EEG source connectivity to localize the seizure onset zone in patients with drug resistant epilepsy

Electrical source imaging (ESI) from interictal scalp EEG is increasingly validated and used as a valuable tool in the presurgical evaluation of epilepsy as a reflection of the irritative zone. ESI of ictal scalp EEG to localize the seizure onset zone (SOZ) remains challenging. We investigated the value of an approach for ictal imaging using ESI and functional connectivity analysis (FC). Ictal scalp EEG from 111 seizures in 27 patients who had Engel class I outcome at least 1 year following resective surgery was analyzed. For every seizure, an artifact-free epoch close to the seizure onset was selected and ESI using LORETA was applied. In addition, the reconstructed sources underwent FC using the spectrum-weighted Adaptive Directed Transfer Function. This resulted in the estimation of the SOZ in two ways: (i) the source with maximal power after ESI, (ii) the source with the strongest outgoing connections after combined ESI and FC. Next, we calculated the distance between the estimated SOZ and the border of the resected zone (RZ) for both approaches and called this the localization error ((i) LEpow and (ii) LEconn respectively). By comparing LEpow and LEconn, we assessed the added value of FC. The source with maximal power after ESI was inside the RZ (LEpow = 0 mm) in 31% of the seizures and estimated within 10 mm from the border of the RZ (LEpow ≤ 10 mm) in 42%. Using ESI and FC, these numbers increased to 72% for LEconn = 0 mm and 94% for LEconn ≤ 10 mm. FC provided a significant added value to ESI alone (p < 0.001). ESI combined with subsequent FC is able to localize the SOZ in a non-invasive way with high accuracy. Therefore it could be a valuable tool in the presurgical evaluation of epilepsy.

[1]  P Jayakar,et al.  Localization of Seizure Foci: Pitfalls and Caveats , 1991, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[2]  Gregor Strobbe,et al.  The Role of Skull Modeling in EEG Source Imaging for Patients with Refractory Temporal Lobe Epilepsy , 2016, Brain Topography.

[3]  John S Duncan,et al.  The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study , 2011, The Lancet.

[4]  S. Noachtar,et al.  Congruence and discrepancy of interictal and ictal EEG with MRI lesions in focal epilepsies , 2011, Neurology.

[5]  Pieter van Mierlo,et al.  Electrical source imaging of interictal spikes using multiple sparse volumetric priors for presurgical epileptogenic focus localization , 2016, NeuroImage: Clinical.

[6]  Hans Hallez,et al.  Accurate epileptogenic focus localization through time-variant functional connectivity analysis of intracranial electroencephalographic signals , 2011, NeuroImage.

[7]  W T Blume,et al.  A randomized, controlled trial of surgery for temporal-lobe epilepsy. , 2001, The New England journal of medicine.

[8]  Gregor Strobbe,et al.  Seizure Onset Zone Localization from Ictal High-Density EEG in Refractory Focal Epilepsy , 2017, Brain Topography.

[9]  Giovanni Pellegrino,et al.  Source localization of the seizure onset zone from ictal EEG/MEG data , 2016, Human brain mapping.

[10]  D. Lehmann,et al.  Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[11]  W S Lee,et al.  Complications and results of subdural grid electrode implantation in epilepsy surgery. , 2000, Surgical neurology.

[12]  G. Pfurtscheller,et al.  A criterion for adaptive autoregressive models , 2000, Proceedings of the 22nd Annual International Conference of the IEEE Engineering in Medicine and Biology Society (Cat. No.00CH37143).

[13]  J S Ebersole,et al.  Noninvasive Localization of Epileptogenic Foci by EEG Source Modeling , 2000, Epilepsia.

[14]  G Lantz,et al.  Frequency domain EEG source localization of ictal epileptiform activity in patients with partial complex epilepsy of temporal lobe origin , 1999, Clinical Neurophysiology.

[15]  Bart Vanrumste,et al.  Ictal Source Localization in Presurgical Patients With Refractory Epilepsy , 2002, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[16]  Evelien Carrette,et al.  The management of pharmacologically refractory epilepsy , 2011 .

[17]  Zoltan J. Koles,et al.  A Comparison of LORETA and the Borgiotti-Kaplan Beamformer in Simulated EEG Source Localization with a Realistic Head Model , 2007 .

[18]  J. Hahn,et al.  Complications of invasive video-EEG monitoring with subdural grid electrodes , 2002, Neurology.

[19]  Bin He,et al.  Seizure source imaging by means of FINE spatio-temporal dipole localization and directed transfer function in partial epilepsy patients , 2012, Clinical Neurophysiology.

[20]  C. Braun,et al.  Adaptive AR modeling of nonstationary time series by means of Kalman filtering , 1998, IEEE Transactions on Biomedical Engineering.

[21]  Laura Astolfi,et al.  Tracking the Time-Varying Cortical Connectivity Patterns by Adaptive Multivariate Estimators , 2008, IEEE Transactions on Biomedical Engineering.

[22]  Margitta Seeck,et al.  Dynamic directed interictal connectivity in left and right temporal lobe epilepsy , 2015, Epilepsia.

[23]  Mark P Richardson,et al.  Large scale brain models of epilepsy: dynamics meets connectomics , 2012, Journal of Neurology, Neurosurgery & Psychiatry.

[24]  Hans Hallez,et al.  Ictal‐onset localization through connectivity analysis of intracranial EEG signals in patients with refractory epilepsy , 2013, Epilepsia.

[25]  Luca Faes,et al.  Critical Comments on EEG Sensor Space Dynamical Connectivity Analysis , 2016, Brain Topography.

[26]  Mohammad Ashfak Habib,et al.  Ictal EEG Source Imaging for Presurgical Evaluation of Refractory Focal Epilepsy. , 2016, World neurosurgery.

[27]  A. R. Anwar,et al.  Dynamic Imaging of Coherent Sources Reveals Different Network Connectivity Underlying the Generation and Perpetuation of Epileptic Seizures , 2013, PloS one.

[28]  Jean-Michel Badier,et al.  Source localization of ictal epileptic activity investigated by high resolution EEG and validated by SEEG , 2010, NeuroImage.

[29]  Gregory A. Worrell,et al.  Ictal source analysis: Localization and imaging of causal interactions in humans , 2007, NeuroImage.

[30]  Gene H. Golub,et al.  Singular value decomposition and least squares solutions , 1970, Milestones in Matrix Computation.

[31]  Ki-Young Jung,et al.  Spatiotemporospectral characteristics of scalp ictal EEG in mesial temporal lobe epilepsy with hippocampal sclerosis , 2009, Brain Research.

[32]  J S Ebersole,et al.  Continuous Source Imaging of Scalp Ictal Rhythms in Temporal Lobe Epilepsy , 1997, Epilepsia.

[33]  Tzyy-Ping Jung,et al.  Independent Component Analysis of Electroencephalographic Data , 1995, NIPS.

[34]  S. Spencer Neural Networks in Human Epilepsy: Evidence of and Implications for Treatment , 2002, Epilepsia.

[35]  Bin He,et al.  Interictal spike analysis of high-density EEG in patients with partial epilepsy , 2011, Clinical Neurophysiology.

[36]  F. Schlindwein,et al.  Selection of the order of autoregressive models for spectral analysis of Doppler ultrasound signals. , 1990, Ultrasound in medicine & biology.

[37]  Seungjin Choi,et al.  Independent Component Analysis , 2009, Handbook of Natural Computing.

[38]  J. Stockman The long-term outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study , 2013 .

[39]  C. Adam,et al.  Dipole Modeling in Epilepsy Surgery Candidates , 1997, Epilepsia.

[40]  Bin He,et al.  Dynamic imaging of ictal oscillations using non-invasive high-resolution EEG , 2011, NeuroImage.