Electrical stimulation mapping of language with stereo-EEG

OBJECTIVE We prospectively validated stereo-electroencephalography (EEG) electrical stimulation mapping (ESM) of language against a reference standard of meta-analytic functional magnetic resonance imaging (fMRI) framework (Neurosynth). METHODS Language ESM was performed using 50 Hz, biphasic, bipolar, stimulation at 1-8 mA, with a picture naming task. Electrode contacts (ECs) were scored as ESM+ if ESM interfered with speech/language function. For each patient, presurgical MRI was transformed to a standard space and coregistered with computed tomographic (CT) scan to obtain EC locations. After whole-brain parcellation, this fused image data were intersected with three-dimensional language fMRI (Neurosynth), and each EC was classified as lying within/outside the fMRI language parcel. Diagnostic odds ratio (DOR) and other indices were estimated. Current thresholds for language inhibition and after-discharges (ADs) were analyzed using multivariable linear mixed models. RESULTS In 10 patients (5 females), aged 5.4-21.2 years, speech/language inhibition was noted with ESM on 87/304 (29%) ECs. Stereo-EEG language ESM was a valid classifier of fMRI (Neurosynth) language sites (DOR: 9.02, p < 0.0001), with high specificity (0.87) but poor sensitivity (0.57). Similar diagnostic indices were seen for ECs in frontal or posterior regions, and gray or white matter. Language threshold (3.1 ± 1.5 mA) was lower than AD threshold (4.0 ± 2.0 mA, p = 0.0001). Language and AD thresholds decreased with age and intelligence quotient. Electrical stimulation mapping triggered seizures/auras represented patients' habitual semiology with 1 Hz stimulation. CONCLUSIONS Stereo-EEG ESM can reliably identify cerebral parcels with/without language function but may under detect all language sites. We suggest a 50-Hz stimulation protocol for language ESM with stereo-EEG.

[1]  Adeen Flinker,et al.  Spatial-temporal functional mapping of language at the bedside with electrocorticography , 2016, Neurology.

[2]  M. Hamberger,et al.  Cortical Language Mapping in Epilepsy: A Critical Review , 2007, Neuropsychology Review.

[3]  Jeffrey R. Tenney,et al.  Language and motor function thresholds during pediatric extra-operative electrical cortical stimulation brain mapping , 2017, Clinical Neurophysiology.

[4]  Eishi Asano,et al.  Three- and four-dimensional mapping of speech and language in patients with epilepsy , 2017, Brain : a journal of neurology.

[5]  J. A. Wilson,et al.  Neuropsychological outcomes after resection of cortical sites with visual naming associated electrocorticographic high-gamma modulation , 2019, Epilepsy Research.

[6]  Michael L Lipton,et al.  Note: This Copy Is for Your Personal, Non-commercial Use Only. to Order Presentation-ready Copies for Distribution to Your Colleagues or Clients, Contact Us at Www.rsna.org/rsnarights. Materials and Methods , 2022 .

[7]  Jorge Gonzalez-Martinez,et al.  Is SEEG safe? A systematic review and meta‐analysis of stereo‐electroencephalography–related complications , 2016, Epilepsia.

[8]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[9]  Jeffrey R. Tenney,et al.  After-discharges and seizures during pediatric extra-operative electrical cortical stimulation functional brain mapping: Incidence, thresholds, and determinants , 2017, Clinical Neurophysiology.

[10]  Jeffrey W Britton,et al.  Electrical Stimulation Mapping With Stereo-EEG Electrodes. , 2018, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[11]  Nathan E. Crone,et al.  ECoG high-gamma modulation versus electrical stimulation for presurgical language mapping , 2018, Epilepsy & Behavior.

[12]  R. Rothermel,et al.  Four‐dimensional functional cortical maps of visual and auditory language: Intracranial recording , 2019, Epilepsia.

[13]  William H Theodore,et al.  Language functional MRI and direct cortical stimulation in epilepsy preoperative planning , 2017, Annals of neurology.

[14]  Mitchel S Berger,et al.  Functional outcome after language mapping for glioma resection. , 2008, The New England journal of medicine.

[15]  Orrin Devinsky,et al.  Pediatric Language Mapping: Sensitivity of Neurostimulation and Wada Testing in Epilepsy Surgery , 2007, Epilepsia.

[16]  G. Klem,et al.  Extraoperative Cortical Functional Localization in Patients with Epilepsy , 1987, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[17]  Fosphenytoin pre-medication for pediatric extra-operative electrical stimulation brain mapping , 2018, Epilepsy Research.

[18]  R P Lesser,et al.  Cortical Afterdischarge and Functional Response Thresholds: Results of Extraoperative Testing , 1984, Epilepsia.

[19]  Lorella Minotti,et al.  French guidelines on stereoelectroencephalography (SEEG) , 2017, Neurophysiologie Clinique.

[20]  J. A. Wilson,et al.  Development of information sharing in language neocortex in childhood‐onset drug‐resistant epilepsy , 2019, Epilepsia.

[21]  Francesco Cardinale,et al.  Stereoelectroencephalography in the Presurgical Evaluation of Focal Epilepsy: A Retrospective Analysis of 215 Procedures , 2005, Neurosurgery.

[22]  N. Jausovec,et al.  Differences in event-related and induced brain oscillations in the theta and alpha frequency bands related to human intelligence , 2000, Neuroscience Letters.

[23]  J. B. Ranck,et al.  Which elements are excited in electrical stimulation of mammalian central nervous system: A review , 1975, Brain Research.

[24]  E. Asano,et al.  How to establish causality in epilepsy surgery , 2013, Brain and Development.

[25]  Patrick Chauvel,et al.  Electrical Stimulation for Seizure Induction and Functional Mapping in Stereoelectroencephalography , 2016, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[26]  Costanza Papagno,et al.  Is Preoperative Functional Magnetic Resonance Imaging Reliable for Language Areas Mapping in Brain Tumor Surgery? Review of Language Functional Magnetic Resonance Imaging and Direct Cortical Stimulation Correlation Studies , 2010, Neurosurgery.

[27]  H. Otsubo,et al.  Extraoperative cortical stimulation of motor function in children. , 2001, Pediatric neurology.

[28]  W. Blume,et al.  Properties of after-discharges from cortical electrical stimulation in focal epilepsies , 2004, Clinical Neurophysiology.

[29]  J. H. Cross,et al.  Diagnostic test utilization in evaluation for resective epilepsy surgery in children , 2014, Epilepsia.

[30]  J. Durand,et al.  Variability of intraoperative electrostimulation parameters in conscious individuals: language cortex. , 2017, Journal of neurosurgery.

[31]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[32]  Anthony M. Norcia,et al.  In‐vivo measurements of human brain tissue conductivity using focal electrical current injection through intracerebral multicontact electrodes , 2017, Human brain mapping.

[33]  Ravindra Arya,et al.  Adverse events related to extraoperative invasive EEG monitoring with subdural grid electrodes: A systematic review and meta‐analysis , 2013, Epilepsia.

[34]  Johannes B Reitsma,et al.  Can fMRI safely replace the Wada test for preoperative assessment of language lateralisation? A meta-analysis and systematic review , 2013, Journal of Neurology, Neurosurgery & Psychiatry.

[35]  L. Nobili,et al.  Stereo-EEG in children , 2006, Child's Nervous System.

[36]  F. Rattay,et al.  The basic mechanism for the electrical stimulation of the nervous system , 1999, Neuroscience.

[37]  V. Navarro,et al.  Planning and management of SEEG , 2017, Neurophysiologie Clinique.