Intraoperative mapping of expressive language cortex using passive real-time electrocorticography

In this case report, we investigated the utility and practicality of passive intraoperative functional mapping of expressive language cortex using high-resolution electrocorticography (ECoG). The patient presented here experienced new-onset seizures caused by a medium-grade tumor in very close proximity to expressive language regions. In preparation of tumor resection, the patient underwent multiple functional language mapping procedures. We examined the relationship of results obtained with intraoperative high-resolution ECoG, extraoperative ECoG utilizing a conventional subdural grid, extraoperative electrical cortical stimulation (ECS) mapping, and functional magnetic resonance imaging (fMRI). Our results demonstrate that intraoperative mapping using high-resolution ECoG is feasible and, within minutes, produces results that are qualitatively concordant to those achieved by extraoperative mapping modalities. They also suggest that functional language mapping of expressive language areas with ECoG may prove useful in many intraoperative conditions given its time efficiency and safety. Finally, they demonstrate that integration of results from multiple functional mapping techniques, both intraoperative and extraoperative, may serve to improve the confidence in or precision of functional localization when pathology encroaches upon eloquent language cortex.

[1]  J W Belliveau,et al.  Location of language in the cortex: a comparison between functional MR imaging and electrocortical stimulation. , 1997, AJNR. American journal of neuroradiology.

[2]  J. Ojemann,et al.  Electrocorticographic sensorimotor mapping , 2013, Clinical Neurophysiology.

[3]  Gerwin Schalk,et al.  Localizing ECoG electrodes on the cortical anatomy without post-implantation imaging , 2014, NeuroImage: Clinical.

[4]  T M Peters,et al.  Localization of somatosensory function by using positron emission tomography scanning: a comparison with intraoperative cortical stimulation. , 1999, Journal of neurosurgery.

[5]  Guy Marchal,et al.  Multimodality image registration by maximization of mutual information , 1997, IEEE Transactions on Medical Imaging.

[6]  Alexandra Golby,et al.  FUNCTIONAL BRAIN MAPPING AND ITS APPLICATIONS TO NEUROSURGERY , 2007, Neurosurgery.

[7]  B. Scheithauer,et al.  Prospective randomized trial of low- versus high-dose radiation therapy in adults with supratentorial low-grade glioma: initial report of a North Central Cancer Treatment Group/Radiation Therapy Oncology Group/Eastern Cooperative Oncology Group study. , 2002, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

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

[9]  Andrew W McEvoy,et al.  Presurgical functional mapping with functional MRI , 2008, Current opinion in neurology.

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

[11]  J. R. Wolpaw,et al.  Brain–computer interfaces (BCIs): Detection instead of classification , 2008, Journal of Neuroscience Methods.

[12]  D. Wechsler,et al.  Wechsler Adult Intelligence Scale—Fourth Edition (WAIS-IV) , 2010 .

[13]  John O. Willis,et al.  Wechsler Adult Intelligence Scale–Fourth Edition , 2014 .

[14]  Gerwin Schalk,et al.  NeuralAct: A Tool to Visualize Electrocortical (ECoG) Activity on a Three-Dimensional Model of the Cortex , 2015, Neuroinformatics.

[15]  H J Reulen,et al.  [Tumor surgery of the speech cortex in local anesthesia. Neuropsychological and neurophysiological monitoring during operations in the dominant hemisphere]. , 1997, Der Nervenarzt.

[16]  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.

[17]  P Kahane,et al.  Intracranial EEG and human brain mapping , 2003, Journal of Physiology-Paris.

[18]  G. Schalk,et al.  ELECTROCORTICOGRAPHIC FREQUENCY ALTERATION MAPPING: A CLINICAL TECHNIQUE FOR MAPPING THE MOTOR CORTEX , 2007, Neurosurgery.

[19]  Rajesh P. N. Rao,et al.  Real-time functional brain mapping using electrocorticography , 2007, NeuroImage.

[20]  N. Ramsey,et al.  Neurophysiologic correlates of fMRI in human motor cortex , 2012, Human brain mapping.

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

[22]  W. Freeman,et al.  Spatial spectral analysis of human electrocorticograms including the alpha and gamma bands , 2000, Journal of Neuroscience Methods.

[23]  W. Penfield,et al.  SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION , 1937 .

[24]  K. Boulanouar,et al.  Language Functional Magnetic Resonance Imaging in Preoperative Assessment of Language Areas: Correlation with Direct Cortical Stimulation , 2003, Neurosurgery.

[25]  Horst Bischof,et al.  A practical procedure for real-time functional mapping of eloquent cortex using electrocorticographic signals in humans , 2009, Epilepsy & Behavior.

[26]  Nader Pouratian,et al.  Utility of preoperative functional magnetic resonance imaging for identifying language cortices in patients with vascular malformations. , 2002, Journal of neurosurgery.

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

[28]  David Brauge,et al.  Awake Craniotomy vs Surgery Under General Anesthesia for Resection of Supratentorial Lesions , 2011, Neurosurgery.

[29]  Paul Ferrari,et al.  Preoperative magnetic source imaging for brain tumor surgery: a quantitative comparison with intraoperative sensory and motor mapping. , 2002, Neurosurgical focus.

[30]  J A Maldjian,et al.  Decreased BOLD functional MR activation of the motor and sensory cortices adjacent to a glioblastoma multiforme: implications for image-guided neurosurgery. , 1999, AJNR. American journal of neuroradiology.

[31]  N. Anderson,et al.  Electrocorticographic Frequency Alteration Mapping of Speech Cortex during an Awake Craniotomy: Case Report , 2009, Stereotactic and Functional Neurosurgery.

[32]  David T. Bundy,et al.  Microscale recording from human motor cortex: implications for minimally invasive electrocorticographic brain-computer interfaces. , 2009, Neurosurgical focus.

[33]  Rajesh P. N. Rao,et al.  Spectral Changes in Cortical Surface Potentials during Motor Movement , 2007, The Journal of Neuroscience.

[34]  P. Bucy,et al.  American Association of Neurological Surgeons , 1986 .

[35]  G A Ojemann,et al.  Electrocorticographic (ECoG) correlates of language. I. Desynchronization in temporal language cortex during object naming. , 1989, Electroencephalography and clinical neurophysiology.

[36]  C. Nimsky,et al.  Functional neuronavigation with magnetoencephalography: outcome in 50 patients with lesions around the motor cortex. , 1999, Journal of neurosurgery.

[37]  G Pfurtscheller,et al.  Visualization of significant ERD/ERS patterns in multichannel EEG and ECoG data , 2002, Clinical Neurophysiology.

[38]  Paul Ferrari,et al.  Preoperative magnetic source imaging for brain tumor surgery: a quantitative comparison with intraoperative sensory and motor mapping. , 2003, Journal of neurosurgery.

[39]  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.

[40]  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.

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

[42]  J. Maunsell,et al.  Different Origins of Gamma Rhythm and High-Gamma Activity in Macaque Visual Cortex , 2011, PLoS biology.

[43]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[44]  D J Weber,et al.  Human motor cortical activity recorded with Micro-ECoG electrodes, during individual finger movements , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[45]  Adam Wilson,et al.  A Procedure for Measuring Latencies in Brain–Computer Interfaces , 2010, IEEE Transactions on Biomedical Engineering.

[46]  A. Bizzi,et al.  Presurgical functional MR imaging of language and motor functions: validation with intraoperative electrocortical mapping. , 2008, Radiology.

[47]  J Hennig,et al.  The influence of gliomas and nonglial space-occupying lesions on blood-oxygen-level-dependent contrast enhancement. , 2000, AJNR. American journal of neuroradiology.

[48]  Nick F. Ramsey,et al.  Automated electrocorticographic electrode localization on individually rendered brain surfaces , 2010, Journal of Neuroscience Methods.

[49]  N. F. Ramsey,et al.  Reproducibility of fMRI-Determined Language Lateralization in Individual Subjects , 2002, Brain and Language.

[50]  H. Noordmans,et al.  Development of a functional magnetic resonance imaging protocol for intraoperative localization of critical temporoparietal language areas , 2002, Annals of neurology.

[51]  N. Birbaumer,et al.  BCI2000: a general-purpose brain-computer interface (BCI) system , 2004, IEEE Transactions on Biomedical Engineering.

[52]  G. Ojemann Cortical organization of language , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[53]  N. F. Ramsey,et al.  Task-free electrocorticography frequency mapping of the motor cortex , 2013, Clinical Neurophysiology.

[54]  Jeffrey G. Ojemann,et al.  Power-Law Scaling in the Brain Surface Electric Potential , 2009, PLoS Comput. Biol..

[55]  Isaiah Norton,et al.  Special surgical considerations for functional brain mapping. , 2011, Neurosurgery clinics of North America.