Development of Differential Connectivity Graph for Characterization of Brain Regions Involved in Epilepsy

Drug-resistant epileptic patients suffering from focal epilepsy are recommended for epilepsy surgery. The aim of this surgery is to remove the seizure onset zones (SOZ) without creating new neurological deficits. To identify the SOZs, the best way is to record the seizures from intracerebral electroencephalogram (iEEG) recordings. However recording seizures is complicated contrary to the recording of interictal epileptiform discharges (IED). Therefore prediction of SOZ by estimating the IED regions is very valuable. There are several studies wondering if the estimation of the IED regions can be useful to predict the SOZ and eventually for presurgery evaluations. Although the encouraging results of these studies, the problem is still an open issue. The main problem of the previous studies is the reliability of the results. The aim of this thesis is to estimate the leading IED (LIED) regions from interictal analysis of iEEG recordings through connectivity graph. The main originality of the proposed method refers to a new reliable graph analysis method called differential connectivity graph (DCG). This graph is designed to identify the significant discriminated connections between IED and non-IED brain states. The statistical reliability of DCG is obtained by using permutation-based multiple testing. In the proposed method, multiple DCGs associated with different frequency bands are constructed. Each DCG includes both source and sink nodes involved in IED events. To identify the source nodes related to LIED regions, the directions of the edges of DCG are estimated and a new measure called local information (LI) is proposed to measure the emittance contribution of each node. To estimate the LIED regions from the LI values related to multiple directed DCGs, a multi-objective optimization method is used. The proposed method is applied on five epileptic patients. These patients underwent resective surgery and they are seizure-free after the surgery. Estimated LIED regions are compared with SOZ detected visually by the epileptologist and SOZ detected by a method using induced ictal iEEG. The comparison reveals congruent results between estimated LIED regions and SOZs. Being all of the patients seizure free and inclusion of estimated LIED regions in the removed regions during surgery shows the reliability of estimated LIED regions for presurgery evaluations.

[1]  Ingrid Daubechies,et al.  Ten Lectures on Wavelets , 1992 .

[2]  Xiaoli Li,et al.  Fractal spectral analysis of pre-epileptic seizures in terms of criticality , 2005, Journal of neural engineering.

[3]  C. Stam,et al.  Synchronization likelihood: an unbiased measure of generalized synchronization in multivariate data sets , 2002 .

[4]  Gholam-Ali Hossein-Zadeh,et al.  Sparse differential connectivity graph of scalp EEG for epileptic patients , 2009, ESANN.

[5]  J. Tukey Some thoughts on clinical trials, especially problems of multiplicity. , 1977, Science.

[6]  A. Kraskov,et al.  On the predictability of epileptic seizures , 2005, Clinical Neurophysiology.

[7]  R. Duckrow,et al.  Regional coherence and the transfer of ictal activity during seizure onset in the medial temporal lobe. , 1992, Electroencephalography and clinical neurophysiology.

[8]  Lang Tong,et al.  Indeterminacy and identifiability of blind identification , 1991 .

[9]  Minfen Shen,et al.  The investigation of time-varying synchrony of EEG during sentence learning using wavelet analysis , 2002, Proceedings of the 9th International Conference on Neural Information Processing, 2002. ICONIP '02..

[10]  Brandon J. Whitcher,et al.  Assessing Nonstationary Time Series Using Wavelets , 1998 .

[11]  Fabrice Wendling,et al.  A Physiologically Plausible Spatio-Temporal Model for EEG Signals Recorded With Intracerebral Electrodes in Human Partial Epilepsy , 2007, IEEE Transactions on Biomedical Engineering.

[12]  Jochen Triesch,et al.  Democratic Integration: Self-Organized Integration of Adaptive Cues , 2001, Neural Computation.

[13]  Régine Le Bouquin-Jeannès,et al.  Linear and nonlinear causality between signals: methods, examples and neurophysiological applications , 2006, Biological Cybernetics.

[14]  Luiz A. Baccalá,et al.  Partial directed coherence: a new concept in neural structure determination , 2001, Biological Cybernetics.

[15]  E. John,et al.  A Field Theory of Consciousness , 2001, Consciousness and Cognition.

[16]  F. Cincotti,et al.  Cortical Activity and Connectivity of Human Brain during the Prisoner's Dilemma: an EEG Hyperscanning Study , 2007, 2007 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[17]  G. Alarcón,et al.  Electrophysiological aspects of interictal and ictal activity in human partial epilepsy , 1996, Seizure.

[18]  I. Daubechies Orthonormal bases of compactly supported wavelets , 1988 .

[19]  Richard Kronland-Martinet,et al.  Asymptotic wavelet and Gabor analysis: Extraction of instantaneous frequencies , 1992, IEEE Trans. Inf. Theory.

[20]  Christian Jutten,et al.  Multichannel Electrocardiogram Decomposition Using Periodic Component Analysis , 2008, IEEE Transactions on Biomedical Engineering.

[21]  C. Granger Investigating Causal Relations by Econometric Models and Cross-Spectral Methods , 1969 .

[22]  J. Geweke,et al.  Measurement of Linear Dependence and Feedback between Multiple Time Series , 1982 .

[23]  Alexander B. Pinus,et al.  Origin of the Radio Frequency Pulse Artifact in Simultaneous EEG-fMRI Recording: Rectification at the Carbon-Metal Interface , 2007, IEEE Transactions on Biomedical Engineering.

[24]  Rudy Moddemeijer,et al.  A statistic to estimate the variance of the histogram-based mutual information estimator based on dependent pairs of observations , 1999, Signal Process..

[25]  Sonja Grün,et al.  Data-driven significance estimation for precise spike correlation. , 2009, Journal of neurophysiology.

[26]  Lucas C. Parra,et al.  Blind Source Separation via Generalized Eigenvalue Decomposition , 2003, J. Mach. Learn. Res..

[27]  Saeid Sanei,et al.  Scanner Artifact Removal in Simultaneous EEG-fMRI for Epileptic Seizure Prediction , 2006, 18th International Conference on Pattern Recognition (ICPR'06).

[28]  Edward T. Bullmore,et al.  Broadband Criticality of Human Brain Network Synchronization , 2009, PLoS Comput. Biol..

[29]  K. P. Indiradevi,et al.  A multi-level wavelet approach for automatic detection of epileptic spikes in the electroencephalogram , 2008, Comput. Biol. Medicine.

[30]  Peng Xu,et al.  A new method based on sparse component decomposition to remove MRI artifacts in the continuous EEG recordings , 2007, 2005 IEEE Engineering in Medicine and Biology 27th Annual Conference.

[31]  D. Lehmann Multichannel topography of human alpha EEG fields. , 1971, Electroencephalography and clinical neurophysiology.

[32]  Lotfi Senhadji,et al.  Quantitative evaluation of linear and nonlinear methods characterizing interdependencies between brain signals. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[33]  Ayako Ochi,et al.  Complications of invasive subdural grid monitoring in children with epilepsy. , 2003, Journal of neurosurgery.

[34]  Michael R. Chernick,et al.  Wavelet Methods for Time Series Analysis , 2001, Technometrics.

[35]  H. Lu,et al.  Resting-State Functional Connectivity in Rat Brain , 2005 .

[36]  B. Pompe Measuring statistical dependences in a time series , 1993 .

[37]  Boualem Boashash,et al.  Estimating and interpreting the instantaneous frequency of a signal. I. Fundamentals , 1992, Proc. IEEE.

[38]  M. Besserve,et al.  Towards a proper estimation of phase synchronization from time series , 2006, Journal of Neuroscience Methods.

[39]  D. Mantini,et al.  Fusion of EEG and fMRI for the investigation of functional connectivity during a visual oddball task , 2007, 2007 Joint Meeting of the 6th International Symposium on Noninvasive Functional Source Imaging of the Brain and Heart and the International Conference on Functional Biomedical Imaging.

[40]  Xin-Ping Guan,et al.  Application of wavelet-based similarity analysis to epileptic seizures prediction , 2007, Comput. Biol. Medicine.

[41]  Lotfi Senhadji,et al.  Epileptic transient detection: wavelets and time-frequency approaches , 2002, Neurophysiologie Clinique/Clinical Neurophysiology.

[42]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[43]  Mingzhou Ding,et al.  Evaluating causal relations in neural systems: Granger causality, directed transfer function and statistical assessment of significance , 2001, Biological Cybernetics.

[44]  David Rudrauf,et al.  Estimating the time-course of coherence between single-trial brain signals: an introduction to wavelet coherence , 2002, Neurophysiologie Clinique/Clinical Neurophysiology.

[45]  Karl J. Friston,et al.  Modelling event-related responses in the brain , 2005, NeuroImage.

[46]  Kazuki Iwata,et al.  Artifact reduction for simultaneous EEG/fMRI recording: Adaptive FIR reduction of imaging artifacts , 2006, Clinical Neurophysiology.

[47]  K. J. Blinowska,et al.  The application of parametric multichannel spectral estimates in the study of electrical brain activity , 2004, Biological Cybernetics.

[48]  Juergen Kurths,et al.  Phase Synchronization in Regular and Chaotic Systems: a Tutorial , 1999 .

[49]  R Biscay,et al.  Multiresolution decomposition of non-stationary EEG signals: a preliminary study. , 1995, Computers in biology and medicine.

[50]  P. Nunez,et al.  EEG and MEG coherence: Measures of functional connectivity at distinct spatial scales of neocortical dynamics , 2007, Journal of Neuroscience Methods.

[51]  P Y Ktonas,et al.  Estimation of time delay between EEG signals for epileptic focus localization: statistical error considerations. , 1991, Electroencephalography and clinical neurophysiology.

[52]  J. Régis,et al.  Enhanced EEG functional connectivity in mesial temporal lobe epilepsy , 2008, Epilepsy Research.

[53]  C. Yamaguchi,et al.  Fourier and wavelet analyses of normal and epileptic electroencephalogram (EEG) , 2003, First International IEEE EMBS Conference on Neural Engineering, 2003. Conference Proceedings..

[54]  S. N. Dorogovtsev,et al.  Complex networks created by aggregation. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[55]  D. Lehmann,et al.  Segmentation of brain electrical activity into microstates: model estimation and validation , 1995, IEEE Transactions on Biomedical Engineering.

[56]  Gonzalo R. Arce,et al.  Nonlinear Signal Processing - A Statistical Approach , 2004 .

[57]  Christoph M. Michel,et al.  Spatiotemporal Analysis of Multichannel EEG: CARTOOL , 2011, Comput. Intell. Neurosci..

[58]  F Cincotti,et al.  Imaging functional brain connectivity patterns from high-resolution EEG and fMRI via graph theory. , 2007, Psychophysiology.

[59]  C. Stam,et al.  Small-world networks and epilepsy: Graph theoretical analysis of intracerebrally recorded mesial temporal lobe seizures , 2007, Clinical Neurophysiology.

[60]  Görsev Yener,et al.  Decrease of evoked delta, theta and alpha coherences in Alzheimer patients during a visual oddball paradigm , 2008, Brain Research.

[61]  Juliane Britz,et al.  EEG microstate sequences in healthy humans at rest reveal scale-free dynamics , 2010, Proceedings of the National Academy of Sciences.

[62]  E. M. Hickin Modulation, Noise and Spectral Analysis , 1966 .

[63]  J P Lieb,et al.  Inter-hemispheric propagation of human mesial temporal lobe seizures: a coherence/phase analysis. , 1987, Electroencephalography and clinical neurophysiology.

[64]  Lonnie H. Hudgins,et al.  Wavelet transforms and atmopsheric turbulence. , 1993, Physical review letters.

[65]  Z. Šidák Rectangular Confidence Regions for the Means of Multivariate Normal Distributions , 1967 .

[66]  N. Mars,et al.  Time delay estimation in non-linear systems using average amount of mutual information analysis , 1982 .

[67]  C. Stam,et al.  Using graph theoretical analysis of multi channel EEG to evaluate the neural efficiency hypothesis , 2006, Neuroscience Letters.

[68]  Albert,et al.  Emergence of scaling in random networks , 1999, Science.

[69]  K. Pollard,et al.  Resampling-based Multiple Testing: Asymptotic Control of Type I Error and Applications to Gene Expression Data , 2003 .

[70]  A. Kraskov,et al.  Estimating mutual information. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[71]  E. Bedrosian A Product Theorem for Hilbert Transforms , 1963 .

[72]  Bin He,et al.  Cortical Activation Mapping of Epileptiform Activity Derived from Interictal ECoG Spikes , 2007, Epilepsia.

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

[74]  J Gotman,et al.  Interhemispheric interactions in seizures of focal onset: data from human intracranial recordings. , 1987, Electroencephalography and clinical neurophysiology.

[75]  Jürgen Kurths,et al.  Detection of n:m Phase Locking from Noisy Data: Application to Magnetoencephalography , 1998 .

[76]  J. Bellanger,et al.  A method to identify reproducible subsets of co-activated structures during interictal spikes. Application to intracerebral EEG in temporal lobe epilepsy , 2005, Clinical Neurophysiology.

[77]  J. Galambos Review: M. R. Leadbetter, Georg Lindgren and Holger Rootzen, Extremes and related properties of random sequences and processes , 1985 .

[78]  R. Andrzejak,et al.  Detection of weak directional coupling: phase-dynamics approach versus state-space approach. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[79]  P. Grassberger,et al.  A robust method for detecting interdependences: application to intracranially recorded EEG , 1999, chao-dyn/9907013.

[80]  F. L. D. Silva,et al.  Localization of epileptogenic foci using a new signal analytical approach , 1990, Neurophysiologie Clinique/Clinical Neurophysiology.

[81]  Gholam-Ali Hossein-Zadeh,et al.  MR artifact reduction in the simultaneous acquisition of EEG and FMRI of epileptic patients , 2008, 2008 16th European Signal Processing Conference.

[82]  Dietmar Plenz,et al.  Efficient Network Reconstruction from Dynamical Cascades Identifies Small-World Topology of Neuronal Avalanches , 2009, PLoS Comput. Biol..

[83]  Katarzyna J. Blinowska,et al.  A new method of the description of the information flow in the brain structures , 1991, Biological Cybernetics.

[84]  Mark J. van der Laan,et al.  Choice of a null distribution in resampling-based multiple testing , 2004 .

[85]  Kurths,et al.  Phase synchronization of chaotic oscillators. , 1996, Physical review letters.

[86]  Donald P. Percival,et al.  On estimation of the wavelet variance , 1995 .

[87]  D. Percival,et al.  Analysis of Subtidal Coastal Sea Level Fluctuations Using Wavelets , 1997 .

[88]  S. Smith,et al.  Measurement of interhemispheric time differences in generalised spike-and-wave. , 1992, Electroencephalography and clinical neurophysiology.

[89]  M Palus,et al.  Synchronization as adjustment of information rates: detection from bivariate time series. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[90]  R. Burke,et al.  Detecting dynamical interdependence and generalized synchrony through mutual prediction in a neural ensemble. , 1996, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[91]  L Tassi,et al.  [Electroclinical manifestations elicited by intracerebral electric stimulation "shocks" in temporal lobe epilepsy]. , 1993, Neurophysiologie clinique = Clinical neurophysiology.

[92]  Jr. J. L. Brown Analytic signals and product theorems for Hilbert transforms , 1974 .

[93]  F. H. Lopes da Silva,et al.  The role of hippocampal commissures in the interhemispheric transfer of epileptiform afterdischarges in the rat: a study using linear and non-linear regression analysis. , 1990, Electroencephalography and clinical neurophysiology.

[94]  F. Mormann,et al.  Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients , 2000 .

[95]  J. Bellanger,et al.  Interictal to Ictal Transition in Human Temporal Lobe Epilepsy: Insights From a Computational Model of Intracerebral EEG , 2005, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

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

[97]  M.A. Mananas,et al.  Connectivity analysis of EEG under drug therapy , 2007, 2007 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[98]  H. Keselman,et al.  Multiple Comparison Procedures , 2005 .

[99]  Koichi Sameshima,et al.  Using partial directed coherence to describe neuronal ensemble interactions , 1999, Journal of Neuroscience Methods.