Individualized localization and cortical surface-based registration of intracranial electrodes

In addition to its widespread clinical use, the intracranial electroencephalogram (iEEG) is increasingly being employed as a tool to map the neural correlates of normal cognitive function as well as for developing neuroprosthetics. Despite recent advances, and unlike other established brain-mapping modalities (e.g. functional MRI, magneto- and electroencephalography), registering the iEEG with respect to neuroanatomy in individuals-and coregistering functional results across subjects-remains a significant challenge. Here we describe a method which coregisters high-resolution preoperative MRI with postoperative computerized tomography (CT) for the purpose of individualized functional mapping of both normal and pathological (e.g., interictal discharges and seizures) brain activity. Our method accurately (within 3mm, on average) localizes electrodes with respect to an individual's neuroanatomy. Furthermore, we outline a principled procedure for either volumetric or surface-based group analyses. We demonstrate our method in five patients with medically-intractable epilepsy undergoing invasive monitoring of the seizure focus prior to its surgical removal. The straight-forward application of this procedure to all types of intracranial electrodes, robustness to deformations in both skull and brain, and the ability to compare electrode locations across groups of patients makes this procedure an important tool for basic scientists as well as clinicians.

[1]  Biyu J. He,et al.  Electrophysiological correlates of the brain's intrinsic large-scale functional architecture , 2008, Proceedings of the National Academy of Sciences.

[2]  A. Engel,et al.  Invasive recordings from the human brain: clinical insights and beyond , 2005, Nature Reviews Neuroscience.

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

[4]  M A Viergever,et al.  Localization of implanted EEG electrodes in a virtual-reality environment. , 2001, Computer aided surgery : official journal of the International Society for Computer Aided Surgery.

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

[6]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[7]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[8]  J. A. Wilson,et al.  Electrocorticographically controlled brain-computer interfaces using motor and sensory imagery in patients with temporary subdural electrode implants. Report of four cases. , 2007, Journal of neurosurgery.

[9]  R.N.Dej.,et al.  Epilepsy and the Functional Anatomy of the Human Brain , 1954, Neurology.

[10]  Nima Dehghani,et al.  The Human K-Complex Represents an Isolated Cortical Down-State , 2009, Science.

[11]  Peter Hastreiter,et al.  Strategies for brain shift evaluation , 2004, Medical Image Anal..

[12]  Horst Urbach,et al.  COREGISTRATION OF DIGITAL PHOTOGRAPHY OF THE HUMAN CORTEX AND CRANIAL MAGNETIC RESONANCE IMAGING FOR VISUALIZATION OF SUBDURAL ELECTRODES IN EPILEPSY SURGERY , 2007, Neurosurgery.

[13]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[14]  M. Y. Wang,et al.  Measurement of Intraoperative Brain Surface Deformation Under a Craniotomy , 1998, MICCAI.

[15]  J. Gieseke,et al.  Localisation of intracranial EEG electrodes using three dimensional surface reconstructions of the brain , 2004, European Radiology.

[16]  J. A. Wilson,et al.  Two-dimensional movement control using electrocorticographic signals in humans , 2008, Journal of neural engineering.

[17]  Yasushi Miyagi,et al.  Brain shift: an error factor during implantation of deep brain stimulation electrodes. , 2007, Journal of neurosurgery.

[18]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[19]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

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

[21]  R. Reale,et al.  Functional localization of auditory cortical fields of human: Click-train stimulation , 2008, Hearing Research.

[22]  Xiaoping Hu,et al.  Retrospective Fusion of Radiographic and MR Data for Localization of Subdural Electrodes , 1992, Journal of computer assisted tomography.

[23]  E K Ritzl,et al.  Transforming Electrocortical Mapping Data into Standardized Common Space , 2007, Clinical EEG and neuroscience.

[24]  C. Kelly,et al.  Correction for Roberts et al., Isocyanic acid in the atmosphere and its possible link to smoke-related health effects , 2011, Proceedings of the National Academy of Sciences.

[25]  G. Schalk,et al.  ECoG factors underlying multimodal control of a brain-computer interface , 2006, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[26]  Gerwin Schalk,et al.  Can Electrocorticography (ECoG) Support Robust and Powerful Brain–Computer Interfaces? , 2010, Front. Neuroeng..

[27]  D. Kovalev,et al.  Rapid and fully automated visualization of subdural electrodes in the presurgical evaluation of epilepsy patients. , 2005, AJNR. American journal of neuroradiology.

[28]  Rajesh P. N. Rao,et al.  Cortical electrode localization from X-rays and simple mapping for electrocorticographic research: The “Location on Cortex” (LOC) package for MATLAB , 2007, Journal of Neuroscience Methods.

[29]  Samir Shaikh,et al.  Locating chronically implanted subdural electrodes using surface reconstruction , 2005, Clinical Neurophysiology.

[31]  Philippe Kahane,et al.  Task‐related gamma‐band dynamics from an intracerebral perspective: Review and implications for surface EEG and MEG , 2009, Human brain mapping.

[32]  G. Marchal,et al.  Multi-modal volume registration by maximization of mutual information , 1997 .

[33]  Daniel Yoshor,et al.  Receptive fields in human visual cortex mapped with surface electrodes. , 2007, Cerebral cortex.

[34]  Meritxell Bach Cuadra,et al.  A Surface-Based Approach to Quantify Local Cortical Gyrification , 2008, IEEE Transactions on Medical Imaging.

[35]  Christian Vollmar,et al.  Usefulness of 3-D reconstructed images of the human cerebral cortex for localization of subdural electrodes in epilepsy surgery , 2000, Epilepsy Research.

[36]  Eric Halgren,et al.  Sequential Processing of Lexical, Grammatical, and Phonological Information Within Broca’s Area , 2009, Science.

[37]  C Schaller,et al.  Fusion of MRI and CT with subdural grid electrodes. , 2004, Zentralblatt fur Neurochirurgie.

[38]  J. Ebersole,et al.  The accuracy and reliability of 3D CT/MRI co-registration in planning epilepsy surgery , 2009, Clinical Neurophysiology.

[39]  B. Gordon,et al.  Induced electrocorticographic gamma activity during auditory perception. Brazier Award-winning article, 2001. , 2001, Clinical neurophysiology : official journal of the International Federation of Clinical Neurophysiology.

[40]  Derek L. G. Hill,et al.  Measurement of Intraoperative Brain Surface Deformation Under a Craniotomy , 1998, MICCAI.

[41]  Rajesh P. N. Rao,et al.  Electrocorticography-based brain computer Interface-the seattle experience , 2006, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[42]  Robert T. Knight,et al.  Localization of neurosurgically implanted electrodes via photograph–MRI–radiograph coregistration , 2008, Journal of Neuroscience Methods.

[43]  D L Hill,et al.  Sources of error in comparing functional magnetic resonance imaging and invasive electrophysiological recordings. , 2000, Journal of neurosurgery.

[44]  Rajesh P. N. Rao,et al.  Generalized Features for Electrocorticographic BCIs , 2008, IEEE Transactions on Biomedical Engineering.