MEG Coherence and DTI Connectivity in mTLE

Magnetoencephalography (MEG) is a noninvasive imaging method for localization of focal epileptiform activity in patients with epilepsy. Diffusion tensor imaging (DTI) is a noninvasive imaging method for measuring the diffusion properties of the underlying white matter tracts through which epileptiform activity is propagated. This study investigates the relationship between the cerebral functional abnormalities quantified by MEG coherence and structural abnormalities quantified by DTI in mesial temporal lobe epilepsy (mTLE). Resting state MEG data was analyzed using MEG coherence source imaging (MEG-CSI) method to determine the coherence in 54 anatomical sites in 17 adult mTLE patients with surgical resection and Engel class I outcome, and 17 age- and gender- matched controls. DTI tractography identified the fiber tracts passing through these same anatomical sites of the same subjects. Then, DTI nodal degree and laterality index were calculated and compared with the corresponding MEG coherence and laterality index. MEG coherence laterality, after Bonferroni adjustment, showed significant differences for right versus left mTLE in insular cortex and both lateral orbitofrontal and superior temporal gyri (p < 0.017). Likewise, DTI nodal degree laterality, after Bonferroni adjustment, showed significant differences for right versus left mTLE in gyrus rectus, insular cortex, precuneus and superior temporal gyrus (p < 0.017). In insular cortex, MEG coherence laterality correlated with DTI nodal degree laterality ($$R^{2} = 0.46; p = 0.003)$$R2=0.46;p=0.003) in the cases of mTLE. None of these anatomical sites showed statistically significant differences in coherence laterality between right and left sides of the controls. Coherence laterality was in agreement with the declared side of epileptogenicity in insular cortex (in 82 % of patients) and both lateral orbitofrontal (88 %) and superior temporal gyri (88 %). Nodal degree laterality was also in agreement with the declared side of epileptogenicity in gyrus rectus (in 88 % of patients), insular cortex (71 %), precuneus (82 %) and superior temporal gyrus (94 %). Combining all significant laterality indices improved the lateralization accuracy to 94 % and 100 % for the coherence and nodal degree laterality indices, respectively. The associated variations in diffusion properties of fiber tracts quantified by DTI and coherence measures quantified by MEG with respect to epileptogenicity possibly reflect the chronic microstructural cerebral changes associated with functional interictal activity. The proposed methodology for using MEG and DTI to investigate diffusion abnormalities related to focal epileptogenicity and propagation may provide a further means of noninvasive lateralization.

[1]  Christopher H. Chapman,et al.  Radiation therapy effects on white matter fiber tracts of the limbic circuit. , 2012, Medical physics.

[2]  J E Moran,et al.  ICA methods for MEG imaging. , 2004, Neurology & clinical neurophysiology : NCN.

[3]  Luis Concha,et al.  Bilateral limbic diffusion abnormalities in unilateral temporal lobe epilepsy , 2005, Annals of neurology.

[4]  Zhen Zhou,et al.  Identifying the affected hemisphere with a multimodal approach in MRI-positive or negative, unilateral or bilateral temporal lobe epilepsy , 2014, Neuropsychiatric disease and treatment.

[5]  D. Hosmer,et al.  Applied Logistic Regression , 1991 .

[6]  John C. Gore,et al.  Lateralization of temporal lobe epilepsy using resting functional magnetic resonance imaging connectivity of hippocampal networks , 2012, Epilepsia.

[7]  M. Brazier Spread of seizure discharges in epilepsy: anatomical and electrophysiological considerations. , 1972, Experimental neurology.

[8]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[9]  Dominique Hasboun,et al.  Interictal diffusion MRI in partial epilepsies explored with intracerebral electrodes. , 2006, Brain : a journal of neurology.

[10]  Don M. Tucker,et al.  Methods for Examining Electrophysiological Coherence in Epileptic Networks , 2013, Front. Neurol..

[11]  Yong He,et al.  BrainNet Viewer: A Network Visualization Tool for Human Brain Connectomics , 2013, PloS one.

[12]  John S. Duncan,et al.  Abnormalities of language networks in temporal lobe epilepsy , 2007, NeuroImage.

[13]  John S Ebersole,et al.  Clinical Application of Dipole Models in the Localization of Epileptiform Activity , 2007, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[14]  John E. Moran,et al.  MEG coherence imaging compared to electrocortical recordings from NeuroPace implants to determine the location of ictal onset in epilepsy patients , 2007 .

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

[16]  Ayako Ochi,et al.  Diffusion tensor imaging identifies changes in normal-appearing white matter within the epileptogenic zone in tuberous sclerosis complex , 2010, Epilepsy Research.

[17]  Yahya Aghakhani,et al.  Epilepsy surgery in patients with bilateral temporal lobe seizures: A systematic review , 2014, Epilepsia.

[18]  Hamid Soltanian-Zadeh,et al.  A Bayesian averaged response-driven multinomial model for lateralization of temporal lobe epilepsy , 2014, 2014 IEEE 11th International Symposium on Biomedical Imaging (ISBI).

[19]  R. Shumway,et al.  Linear Discriminant Functions for Stationary Time Series , 1974 .

[20]  J. E. Moran,et al.  Multi-Resolution FOCUSS: A Source Imaging Technique Applied to MEG Data , 2005, Brain Topography.

[21]  F. Rugg-Gunn,et al.  Diffusion imaging in epilepsy , 2007, Expert review of neurotherapeutics.

[22]  A. Sharan,et al.  Reduced thalamocortical functional connectivity in temporal lobe epilepsy , 2015, Epilepsia.

[23]  D. Carmichael,et al.  Network Connectivity in Epilepsy: Resting State fMRI and EEG–fMRI Contributions , 2014, Front. Neurol..

[24]  John S Ebersole,et al.  American Clinical Magnetoencephalography Society Clinical Practice Guideline 1: Recording and Analysis of Spontaneous Cerebral Activity* , 2011, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[25]  Linda Douw,et al.  Altered structural connectome in temporal lobe epilepsy. , 2014, Radiology.

[26]  Csaba Juhász,et al.  Diffusion tensor analysis of temporal and extra-temporal lobe tracts in temporal lobe epilepsy , 2008, Epilepsy Research.

[27]  Luis Concha,et al.  Extratemporal White Matter Abnormalities in Mesial Temporal Lobe Epilepsy Demonstrated with Diffusion Tensor Imaging , 2006, Epilepsia.

[28]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[29]  Nitin Tandon,et al.  Thalamic structural connectivity in medial temporal lobe epilepsy , 2014, Epilepsia.

[30]  Scott T. Grafton,et al.  Automated image registration: I. General methods and intrasubject, intramodality validation. , 1998, Journal of computer assisted tomography.

[31]  R. Knowlton,et al.  Can Magnetoencephalography Aid Epilepsy Surgery? , 2008, Epilepsy currents.

[32]  G. Pearlson,et al.  Diffusion Tensor Imaging and Axonal Tracking in the Human Brainstem , 2001, NeuroImage.

[33]  D. Le Bihan,et al.  Uncinate fasciculus fiber tracking in mesial temporal lobe epilepsy. Initial findings , 2007, European Radiology.

[34]  Catharyn T. Liverman,et al.  A Summary of the Institute of Medicine Report: Epilepsy Across the Spectrum: Promoting Health and Understanding , 2012 .

[35]  Norman Tepley,et al.  An assessment of MEG coherence imaging in the study of temporal lobe epilepsy , 2011, Epilepsia.

[36]  Leonardo Bonilha,et al.  Medial temporal lobe epilepsy is associated with neuronal fibre loss and paradoxical increase in structural connectivity of limbic structures , 2012, Journal of Neurology, Neurosurgery & Psychiatry.

[37]  Jean-Philippe Thiran,et al.  Connectivity and tissue microstructural alterations in right and left temporal lobe epilepsy revealed by diffusion spectrum imaging , 2014, NeuroImage: Clinical.

[38]  Hamid Soltanian-Zadeh,et al.  Lateralization of temporal lobe epilepsy by multimodal multinomial hippocampal response-driven models , 2014, Journal of the Neurological Sciences.

[39]  Michael H Kohrman,et al.  What is Epilepsy? Clinical Perspectives in the Diagnosis and Treatment , 2007, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[40]  Heidi E Kirsch,et al.  Epileptogenic zone localization using magnetoencephalography predicts seizure freedom in epilepsy surgery , 2015, Epilepsia.

[41]  Catherine R. Traynor,et al.  Thalamotemporal impairment in temporal lobe epilepsy: A combined MRI analysis of structure, integrity, and connectivity , 2014, Epilepsia.

[42]  Stephen M. Smith,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[43]  R. Goodman,et al.  Cortical abnormalities in epilepsy revealed by local EEG synchrony , 2007, NeuroImage.

[44]  Richard O. Duda,et al.  Pattern classification and scene analysis , 1974, A Wiley-Interscience publication.

[45]  Phiroz E. Tarapore,et al.  Global and regional functional connectivity maps of neural oscillations in focal epilepsy. , 2015, Brain : a journal of neurology.

[46]  Z. Haneef,et al.  Graph theory findings in the pathophysiology of temporal lobe epilepsy , 2014, Clinical Neurophysiology.

[47]  D. Louis Collins,et al.  Whole-brain voxel-based statistical analysis of gray matter and white matter in temporal lobe epilepsy , 2004, NeuroImage.

[48]  H Hosaka,et al.  Part II: magnetic field produced by a current dipole. , 1976, Journal of electrocardiology.

[49]  J. Engel,et al.  Surgery for seizures. , 1996, The New England journal of medicine.

[50]  John S. Duncan,et al.  Tractography of the parahippocampal gyrus and material specific memory impairment in unilateral temporal lobe epilepsy , 2007, NeuroImage.

[51]  R. Kumaresan,et al.  Data adaptive signal estimation by singular value decomposition of a data matrix , 1982, Proceedings of the IEEE.

[52]  Olivier Colliot,et al.  Structural connectivity differences in left and right temporal lobe epilepsy , 2014, NeuroImage.

[53]  Arthur W. Toga,et al.  Construction of a 3D probabilistic atlas of human cortical structures , 2008, NeuroImage.

[54]  Walter H Backes,et al.  White matter network abnormalities are associated with cognitive decline in chronic epilepsy. , 2012, Cerebral cortex.

[55]  Olaf Sporns,et al.  THE HUMAN CONNECTOME: A COMPLEX NETWORK , 2011, Schizophrenia Research.

[56]  R. Kuzniecky,et al.  Multimodality MRI in mesial temporal sclerosis: Relative sensitivity and specificity , 1997, Neurology.

[57]  Edward T. Bullmore,et al.  Network-based statistic: Identifying differences in brain networks , 2010, NeuroImage.

[58]  Mahinda Yogarajah,et al.  Diffusion‐based magnetic resonance imaging and tractography in epilepsy , 2008, Epilepsia.

[59]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[60]  John S. Duncan,et al.  Voxel-based diffusion tensor imaging in patients with mesial temporal lobe epilepsy and hippocampal sclerosis , 2008, NeuroImage.

[61]  C. Nimsky,et al.  Periventricular nodular heterotopia: A challenge for epilepsy surgery , 2007, Seizure.

[62]  J. Gotman,et al.  Patterns of altered functional connectivity in mesial temporal lobe epilepsy , 2012, Epilepsia.

[63]  M. N. Murty,et al.  Linear Discriminant Function , 2016 .

[64]  P. Basser,et al.  Water Diffusion Changes in Wallerian Degeneration and Their Dependence on White Matter Architecture , 2000 .

[65]  S. Lehéricy,et al.  Hippocampal‐thalamic wiring in medial temporal lobe epilepsy: Enhanced connectivity per hippocampal voxel , 2015, Epilepsia.

[66]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[67]  J. Engel,et al.  Functional connectivity of hippocampal networks in temporal lobe epilepsy , 2014, Epilepsia.

[68]  J Gotman,et al.  Interhemispheric Relations During Bilateral Spike‐and‐Wave Activity , 1981, Epilepsia.

[69]  Hamid Soltanian-Zadeh,et al.  DTI-based response-driven modeling of mTLE laterality☆ , 2015, NeuroImage: Clinical.

[70]  Susumu Mori,et al.  Fiber tracking: principles and strategies – a technical review , 2002, NMR in biomedicine.

[71]  Rodney X. Sturdivant,et al.  Applied Logistic Regression: Hosmer/Applied Logistic Regression , 2005 .

[72]  G. Barkley,et al.  MEG and EEG in Epilepsy , 2003, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[73]  Andrea M. Schultz,et al.  Epilepsy Across the Spectrum , 2012 .

[74]  J. Engel,et al.  Network analysis of the default mode network using functional connectivity MRI in Temporal Lobe Epilepsy. , 2014, Journal of visualized experiments : JoVE.

[75]  Ravindra Arya,et al.  Adverse events related to extraoperative invasive EEG monitoring with subdural grid electrodes: A systematic review and meta‐analysis , 2013, Epilepsia.

[76]  Dustin Scheinost,et al.  DTI abnormalities in anterior corpus callosum of rats with spike–wave epilepsy , 2009, NeuroImage.

[77]  V L Towle,et al.  Electrocorticographic coherence patterns. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[78]  Hamid Soltanian-Zadeh,et al.  Lateralization of temporal lobe epilepsy using a novel uncertainty analysis of MR diffusion in hippocampus, cingulum, and fornix, and hippocampal volume and FLAIR intensity , 2014, Journal of the Neurological Sciences.

[79]  D L Collins,et al.  White-matter diffusion abnormalities in temporal-lobe epilepsy with and without mesial temporal sclerosis , 2008, Journal of Neurology, Neurosurgery, and Psychiatry.

[80]  Orrin Devinsky,et al.  Thalamic functional connectivity predicts seizure laterality in individual TLE patients: Application of a biomarker development strategy , 2014, NeuroImage: Clinical.

[81]  J. Schoffelen,et al.  Source connectivity analysis with MEG and EEG , 2009, Human brain mapping.

[82]  W W Sutherling,et al.  Influence of magnetic source imaging for planning intracranial EEG in epilepsy , 2008, Neurology.

[83]  Vince D. Calhoun,et al.  Measuring brain connectivity: Diffusion tensor imaging validates resting state temporal correlations , 2008, NeuroImage.