Presurgical language mapping using event-related high-gamma activity: The Detroit procedure

A number of investigators have reported that event-related augmentation of high-gamma activity at 70-110 Hz on electrocorticography (ECoG) can localize functionally-important brain regions in children and adults who undergo epilepsy surgery. The advantages of ECoG-based language mapping over the gold-standard stimulation include: (i) lack of stimulation-induced seizures, (ii) better sensitivity of localization of language areas in young children, and (iii) shorter patient participant time. Despite its potential utility, ECoG-based language mapping is far less commonly practiced than stimulation mapping. Here, we have provided video presentations to explain, point-by-point, our own hardware setting and time-frequency analysis procedures. We also have provided standardized auditory stimuli, in multiple languages, ready to be used for ECoG-based language mapping. Finally, we discussed the technical aspects of ECoG-based mapping, including its pitfalls, to facilitate appropriate interpretation of the data.

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

[2]  R. Kass,et al.  Automatic correction of ocular artifacts in the EEG: a comparison of regression-based and component-based methods , 2004 .

[3]  B Milner,et al.  THE ROLE OF EARLY LEFT‐BRAIN INJURY IN DETERMINING LATERALIZATION OF CEREBRAL SPEECH FUNCTIONS , 1977, Annals of the New York Academy of Sciences.

[4]  J. Gotman,et al.  High-frequency changes during interictal spikes detected by time-frequency analysis , 2011, Clinical Neurophysiology.

[5]  Karsten Hoechstetter,et al.  BESA Source Coherence: A New Method to Study Cortical Oscillatory Coupling , 2003, Brain Topography.

[6]  Christian E Elger,et al.  Multitask electrical stimulation for cortical language mapping: Hints for necessity and economic mode of application , 2009, Epilepsia.

[7]  N. Logothetis,et al.  Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1 , 2006, Nature Neuroscience.

[8]  Nao Ninomiya,et al.  The 10th anniversary of journal of visualization , 2007, J. Vis..

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

[10]  O. Bertrand,et al.  Neural correlates of consolidation in working memory , 2007, Human brain mapping.

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

[12]  Nicole M. Long,et al.  Human intracranial high-frequency activity maps episodic memory formation in space and time , 2014, NeuroImage.

[13]  Sébastien M. Crouzet,et al.  Fast saccades toward faces: face detection in just 100 ms. , 2010, Journal of vision.

[14]  Rajesh P. N. Rao,et al.  Broadband changes in the cortical surface potential track activation of functionally diverse neuronal populations , 2014, NeuroImage.

[15]  J. Findlay,et al.  Rapid Detection of Person Information in a Naturalistic Scene , 2008, Perception.

[16]  Manuel R. Mercier,et al.  Evaluation of cortical local field potential diffusion in stereotactic electro-encephalography recordings: A glimpse on white matter signal , 2017, NeuroImage.

[17]  Philippe Kahane,et al.  Saccade Related Gamma-Band Activity in Intracerebral EEG: Dissociating Neural from Ocular Muscle Activity , 2009, Brain Topography.

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

[19]  Akitoshi Hanazawa,et al.  Occipital gamma-oscillations modulated during eye movement tasks: Simultaneous eye tracking and electrocorticography recording in epileptic patients , 2011, NeuroImage.

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

[21]  Emad N. Eskandar,et al.  Intra-stimulation discharges: An overlooked cortical electrographic entity triggered by direct electrical stimulation , 2015, Clinical Neurophysiology.

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

[23]  J. M. Lina,et al.  Recording and analysis techniques for high-frequency oscillations , 2012, Progress in Neurobiology.

[24]  Masaaki Nishida,et al.  Cortical glucose metabolism positively correlates with gamma-oscillations in nonlesional focal epilepsy , 2008, NeuroImage.

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

[26]  E. Niebur,et al.  Neural Correlates of High-Gamma Oscillations (60–200 Hz) in Macaque Local Field Potentials and Their Potential Implications in Electrocorticography , 2008, The Journal of Neuroscience.

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

[28]  W. Singer,et al.  Hemodynamic Signals Correlate Tightly with Synchronized Gamma Oscillations , 2005, Science.

[29]  Eishi Asano,et al.  Gamma activity modulated by picture and auditory naming tasks: Intracranial recording in patients with focal epilepsy , 2013, Clinical Neurophysiology.

[30]  Masaaki Nishida,et al.  Cortical gamma-oscillations modulated by listening and overt repetition of phonemes , 2010, NeuroImage.

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

[32]  Nathan E. Crone,et al.  Subdural electrodes , 2010, Clinical Neurophysiology.

[33]  W. Stacey,et al.  Effect of sampling rate and filter settings on High Frequency Oscillation detections , 2016, Clinical Neurophysiology.

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

[35]  Song Zhang,et al.  Ictal high‐frequency oscillations in neocortical epilepsy: implications for seizure localization and surgical resection , 2011, Epilepsia.

[36]  G. Alarcón,et al.  Lateralising Value of Neuropsychological Protocols for Presurgical Assessment of Temporal Lobe Epilepsy , 2003, Epilepsia.

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

[38]  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.

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

[40]  Andreas Schulze-Bonhage,et al.  Signal quality of simultaneously recorded invasive and non-invasive EEG , 2009, NeuroImage.

[41]  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.

[42]  Jeremy R. Manning,et al.  Broadband Shifts in Local Field Potential Power Spectra Are Correlated with Single-Neuron Spiking in Humans , 2009, The Journal of Neuroscience.

[43]  Tobias Loddenkemper,et al.  Atypical language lateralization in epilepsy patients , 2009, Epilepsia.

[44]  Christopher K. Kovach,et al.  Manifestation of ocular-muscle EMG contamination in human intracranial recordings , 2011, NeuroImage.

[45]  Jean Gotman,et al.  Ictal and interictal high frequency oscillations in patients with focal epilepsy , 2011, Clinical Neurophysiology.

[46]  Gerwin Schalk,et al.  Passive real-time identification of speech and motor cortex during an awake craniotomy , 2010, Epilepsy & Behavior.

[47]  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.

[48]  Eishi Asano,et al.  Human occipital cortices differentially exert saccadic suppression: Intracranial recording in children , 2013, NeuroImage.

[49]  R. Oostenveld,et al.  Neuronal Dynamics Underlying High- and Low-Frequency EEG Oscillations Contribute Independently to the Human BOLD Signal , 2011, Neuron.

[50]  Gerwin Schalk,et al.  Electrocorticographic Frequency Alteration Mapping for Extraoperative Localization of Speech Cortex , 2010, Neurosurgery.

[51]  J. Gotman,et al.  Effect of sleep stage on interictal high‐frequency oscillations recorded from depth macroelectrodes in patients with focal epilepsy , 2009, Epilepsia.

[52]  N. Logothetis,et al.  Frequency-Band Coupling in Surface EEG Reflects Spiking Activity in Monkey Visual Cortex , 2009, Neuron.

[53]  N Papp,et al.  Critical evaluation of complex demodulation techniques for the quantification of bioelectrical activity. , 1977, Biomedical sciences instrumentation.

[54]  Eishi Asano,et al.  Clinical significance and developmental changes of auditory-language-related gamma activity , 2013, Clinical Neurophysiology.

[55]  Eishi Asano,et al.  Statistical mapping of ictal high‐frequency oscillations in epileptic spasms , 2011, Epilepsia.

[56]  B. Rossion,et al.  Revisiting Snodgrass and Vanderwart's Object Pictorial Set: The Role of Surface Detail in Basic-Level Object Recognition , 2004, Perception.

[57]  Eishi Asano,et al.  Role of subdural electrocorticography in prediction of long-term seizure outcome in epilepsy surgery. , 2009, Brain : a journal of neurology.

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

[59]  Naoyuki Matsuzaki,et al.  Gamma activity modulated by naming of ambiguous and unambiguous images: Intracranial recording , 2015, Clinical Neurophysiology.

[60]  Josef Halámek,et al.  Intracerebrally recorded high frequency oscillations: Simple visual assessment versus automated detection , 2013, Clinical Neurophysiology.

[61]  Scott Makeig,et al.  Interictal high-frequency oscillations generated by seizure onset and eloquent areas may be differentially coupled with different slow waves , 2016, Clinical Neurophysiology.

[62]  C. Elger,et al.  Digital Photography and 3D MRI–based Multimodal Imaging for Individualized Planning of Resective Neocortical Epilepsy Surgery , 2002, Epilepsia.

[63]  Nobuhito Saito,et al.  Characteristic profiles of high gamma activity and blood oxygenation level-dependent responses in various language areas , 2013, NeuroImage.

[64]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

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

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