ECoG high-gamma modulation versus electrical stimulation for presurgical language mapping

OBJECTIVE This meta-analysis compared diagnostic validity of electrocorticographic (ECoG) high-γ modulation (HGM) with electrical stimulation mapping (ESM) for presurgical language localization. METHODS From a structured literature search, studies with electrode level data comparing ECoG HGM and ESM for language localization were included in the meta-analysis. Outcomes included global measures of diagnostic validity: area under the summary receiver operating characteristic (SROC) curve (AUC), and diagnostic odds ratio (DOR); as well as pooled estimates of sensitivity and specificity. Clinical and technical determinants of sensitivity/specificity were explored. RESULTS Fifteen studies were included in qualitative synthesis, and 10 studies included in the meta-analysis (number of patients 1-17, mean age 10.3-53.6years). Overt picture naming was the most commonly used task for language mapping with either method. Electrocorticographic high-γ modulation was analyzed at 50-400Hz with different bandwidths in individual studies. For ESM, pulse duration, train duration, and maximum current varied greatly among studies. Sensitivity (0.23-0.99), specificity (0.48-0.96), and DOR (1.45-376.28) varied widely across studies. The pooled estimates are: sensitivity 0.61 (95% CI 0.44, 0.76), specificity 0.79 (95% CI 0.68, 0.88), and DOR 6.44 (95% CI 3.47, 11.94). Area under the SROC curve was 0.77. Results of bivariate meta-regression were limited by small samples for individual variables. CONCLUSION Electrocorticographic high-γ modulation is a specific but not sensitive method for language localization compared with gold-standard ESM. Given the pooled DOR of 6.44 and AUC of 0.77, ECoG HGM can fairly reliably ascertain electrodes overlying ESM cortical language sites.

[1]  D. Altman,et al.  Measuring inconsistency in meta-analyses , 2003, BMJ : British Medical Journal.

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

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

[4]  Nick F. Ramsey,et al.  Mismatch Between Electrocortical Stimulation and Electrocorticography Frequency Mapping of Language , 2013, Brain Stimulation.

[5]  Gerwin Schalk,et al.  Real-time functional mapping: potential tool for improving language outcome in pediatric epilepsy surgery. , 2014, Journal of neurosurgery. Pediatrics.

[6]  O. Bertrand,et al.  Relationship between task‐related gamma oscillations and BOLD signal: New insights from combined fMRI and intracranial EEG , 2007, Human brain mapping.

[7]  G Ojemann,et al.  Human language cortex: localization of memory, syntax, and sequential motor-phoneme identification systems. , 1979, Science.

[8]  J. A. Wilson,et al.  Presurgical language localization with visual naming associated ECoG high‐ gamma modulation in pediatric drug‐resistant epilepsy , 2017, Epilepsia.

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

[10]  R P Lesser,et al.  Cognitive Effects of Resecting Basal Temporal Language Areas , 1996, Epilepsia.

[11]  Michael H Kohrman,et al.  ECoG gamma activity during a language task: differentiating expressive and receptive speech areas. , 2008, Brain : a journal of neurology.

[12]  R. Goodman,et al.  Anatomic dissociation of auditory and visual naming in the lateral temporal cortex , 2001, Neurology.

[13]  George A. Ojemann,et al.  Electrical stimulation and the neurobiology of language , 1983, Behavioral and Brain Sciences.

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

[15]  B. Gordon,et al.  Induced electrocorticographic gamma activity during auditory perception , 2001, Clinical Neurophysiology.

[16]  I. Módy,et al.  High-frequency oscillations : What is normal and what is not ? , 2008 .

[17]  C. Crainiceanu,et al.  Electrocorticographic high gamma activity versus electrical cortical stimulation mapping of naming. , 2005, Brain : a journal of neurology.

[18]  I. J. P. Howard Meta-Analysis withR , 2015 .

[19]  Christoph Guger,et al.  Clinical Impact and Implication of Real-Time Oscillation Analysis for Language Mapping. , 2017, World neurosurgery.

[20]  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.

[21]  N. Crone,et al.  Cortical γ responses: searching high and low. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[22]  Nathan E. Crone,et al.  Electrocorticographic language mapping in children by high-gamma synchronization during spontaneous conversation: Comparison with conventional electrical cortical stimulation , 2015, Epilepsy Research.

[23]  Eishi Asano,et al.  Multimodality language mapping in patients with left-hemispheric language dominance on Wada test , 2012, Clinical Neurophysiology.

[24]  Christoph Guger,et al.  Passive language mapping combining real-time oscillation analysis with cortico-cortical evoked potentials for awake craniotomy. , 2016, Journal of neurosurgery.

[25]  Johanna Ruescher,et al.  Somatotopic mapping of natural upper- and lower-extremity movements and speech production with high gamma electrocorticography , 2013, NeuroImage.

[26]  N. Laird,et al.  Meta-analysis in clinical trials. , 1986, Controlled clinical trials.

[27]  P. Gosselaar,et al.  Electrocorticographic language mapping with a listening task consisting of alternating speech and music phrases , 2016, Clinical Neurophysiology.

[28]  Piotr J. Franaszczuk,et al.  Electrocorticographic functional mapping identifies human cortex critical for auditory and visual naming , 2013, NeuroImage.

[29]  Andrew C. Papanicolaou,et al.  Language mapping using high gamma electrocorticography, fMRI, and TMS versus electrocortical stimulation , 2016, Clinical Neurophysiology.

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

[31]  Kai J Miller,et al.  Rapid online language mapping with electrocorticography. , 2011, Journal of neurosurgery. Pediatrics.

[32]  N. Crone,et al.  High-frequency gamma oscillations and human brain mapping with electrocorticography. , 2006, Progress in brain research.

[33]  Ettore Lettich,et al.  Cortical stimulation mapping of language cortex by using a verb generation task: effects of learning and comparison to mapping based on object naming. , 2002, Journal of neurosurgery.

[34]  G. Ojemann,et al.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. 1989. , 2008, Journal of neurosurgery.

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

[36]  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.

[37]  T. Yoshimoto,et al.  Remote discharges in the posterior language area during basal temporal stimulation , 2000, Neuroreport.

[38]  R. Irizarry,et al.  Electrocorticographic gamma activity during word production in spoken and sign language , 2001, Neurology.

[39]  C. M. Michel,et al.  Comparison of high gamma electrocorticography and fMRI with electrocortical stimulation for localization of somatosensory and language cortex , 2014, Clinical Neurophysiology.

[40]  Johannes B Reitsma,et al.  Bivariate analysis of sensitivity and specificity produces informative summary measures in diagnostic reviews. , 2005, Journal of clinical epidemiology.