, Chrastina J, et al. High frequency oscillations in epileptic and non-epileptic human hippocampus during a cognitive task. Sci Rep. 2020;10:18147. https://doi.org/10.1038/S41598-020-74306-3

Melani F, Zelmann R, Mari F, Gotman J. Continuous high frequency activity: a peculiar SEEG pattern related to specific brain regions. Clin Neurophysiol. 2013;124:1507-1516. https://doi.org/10.1016/J.CLINPH.2012.11.016

Mooij AH, Huiskamp GJM, Aarts E, Ferrier CH, Braun KPJ, Zijlmans M. Accurate differentiation between physiological and pathological ripples recorded with scalp-EEG. Clin Neurophysiol. 2022;143:172-181. https://doi.org/10.1016/J.CLINPH.2022.08.014

Zweiphenning W, van't Klooster MA, van Klink NEC, Leijten FSS, Ferrier CH, Gebbink T, et al. Intraoperative electrocorticography using high-frequency oscillations or spikes to tailor epilepsy surgery in The Netherlands (the HFO trial): a randomised, single-blind, adaptive non-inferiority trial. Lancet Neurol. 2022;21:982-993. https://doi.org/10.1016/S1474-4422(22)00311-8

Boran E, Ramantani G, Krayenbühl N, Schreiber M, König K, Fedele T, et al. High-density ECoG improves the detection of high frequency oscillations that predict seizure outcome. Clin Neurophysiol. 2019;130:1882-1888. https://doi.org/10.1016/J.CLINPH.2019.07.008

Zweiphenning WJEM, van Diessen E, Aarnoutse EJ, Leijten FSS, van Rijen PC, Braun KPJ, et al. The resolution revolution: comparing spikes and high frequency oscillations in high-density and standard intra-operative electrocorticography of the same patient. Clin Neurophysiol. 2020;131:1040-1043. https://doi.org/10.1016/J.CLINPH.2020.02.006

Thomas J, Kahane P, Abdallah C, Avigdor T, Zweiphenning WJEM, Chabardes S, et al. A subpopulation of spikes predicts successful epilepsy surgery outcome. Ann Neurol. 2023;93:522-535. https://doi.org/10.1002/ANA.26548

Ren L, Kucewicz MT, Cimbalnik J, Matsumoto JY, Brinkmann BH, Hu W, et al. Gamma oscillations precede interictal epileptiform spikes in the seizure onset zone. Neurology. 2015;84:602-608. https://doi.org/10.1212/WNL.0000000000001234

Gumnit RJ, Takahashi T. Changes in direct current activity during experimental focal seizures. Electroencephalogr Clin Neurophysiol. 1965;19:63-74. https://doi.org/10.1016/0013-4694(65)90007-6

Ikeda A, Taki W, Kunieda T, Terada K, Mikuni N, Nagamine T, et al. Focal ictal direct current shifts in human epilepsy as studied by subdural and scalp recording. Brain. 1999;122(Pt 5):827-838. https://doi.org/10.1093/BRAIN/122.5.827

Nakatani M, Inouchi M, Daifu-Kobayashi M, Murai T, Togawa J, Kajikawa S, et al. Ictal direct current shifts contribute to defining the core ictal focus in epilepsy surgery. Brain Commun. 2022;4:fcac222. https://doi.org/10.1093/BRAINCOMMS/FCAC222

Amzica F, Steriade M. Neuronal and glial membrane potentials during sleep and paroxysmal oscillations in the neocortex. J Neurosci. 2000;20:6648-6665. https://doi.org/10.1523/JNEUROSCI.20-17-06648.2000

Ikeda A, Takeyama H, Bernard C, Nakatani M, Shimotake A, Daifu M, et al. Active direct current (DC) shifts and “red slow”: two new concepts for seizure mechanisms and identification of the epileptogenic zone. Neurosci Res. 2020;156:95-101. https://doi.org/10.1016/J.NEURES.2020.01.014

Imamura H, Matsumoto R, Inouchi M, Matsuhashi M, Mikuni N, Takahashi R, et al. Ictal wideband ECoG: direct comparison between ictal slow shifts and high frequency oscillations. Clin Neurophysiol. 2011;122:1500-1504. https://doi.org/10.1016/J.CLINPH.2010.12.060

Hannan S, Ho A, Frauscher B. Clinical utility of sleep recordings during presurgical epilepsy evaluation with stereo-electroencephalography: a systematic review. J Clin Neurophysiol. 2023.

Ho A, Hannan S, Thomas J, Avigdor T, Abdallah C, Dubeau F, et al. Rapid eye movement sleep affects interictal epileptic activity differently in mesiotemporal and neocortical areas. Epilepsia. 2023;64:3036-3048. https://doi.org/10.1111/EPI.17763

Lambert I, Roehri N, Giusiano B, Carron R, Wendling F, Benar C, et al. Brain regions and epileptogenicity influence epileptic interictal spike production and propagation during NREM sleep in comparison with wakefulness. Epilepsia. 2018;59:235-243. https://doi.org/10.1111/EPI.13958

Fouad A, Azizollahi H, Le Douget JE, Lejeune FX, Valderrama M, Mayor L, et al. Interictal epileptiform discharges show distinct spatiotemporal and morphological patterns across wake and sleep. Brain Commun. 2022;4:fcac183. https://doi.org/10.1093/BRAINCOMMS/FCAC183

Frauscher B, Von Ellenrieder N, Dubeau F, Gotman J. EEG desynchronization during phasic REM sleep suppresses interictal epileptic activity in humans. Epilepsia. 2016;57:879-888. https://doi.org/10.1111/EPI.13389

Frauscher B, Von Ellenrieder N, Ferrari-Marinho T, Avoli M, Dubeau F, Gotman J. Facilitation of epileptic activity during sleep is mediated by high amplitude slow waves. Brain. 2015;138:1629-1641. https://doi.org/10.1093/BRAIN/AWV073

von Ellenrieder N, Dubeau F, Gotman J, Frauscher B. Physiological and pathological high-frequency oscillations have distinct sleep-homeostatic properties. Neuroimage Clin. 2017;14:566-573. https://doi.org/10.1016/J.NICL.2017.02.018

Ng M, Pavlova M. Why are seizures rare in rapid eye movement sleep? Review of the frequency of seizures in different sleep stages. Epilepsy Res Treat. 2013;2013:1-10. https://doi.org/10.1155/2013/932790

Hannan S, Thomas J, Jaber K, El Kosseifi C, Ho A, Abdallah C, et al. The Differing Effects of Sleep on Ictal and Interictal Network Dynamics in Drug-Resistant Epilepsy. Ann Neurol. 2023. https://doi.org/10.1002/ana.26796

Peter-Derex L, Klimes P, Latreille V, Bouhadoun S, Dubeau F, Frauscher B. Sleep disruption in epilepsy: ictal and Interictal epileptic activity matter. Ann Neurol. 2020;88:907-920. https://doi.org/10.1002/ANA.25884

Penfield W, Jasper HH Sequel to: Penfield W. Epilepsy and the functional anatomy of the human brain. 1954:896.

Gordon B, Lesser RP, Rance NE, Hart J, Webber R, Uematsu S, et al. Parameters for direct cortical electrical stimulation in the human: histopathologic confirmation. Electroencephalogr Clin Neurophysiol. 1990;75:371-377. https://doi.org/10.1016/0013-4694(90)90082-U

Prime D, Rowlands D, O'Keefe S, Dionisio S. Considerations in performing and analyzing the responses of cortico-cortical evoked potentials in stereo-EEG. Epilepsia. 2018;59:16-26. https://doi.org/10.1111/EPI.13939

Blume WT, Jones DC, Pathak P. Properties of after-discharges from cortical electrical stimulation in focal epilepsies. Clin Neurophysiol. 2004;115:982-989. https://doi.org/10.1016/j.clinph.2003.11.023

Munari C, Kahane P, Tassi L, Francione S, Hoffmann D, Lo Russo G, et al. Intracerebral low frequency electrical stimulation: a new tool for the definition of the “epileptogenic area”? Acta Neurochir Suppl (Wien). 1993;58:181-185. https://doi.org/10.1007/978-3-7091-9297-9_42

Chassoux F, Devaux B, Landré E, Turak B, Nataf F, Varlet P, et al. Stereoelectroencephalography in focal cortical dysplasia: a 3D approach to delineating the dysplastic cortex. Brain. 2000;123(Pt 8):1733-1751. https://doi.org/10.1093/BRAIN/123.8.1733

Sperling MR, O'Connor MJ. Auras and subclinical seizures: characteristics and prognostic significance. Ann Neurol. 1990;28:320-328. https://doi.org/10.1002/ANA.410280304

Gollwitzer S, Hopfengärtner R, Rössler K, Müller T, Olmes DG, Lang J, et al. Afterdischarges elicited by cortical electric stimulation in humans: when do they occur and what do they mean? Epilepsy Behav. 2018;87:173-179. https://doi.org/10.1016/J.YEBEH.2018.09.007

Cuello Oderiz C, Von Ellenrieder N, Dubeau F, Eisenberg A, Gotman J, Hall J, et al. Association of Cortical Stimulation-Induced Seizure with Surgical Outcome in patients with focal drug-resistant epilepsy. JAMA Neurol. 2019;76:1070-1078. https://doi.org/10.1001/JAMANEUROL.2019.1464

Trébuchon A, Chauvel P. Electrical stimulation for seizure induction and functional mapping in Stereoelectroencephalography. J Clin Neurophysiol. 2016;33:511-521. https://doi.org/10.1097/WNP.0000000000000313

McGonigal A, Lagarde S, Trébuchon-Dafonseca A, Roehri N, Bartolomei F. Early onset motor semiology in seizures triggered by cortical stimulation during SEEG. Epilepsy Behav. 2018;88:262-267. https://doi.org/10.1016/J.YEBEH.2018.09.017

Kovac S, Kahane P, Diehl B. Seizures induced by direct electrical cortical stimulation-Mechanisms and clinical considerations. Clin Neurophysiol. 2016;127:31-39. https://doi.org/10.1016/J.CLINPH.2014.12.009

Borchers S, Himmelbach M, Logothetis N, Karnath HO. Direct electrical stimulation of human cortex - the gold standard for mapping brain functions? Nat Rev Neurosci. 2011;13:63-70. https://doi.org/10.1038/NRN3140

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. https://doi.org/10.3389/FNHUM.2021.619521

Perrone-Bertolotti M, Alexandre S, Jobb AS, De Palma L, Baciu M, Mairesse MP, et al. Probabilistic mapping of language networks from high frequency activity induced by direct electrical stimulation. Hum Brain Mapp. 2020;41:4113-4126. https://doi.org/10.1002/HBM.25112

Tantawi M, Miao J, Matias C, Skidmore CT, Sperling MR, Sharan AD, et al. Gray matter sampling differences between subdural electrodes and Stereoelectroencephalography electrodes. Front Neurol. 2021;12:669406. https://doi.org/10.3389/FNEUR.2021.669406

Cossu M, Cardinale F, Colombo N, Mai R, Nobili L, Sartori I, et al. Stereoelectroencephalography in the presurgical evaluation of children with drug-resistant focal epilepsy. J Neurosurg. 2005;103:333-343. https://doi.org/10.3171/ped.2005.103.4.0333

Gupta K, Grover P, Abel TJ. Current conceptual understanding of the epileptogenic network from Stereoelectroencephalography-based connectivity inferences. Front Neurol. 2020;11:569699. https://doi.org/10.3389/FNEUR.2020.569699

Michalak AJ, Greenblatt A, Wu S, Tobochnik S, Dave H, Raghupathi R, et al. Seizure onset patterns predict outcome after stereo-electroencephalography-guided laser amygdalohippocampotomy. Epilepsia. 2023;64:1568-1581. https://doi.org/10.1111/EPI.17602

Shields JA, Greven ACM, Shivamurthy VKN, Dickey AS, Matthews RE, Laxpati NG, et al. Stereoelectroencephalography-guided radiofrequency ablation of the epileptogenic zone as a treatment and predictor of future success of further surgical intervention. Epilepsia. 2023;64:2081-2093. https://doi.org/10.1111/EPI.17673

Contento M, Pizzo F, López-Madrona VJ, Lagarde S, Makhalova J, Trébuchon A, et al. Changes in epileptogenicity biomarkers after stereotactic thermocoagulation. Epilepsia. 2021;62:2048-2059. https://doi.org/10.1111/EPI.16989

Simula S, Garnier E, Contento M, Pizzo F, Makhalova J, Lagarde S, et al. Changes in local and network brain activity after stereotactic thermocoagulation in patients with drug-resistant epilepsy. Epilepsia. 2023;64:1582-1593. https://doi.org/10.1111/EPI.17613

Tomlinson SB, Buch VP, Armstrong D, Kennedy BC. Stereoelectroencephalography in pediatric epilepsy surgery. J Korean Neurosurg Soc. 2019;62:302-312. https://doi.org/10.3340/JKNS.2019.0015

Taussig D, Chipaux M, Fohlen M, Dorison N, Bekaert O, Ferrand-Sorbets S, et al. Invasive evaluation in children (SEEG vs subdural grids). Seizure. 2020;77:43-51. https://doi.org/10.1016/J.SEIZURE.2018.11.008

Peltola ME, Liukkonen E, Granström ML, Paetau R, Kantola-Sorsa E, Valanne L, et al. The effect of surgery in encephalopathy with electrical status epilepticus during sleep. Epilepsia. 2011;52:602-609. https://doi.org/10.1111/J.1528-1167.2010.02783.X

Perry MS, Shandley S, Perelman M, Singh RK, Wong-Kisiel L, Sullivan J, et al. Surgical evaluation in children <3 years of age with drug-resistant epilepsy: patient characteristics, diagnostic utilization, and potential for treatment delays. Epilepsia. 2022;63:96-107. https://doi.org/10.1111/EPI.17124

Barba C, Mai R, Grisotto L, Gozzo F, Pellacani S, Tassi L, et al. Unilobar surgery for symptomatic epileptic spasms. Ann Clin Transl Neurol. 2016;4:36-45. https://doi.org/10.1002/ACN3.373

Liava A, Mai R, Tassi L, Cossu M, Sartori I, Nobili L, et al. Paediatric epilepsy surgery in the posterior cortex: a study of 62 cases. Epileptic Disord. 2014;16:141-173. https://doi.org/10.1684/EPD.2014.0648

Barkovich AJ. Concepts of myelin and myelination in neuroradiology. AJNR Am J Neuroradiol. 2000;21:1099-1109.

Kim W, Shen MY, Provenzano FA, Lowenstein DB, McBrian DK, Mandel AM, et al. The role of stereo-electroencephalography to localize the epileptogenic zone in children with nonlesional brain magnetic resonance imaging. Epilepsy Res. 2021;179:106828. https://doi.org/10.1016/J.EPLEPSYRES.2021.106828

Chipaux M, Dorfmüller G, Fohlen M, Dorison N, Metten MA, Delalande O, et al. Refractory spasms of focal onset-a potentially curable disease that should lead to rapid surgical evaluation. Seizure. 2017;51:163-170. https://doi.org/10.1016/J.SEIZURE.2017.08.010

de la Vaissière S, Milh M, Scavarda D, Carron R, Lépine A, Trébuchon A, et al. Cortical involvement in focal epilepsies with epileptic spasms. Epilepsy Res. 2014;108:1572-1580. https://doi.org/10.1016/J.EPLEPSYRES.2014.08.008

Neal A, Bouet R, Lagarde S, Ostrowsky-Coste K, Maillard L, Kahane P, et al. Epileptic spasms are associated with increased stereo-electroencephalography derived functional connectivity in tuberous sclerosis complex. Epilepsia. 2022;63:2359-2370. https://doi.org/10.1111/EPI.17353

Lagarde S, Bonini F, McGonigal A, Chauvel P, Gavaret M, Scavarda D, et al. Seizure-onset patterns in focal cortical dysplasia and neurodevelopmental tumors: relationship with surgical prognosis and neuropathologic subtypes. Epilepsia. 2016;57:1426-1435. https://doi.org/10.1111/EPI.13464

Zakaria T, Noe K, So E, Cascino GD, Wetjen N, Van Gompel JJ, et al. Scalp and intracranial EEG in medically intractable extratemporal epilepsy with normal MRI. ISRN Neurol. 2012;2012:1-9. https://doi.org/10.5402/2012/942849

Hyslop A, Duchowny M. Electrical stimulation mapping in children. Seizure. 2020;77:59-63. https://doi.org/10.1016/J.SEIZURE.2019.07.023

Taussig D, Chipaux M, Lebas A, Fohlen M, Bulteau C, Ternier J, et al. Stereo-electroencephalography (SEEG) in 65 children: an effective and safe diagnostic method for pre-surgical diagnosis, independent of age. Epileptic Disord. 2014;16:280-295. https://doi.org/10.1684/EPD.2014.0679

Chitoku S, Otsubo H, Harada Y, Jay V, Rutka JT, Weiss SK, et al. Extraoperative cortical stimulation of motor function in children. Pediatr Neurol. 2001;24:344-350. https://doi.org/10.1016/S0887-8994(01)00264-8

Jayakar P, Alvarez LA, Duchowny MS, Resnick TJ. A safe and effective paradigm to functionally map the cortex in childhood. J Clin Neurophysiol. 1992;9:288-293. https://doi.org/10.1097/00004691-199204010-00009

Van Gompel JJ, Worrell GA, Bell ML, Patrick TA, Cascino GD, Raffel C, et al. Intracranial electroencephalography with subdural grid electrodes: techniques, complications, and outcomes. Neurosurgery. 2008;63:498-505. https://doi.org/10.1227/01.NEU.0000324996.37228.F8

Sacino MF, Huang SS, Schreiber J, Gaillard WD, Oluigbo CO. Is the use of stereotactic electroencephalography safe and effective in children? A meta-analysis of the use of stereotactic electroencephalography in comparison to subdural grids for invasive epilepsy monitoring in pediatric subjects. Neurosurgery. 2019;84:1190-1200. https://doi.org/10.1093/NEUROS/NYY466

Arya R, Mangano FT, Horn PS, Holland KD, Rose DF, Glauser TA. Adverse events related to extraoperative invasive EEG monitoring with subdural grid electrodes: a systematic review and meta-analysis. Epilepsia. 2013;54:828-839. https://doi.org/10.1111/EPI.12073

Ojemann G, Ojemann J, Lettich E, Berger M. Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. J Neurosurg. 1989;71:316-326. https://doi.org/10.3171/JNS.1989.71.3.0316

Remick M, Akwayena E, Harford E, Chilukuri A, White GE, Abel TJ. Subdural electrodes versus stereoelectroencephalography for pediatric epileptogenic zone localization: a retrospective cohort study. Neurosurg Focus. 2022;53:E4. https://doi.org/10.3171/2022.7.FOCUS2269

Larrew T, Skoch J, Ihnen SKZ, Arya R, Holland KD, Tenney JR, et al. Comparison of outcomes after stereoelectroencephalography and subdural grid monitoring in pediatric tuberous sclerosis complex. Neurosurg Focus. 2022;53:E5. https://doi.org/10.3171/2022.7.FOCUS22335

Joswig H, Lau JC, Abdallat M, Parrent AG, MacDougall KW, McLachlan RS, et al. Stereoelectroencephalography versus subdural strip electrode implantations: feasibility, complications, and outcomes in 500 intracranial monitoring cases for drug-resistant epilepsy. Neurosurgery. 2020;87:E23-E30. https://doi.org/10.1093/NEUROS/NYAA112

Katz JS, Abel TJ. Stereoelectroencephalography versus subdural electrodes for localization of the epileptogenic zone: what is the evidence? Neurotherapeutics. 2019;16:59-66. https://doi.org/10.1007/S13311-018-00703-2

Lee AT, Nichols NM, Speidel BA, Fan JM, Cajigas I, Knowlton RC, et al. Modern intracranial electroencephalography for epilepsy localization with combined subdural grid and depth electrodes with low and improved hemorrhagic complication rates. J Neurosurg. 2022;138:1-7. https://doi.org/10.3171/2022.5.JNS221118

Takayama Y, Ikegaya N, Iijima K, Kimura Y, Yokosako S, Muraoka N, et al. Single-institutional experience of chronic intracranial electroencephalography based on the combined usage of subdural and depth electrodes. Brain Sci. 2021;11:1-17. https://doi.org/10.3390/BRAINSCI11030307

Oluigbo CO, Gaillard WD, Koubeissi MZ. The end justifies the means-a call for nuance in the increasing Nationwide adoption of Stereoelectroencephalography over subdural electrode monitoring in the surgical evaluation of intractable epilepsy. JAMA Neurol. 2022;79:221-222. https://doi.org/10.1001/JAMANEUROL.2021.4994

Tao JX, Wu S, Lacy M, Rose S, Issa NP, Yang CW, et al. Stereotactic EEG-guided laser interstitial thermal therapy for mesial temporal lobe epilepsy. J Neurol Neurosurg Psychiatry. 2018;89:542-548. https://doi.org/10.1136/JNNP-2017-316833

Bartolomei F, Chauvel P, Wendling F. Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. Brain. 2008;131:1818-1830. https://doi.org/10.1093/BRAIN/AWN111

Wendling F, Badier JM, Chauvel P, Coatrieux JL. A method to quantify invariant information in depth-recorded epileptic seizures. Electroencephalogr Clin Neurophysiol. 1997;102:472-485. https://doi.org/10.1016/S0013-4694(96)96633-3

David O, Blauwblomme T, Job AS, Chabards S, Hoffmann D, Minotti L, et al. Imaging the seizure onset zone with stereo-electroencephalography. Brain. 2011;134:2898-2911. https://doi.org/10.1093/BRAIN/AWR238

Gnatkovsky V, Francione S, Cardinale F, Mai R, Tassi L, Lo Russo G, et al. Identification of reproducible ictal patterns based on quantified frequency analysis of intracranial EEG signals. Epilepsia. 2011;52:477-488. https://doi.org/10.1111/J.1528-1167.2010.02931.X

Schindler K, Leung H, Elger CE, Lehnertz K. Assessing seizure dynamics by analysing the correlation structure of multichannel intracranial EEG. Brain. 2007;130:65-77. https://doi.org/10.1093/BRAIN/AWL304

Jirsa VK, Proix T, Perdikis D, Woodman MM, Wang H, Bernard C, et al. The virtual epileptic patient: individualized whole-brain models of epilepsy spread. Neuroimage. 2017;145:377-388. https://doi.org/10.1016/J.NEUROIMAGE.2016.04.049

Cao M, Galvis D, Vogrin SJ, Woods WP, Vogrin S, Wang F, et al. Virtual intracranial EEG signals reconstructed from MEG with potential for epilepsy surgery. Nat Commun. 2022;13:994. https://doi.org/10.1038/S41467-022-28640-X

Bernabei JM, Li A, Revell AY, Smith RJ, Gunnarsdottir KM, Ong IZ, et al. Quantitative approaches to guide epilepsy surgery from intracranial EEG. Brain. 2023;146:2248-2258. https://doi.org/10.1093/BRAIN/AWAD007

Multicentre analysis of seizure outcome predicted by removal of high-frequency oscillations

Prognostic value of the 5-SENSE Score to predict focality of the seizure-onset zone as assessed by stereoelectroencephalography: a prospective international multicentre validation study