Influence of Time-Series Normalization, Number of Nodes, Connectivity and Graph Measure Selection on Seizure-Onset Zone Localization from Intracranial EEG

We investigated the influence of processing steps in the estimation of multivariate directed functional connectivity during seizures recorded with intracranial EEG (iEEG) on seizure-onset zone (SOZ) localization. We studied the effect of (i) the number of nodes, (ii) time-series normalization, (iii) the choice of multivariate time-varying connectivity measure: Adaptive Directed Transfer Function (ADTF) or Adaptive Partial Directed Coherence (APDC) and (iv) graph theory measure: outdegree or shortest path length. First, simulations were performed to quantify the influence of the various processing steps on the accuracy to localize the SOZ. Afterwards, the SOZ was estimated from a 113-electrodes iEEG seizure recording and compared with the resection that rendered the patient seizure-free. The simulations revealed that ADTF is preferred over APDC to localize the SOZ from ictal iEEG recordings. Normalizing the time series before analysis resulted in an increase of 25–35% of correctly localized SOZ, while adding more nodes to the connectivity analysis led to a moderate decrease of 10%, when comparing 128 with 32 input nodes. The real-seizure connectivity estimates localized the SOZ inside the resection area using the ADTF coupled to outdegree or shortest path length. Our study showed that normalizing the time-series is an important pre-processing step, while adding nodes to the analysis did only marginally affect the SOZ localization. The study shows that directed multivariate Granger-based connectivity analysis is feasible with many input nodes (> 100) and that normalization of the time-series before connectivity analysis is preferred.

[1]  Hualou Liang,et al.  Short-window spectral analysis of cortical event-related potentials by adaptive multivariate autoregressive modeling: data preprocessing, model validation, and variability assessment , 2000, Biological Cybernetics.

[2]  Katarzyna J. Blinowska,et al.  Directed Transfer Function is not influenced by volume conduction—inexpedient pre-processing should be avoided , 2014, Front. Comput. Neurosci..

[3]  Karl J. Friston,et al.  Functional Connectivity: The Principal-Component Analysis of Large (PET) Data Sets , 1993, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[4]  Bin He,et al.  Estimation of Time-Varying Connectivity Patterns Through the Use of an Adaptive Directed Transfer Function , 2008, IEEE Transactions on Biomedical Engineering.

[5]  P J Allen,et al.  Very high-frequency rhythmic activity during SEEG suppression in frontal lobe epilepsy. , 1991, Electroencephalography and clinical neurophysiology.

[6]  J. Bellanger,et al.  Epileptic fast intracerebral EEG activity: evidence for spatial decorrelation at seizure onset. , 2003, Brain : a journal of neurology.

[7]  Roel Van Holen,et al.  EEG source connectivity to localize the seizure onset zone in patients with drug resistant epilepsy , 2017, NeuroImage: Clinical.

[8]  Fabrice Wendling,et al.  Frontiers in Systems Neuroscience Systems Neuroscience , 2022 .

[9]  Bin He,et al.  Graph analysis of epileptogenic networks in human partial epilepsy , 2011, Epilepsia.

[10]  Luiz A Baccalá,et al.  Graph theoretical characterization and tracking of the effective neural connectivity during episodes of mesial temporal epileptic seizure. , 2004, Journal of integrative neuroscience.

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

[12]  Bin He,et al.  Neocortical seizure foci localization by means of a directed transfer function method , 2010, Epilepsia.

[13]  Yvonne Höller,et al.  Altered directed functional connectivity in temporal lobe epilepsy in the absence of interictal spikes: A high density EEG study , 2016, Epilepsia.

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

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

[16]  Joachim Gross,et al.  The effect of filtering on Granger causality based multivariate causality measures , 2010, NeuroImage.

[17]  Georges Van Maele,et al.  Predictive factors for outcome of invasive video-EEG monitoring and subsequent resective surgery in patients with refractory epilepsy , 2010, Clinical Neurology and Neurosurgery.

[18]  Piotr J. Franaszczuk,et al.  Application of the Directed Transfer Function Method to Mesial and Lateral Onset Temporal Lobe Seizures , 2004, Brain Topography.

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

[20]  L.A. Baccald,et al.  Generalized Partial Directed Coherence , 2007, 2007 15th International Conference on Digital Signal Processing.

[21]  Laura Tassi,et al.  Epileptogenic networks of type II focal cortical dysplasia: A stereo-EEG study , 2012, NeuroImage.

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

[23]  Chang-Hwan Im,et al.  Localization of ictal onset zones in Lennox-Gastaut syndrome using directional connectivity analysis of intracranial electroencephalography , 2011, Seizure.

[24]  G. Alarcón,et al.  Power spectrum and intracranial EEG patterns at seizure onset in partial epilepsy. , 1995, Electroencephalography and clinical neurophysiology.

[25]  H Soltanian-Zadeh,et al.  Comparison of five directed graph measures for identification of leading interictal epileptic regions , 2010, Physiological measurement.

[26]  Christoph M. Michel,et al.  Towards the utilization of EEG as a brain imaging tool , 2012, NeuroImage.

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

[28]  Christoph M. Michel,et al.  Directed Functional Brain Connectivity Based on EEG Source Imaging: Methodology and Application to Temporal Lobe Epilepsy , 2016, IEEE Transactions on Biomedical Engineering.

[29]  P J Franaszczuk,et al.  Analysis of mesial temporal seizure onset and propagation using the directed transfer function method. , 1994, Electroencephalography and clinical neurophysiology.

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

[31]  Jorge Gonzalez-Martinez,et al.  The Stereo-Electroencephalography Methodology. , 2016, Neurosurgery clinics of North America.

[32]  E. Carrette,et al.  Functional brain connectivity from EEG in epilepsy: Seizure prediction and epileptogenic focus localization , 2014, Progress in Neurobiology.

[33]  Takaya Saito,et al.  The Precision-Recall Plot Is More Informative than the ROC Plot When Evaluating Binary Classifiers on Imbalanced Datasets , 2015, PloS one.

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

[35]  Laura Astolfi,et al.  Spectrally weighted Granger-causal modeling: Motivation and applications to data from animal models and epileptic patients , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[36]  Katarzyna J. Blinowska,et al.  Review of the methods of determination of directed connectivity from multichannel data , 2011, Medical & Biological Engineering & Computing.

[37]  Andrea Brovelli,et al.  Graph Measures of Node Strength for Characterizing Preictal Synchrony in Partial Epilepsy , 2016, Brain Connect..

[38]  Chang-Hwan Im,et al.  Localization and propagation analysis of ictal source rhythm by electrocorticography , 2010, NeuroImage.

[39]  Mark W. Woolrich,et al.  Measuring functional connectivity in MEG: A multivariate approach insensitive to linear source leakage , 2012, NeuroImage.

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

[41]  Gregory A. Worrell,et al.  Modeling cortical source dynamics and interactions during seizure , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.