Source localization of interictal spike-locked neuromagnetic oscillations in pediatric neocortical epilepsy

OBJECTIVE To evaluate the utility of an event-related beamforming (ERB) algorithm in source localization of interictal discharges. METHODS We analyzed interictal magnetoencephalography data in 35 children with intractable neocortical epilepsy. We used a spatiotemporal beamforming method to estimate the spatial distribution of source power in individual interictal spikes. We compared ERB results to source localization using the equivalent current dipole model and to the seizure onset zones on intracranial EEG. RESULTS Focal beamformer localization was observed in 66% of patients and multifocal in the remaining 34%. ERB localized within 2 cm of the equivalent current dipole cluster centroid in 77% of the patients. ERB localization was concordant with the seizure onset zone on intracranial EEG at the gyral level in 69% of patients. Focal ERB localization area was included in the resection margin in 22/23 patients. However, focal ERB localization was not statistically associated with better surgical outcome. CONCLUSIONS ERB can be used for source localization of interictal spikes and can be predictive of the ictal onset zone in a subset of patients with neocortical epilepsy. SIGNIFICANCE These results support the utility of beamformer source localization as a fast semi-automated method for source localization of interictal spikes and planning the surgical strategy.

[1]  G Lindinger,et al.  Magnetoencephalography in Focal Epilepsy , 2000, Epilepsia.

[2]  H. Otsubo,et al.  Characterizing Magnetoencephalographic Spike Sources in Children with Tuberous Sclerosis Complex , 2005, Epilepsia.

[3]  J. Gotman,et al.  High‐frequency electroencephalographic oscillations correlate with outcome of epilepsy surgery , 2010, Annals of neurology.

[4]  David Poeppel,et al.  Reconstructing spatio-temporal activities of neural sources using an MEG vector beamformer technique , 2001, IEEE Transactions on Biomedical Engineering.

[5]  C. D Binnie,et al.  Comparison of sphenoidal, foramen ovale and anterior temporal placements for detecting interictal epileptiform discharges in presurgical assessment for temporal lobe epilepsy , 1999, Clinical Neurophysiology.

[6]  Jean Gotman,et al.  Systematic source estimation of spikes by a combination of independent component analysis and RAP-MUSIC II: Preliminary clinical application , 2002, Clinical Neurophysiology.

[7]  Stephen T. C. Wong,et al.  Magnetoencephalography in partial epilepsy: Clinical yield and localization accuracy , 1997, Annals of neurology.

[8]  William Gaetz,et al.  Activation of area MT/V5 and the right inferior parietal cortex during the discrimination of transient direction changes in translational motion. , 2007, Cerebral cortex.

[9]  Ayako Ochi,et al.  Localization of epileptic foci in children with intractable epilepsy secondary to multiple cortical tubers by using synthetic aperture magnetometry kurtosis. , 2009, Journal of neurosurgery. Pediatrics.

[10]  Jorge Gonzalez-Martinez,et al.  Long‐term seizure outcome after resective surgery in patients evaluated with intracranial electrodes , 2012, Epilepsia.

[11]  J. Vrba,et al.  Signal processing in magnetoencephalography. , 2001, Methods.

[12]  Kristen Riley,et al.  Magnetic source imaging versus intracranial electroencephalogram in epilepsy surgery: A prospective study , 2006, Annals of neurology.

[13]  M. Duchowny,et al.  Epilepsy surgery in patients with normal or nonfocal MRI scans: Integrative strategies offer long‐term seizure relief , 2008, Epilepsia.

[14]  Elizabeth W. Pang,et al.  Event-related beamforming: A robust method for presurgical functional mapping using MEG , 2007, Clinical Neurophysiology.

[15]  H. Otsubo,et al.  Magnetoencephalographic localization in pediatric epilepsy surgery: Comparison with invasive intracranial electroencephalography , 1999, Annals of neurology.

[16]  Shirin Sarkari,et al.  Toward the Substitution of Invasive Electroencephalography in Epilepsy Surgery , 2005, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[17]  C. Michel,et al.  128-Channel EEG Source Imaging in Epilepsy: Clinical Yield and Localization Precision , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[18]  Srikantan S. Nagarajan,et al.  Fast oscillations associated with interictal spikes localize the epileptogenic zone in patients with partial epilepsy , 2008, NeuroImage.

[19]  Intraoperative Confirmation of Hand Motor Area Identified Preoperatively by Magnetoencephalography , 2008, Pediatric Neurosurgery.

[20]  Eric Halgren,et al.  Dynamic Statistical Parametric Mapping for Analyzing the Magnetoencephalographic Epileptiform Activity in Patients With Epilepsy , 2004, Journal of child neurology.

[21]  Gonzalo Alarcón,et al.  Mechanisms involved in the conduction of anterior temporal epileptiform discharges to the scalp , 2009, Clinical Neurophysiology.

[22]  C. Michel,et al.  EEG Source Imaging in Pediatric Epilepsy Surgery: A New Perspective in Presurgical Workup , 2006, Epilepsia.

[23]  K. Sekihara,et al.  Neural source estimation from a time–frequency component of somatic evoked high-frequency magnetic oscillations to posterior tibial nerve stimulation , 1999, Clinical Neurophysiology.

[24]  Ayako Ochi,et al.  Preoperative simulation of intracerebral epileptiform discharges: synthetic aperture magnetometry virtual sensor analysis of interictal magnetoencephalography data. , 2006, Journal of neurosurgery.

[25]  Seppo P. Ahlfors,et al.  Propagation of epileptic spikes reconstructed from spatiotemporal magnetoencephalographic and electroencephalographic source analysis , 2010, NeuroImage.

[26]  Kensuke Sekihara,et al.  Suppression of background brain activity influence in localizing epileptic spike sources from biomagnetic measurements , 2005, Brain Topography.

[27]  H. Otsubo,et al.  Malignant rolandic-sylvian epilepsy in children , 2001, Neurology.

[28]  Margot J. Taylor,et al.  Inversion and contrast-reversal effects on face processing assessed by MEG , 2006, Brain Research.

[29]  G Scheler,et al.  Magnetic brain source imaging of focal epileptic activity: a synopsis of 455 cases. , 2003, Brain : a journal of neurology.

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

[31]  Lily Riggs,et al.  A complementary analytic approach to examining medial temporal lobe sources using magnetoencephalography , 2009, NeuroImage.

[32]  Ayako Ochi,et al.  Dynamic Changes of Ictal High‐Frequency Oscillations in Neocortical Epilepsy: Using Multiple Band Frequency Analysis , 2007, Epilepsia.

[33]  H. E. Kirsch,et al.  Automated localization of magnetoencephalographic interictal spikes by adaptive spatial filtering , 2006, Clinical Neurophysiology.

[34]  Gabriela Scheler,et al.  Utilization of magnetoencephalography results to obtain favourable outcomes in epilepsy surgery. , 2004, Brain : a journal of neurology.

[35]  Christoph Baumgartner,et al.  Combined MEG/EEG analysis of the interictal spike complex in mesial temporal lobe epilepsy , 2005, NeuroImage.

[36]  J. Gotman,et al.  Systematic source estimation of spikes by a combination of independent component analysis and RAP-MUSIC I: Principles and simulation study , 2002, Clinical Neurophysiology.

[37]  H. Stefan,et al.  Fast activity as a surrogate marker of epileptic network function? , 2006, Clinical Neurophysiology.

[38]  J S Ebersole,et al.  Magnetoencephalography/Magnetic Source Imaging in the Assessment of Patients with Epilepsy , 1997, Epilepsia.

[39]  William Gaetz,et al.  PRESURGICAL LOCALIZATION OF PRIMARY MOTOR CORTEX IN PEDIATRIC PATIENTS WITH BRAIN LESIONS BY THE USE OF SPATIALLY FILTERED MAGNETOENCEPHALOGRAPHY , 2009, Neurosurgery.

[40]  C. N. Guy,et al.  Mechanisms involved in the propagation of interictal epileptiform discharges in partial epilepsy. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[41]  François Mauguière,et al.  Towards source volume estimation of interictal spikes in focal epilepsy using magnetoencephalography , 2012, NeuroImage.

[42]  William Gaetz,et al.  Task-related modulation of early cortical responses during language production: an event-related synthetic aperture magnetometry study. , 2007, Cerebral cortex.

[43]  H. Lüders,et al.  Presurgical evaluation of epilepsy. , 2001, Brain : a journal of neurology.

[44]  D. Cheyne,et al.  Spatiotemporal mapping of cortical activity accompanying voluntary movements using an event‐related beamforming approach , 2006, Human brain mapping.