EEG synchronization measures predict epilepsy-related BOLD-fMRI fluctuations better than commonly used univariate metrics

OBJECTIVE We hypothesize that the hypersynchronization associated with epileptic activity is best described by EEG synchronization measures, and propose to use these as predictors of epilepsy-related BOLD fluctuations. METHODS We computed the phase synchronization index (PSI) and global field synchronization (GFS), within two frequency bands, a broadband (1-45 Hz) and a narrower band focused on the presence of epileptic activity (3-10 Hz). The associated epileptic networks were compared with those obtained using conventional unitary regressors and two power-weighted metrics (total power and root mean square frequency), on nine simultaneous EEG-fMRI datasets from four epilepsy patients, exhibiting inter-ictal epileptiform discharges (IEDs). RESULTS The average PSI within 3-10 Hz achieved the best performance across several measures reflecting reliability in all datasets. The results were cross-validated through electrical source imaging of the IEDs. The applicability of PSI when no IEDs are recorded on the EEG was evaluated on three additional patients, yielding partially plausible networks in all cases. CONCLUSIONS Epileptic networks can be mapped based on the EEG PSI metric within an IED-specific frequency band, performing better than commonly used EEG metrics. SIGNIFICANCE This is the first study to investigate EEG synchronization measures as potential predictors of epilepsy-related BOLD fluctuations.

[1]  M. Castelo‐Branco,et al.  ICA decomposition of EEG signal for fMRI processing in epilepsy , 2009, Human brain mapping.

[2]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[3]  João Jorge,et al.  Presurgical brain mapping in epilepsy using simultaneous EEG and functional MRI at ultra-high field: feasibility and first results , 2016, Magnetic Resonance Materials in Physics, Biology and Medicine.

[4]  C. Michel,et al.  Electromagnetic Inverse Solutions in Anatomically Constrained Spherical Head Models , 2004, Brain Topography.

[5]  Gabriel Curio,et al.  Ultrahigh-frequency EEG during fMRI: Pushing the limits of imaging-artifact correction , 2009, NeuroImage.

[6]  S Warach,et al.  Monitoring the patient's EEG during echo planar MRI. , 1993, Electroencephalography and clinical neurophysiology.

[7]  Karen J. Mullinger,et al.  Reference layer artefact subtraction (RLAS): A novel method of minimizing EEG artefacts during simultaneous fMRI , 2014, NeuroImage.

[8]  Christoph M. Michel,et al.  Neuronal networks in children with continuous spikes and waves during slow sleep , 2010 .

[9]  Christoph M. Michel,et al.  The spatio-temporal mapping of epileptic networks: Combination of EEG–fMRI and EEG source imaging , 2009, NeuroImage.

[10]  Claudio Pollo,et al.  Electrical source imaging for presurgical focus localization in epilepsy patients with normal MRI , 2010, Epilepsia.

[11]  Patrick Dupont,et al.  Semi-automated EEG Enhancement Improves Localization of Ictal Onset Zone With EEG-Correlated fMRI , 2019, Front. Neurol..

[12]  Rodolfo Abreu,et al.  EEG-Informed fMRI: A Review of Data Analysis Methods , 2018, Front. Hum. Neurosci..

[13]  Frédéric Grouiller,et al.  A comparative study of different artefact removal algorithms for EEG signals acquired during functional MRI , 2007, NeuroImage.

[14]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.

[15]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[16]  Christoph M. Michel,et al.  Combination of EEG–fMRI and EEG source analysis improves interpretation of spike-associated activation networks in paediatric pharmacoresistant focal epilepsies , 2009, NeuroImage.

[17]  Rodolfo Abreu,et al.  Objective selection of epilepsy-related independent components from EEG data , 2016, Journal of Neuroscience Methods.

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

[19]  Helmut Laufs,et al.  Where the BOLD signal goes when alpha EEG leaves , 2006, NeuroImage.

[20]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[21]  Hellmuth Obrig,et al.  Correlates of alpha rhythm in functional magnetic resonance imaging and near infrared spectroscopy , 2003, NeuroImage.

[22]  Natasha M. Maurits,et al.  Correlating the alpha rhythm to BOLD using simultaneous EEG/fMRI: Inter-subject variability , 2006, NeuroImage.

[23]  Louis Lemieux,et al.  Simultaneous intracranial EEG and fMRI of interictal epileptic discharges in humans , 2011, NeuroImage.

[24]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[25]  Karl J. Friston,et al.  Hemodynamic correlates of EEG: A heuristic , 2005, NeuroImage.

[26]  Thomas Dierks,et al.  Increased phase synchronization during continuous face integration measured simultaneously with EEG and fMRI , 2012, Clinical Neurophysiology.

[27]  R. Buxton,et al.  Modeling the hemodynamic response to brain activation , 2004, NeuroImage.

[28]  Stephan Wolff,et al.  Spatial filters and automated spike detection based on brain topographies improve sensitivity of EEG–fMRI studies in focal epilepsy , 2007, NeuroImage.

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

[30]  M. Cook,et al.  EEG source localization in focal epilepsy: Where are we now? , 2008, Epilepsia.

[31]  Christoph M. Michel,et al.  Simultaneous EEG–fMRI at ultra-high field: Artifact prevention and safety assessment , 2015, NeuroImage.

[32]  Jean Gotman,et al.  Analysis of the EEG–fMRI response to prolonged bursts of interictal epileptiform activity , 2005, NeuroImage.

[33]  William D. Penny,et al.  Estimating the transfer function from neuronal activity to BOLD using simultaneous EEG-fMRI , 2010, NeuroImage.

[34]  Jean Gotman,et al.  Hemodynamic changes preceding the interictal EEG spike in patients with focal epilepsy investigated using simultaneous EEG-fMRI , 2009, NeuroImage.

[35]  M. Corbetta,et al.  Electrophysiological signatures of resting state networks in the human brain , 2007, Proceedings of the National Academy of Sciences.

[36]  Byron Bernal,et al.  fMRI Under Sedation: What Is the Best Choice in Children? , 2012, Journal of clinical medicine research.

[37]  M. Lassonde,et al.  Nonlinear hemodynamic responses in human epilepsy: A multimodal analysis with fNIRS-EEG and fMRI-EEG , 2012, Journal of Neuroscience Methods.

[38]  K J Werhahn,et al.  Electroencephalography during functional echo‐planar imaging: Detection of epileptic spikes using post‐processing methods , 2000, Magnetic resonance in medicine.

[39]  J. Gotman,et al.  Combining EEG and fMRI: A multimodal tool for epilepsy research , 2006, Journal of magnetic resonance imaging : JMRI.

[40]  M. Curtis,et al.  Interictal spikes in focal epileptogenesis , 2001, Progress in Neurobiology.

[41]  Catie Chang,et al.  Influence of heart rate on the BOLD signal: The cardiac response function , 2009, NeuroImage.

[42]  Karl J. Friston,et al.  Hemodynamic correlates of epileptiform discharges: An EEG-fMRI study of 63 patients with focal epilepsy , 2006, Brain Research.

[43]  L. Lemieux,et al.  Electrophysiological correlates of the BOLD signal for EEG‐informed fMRI , 2014, Human brain mapping.

[44]  Patricia Figueiredo,et al.  A study of the electro-haemodynamic coupling using simultaneously acquired intracranial EEG and fMRI data in humans , 2016, NeuroImage.

[45]  Jean Gotman,et al.  Combining EEG and fMRI in the study of epileptic discharges , 2011, Epilepsia.

[46]  Robert Turner,et al.  A Method for Removing Imaging Artifact from Continuous EEG Recorded during Functional MRI , 2000, NeuroImage.

[47]  Kaspar Anton Schindler,et al.  Synchronization and desynchronization in epilepsy: controversies and hypotheses , 2012, The Journal of physiology.

[48]  C. Michel,et al.  Accuracy of EEG source imaging of epileptic spikes in patients with large brain lesions , 2009, Clinical Neurophysiology.

[49]  Rodolfo Abreu,et al.  Identification of epileptic brain states by dynamic functional connectivity analysis of simultaneous EEG-fMRI: a dictionary learning approach , 2019, Scientific Reports.

[50]  M. Avoli,et al.  Mechanisms of epileptiform synchronization in cortical neuronal networks. , 2014, Current medicinal chemistry.

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

[52]  J. Daunizeau,et al.  The combination of EEG Source Imaging and EEG‐correlated functional MRI to map epileptic networks , 2010, Epilepsia.

[53]  R. Oostenveld,et al.  Frontal theta EEG activity correlates negatively with the default mode network in resting state. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[54]  John S. Duncan,et al.  Imaging haemodynamic changes related to seizures: Comparison of EEG-based general linear model, independent component analysis of fMRI and intracranial EEG , 2010, NeuroImage.

[55]  Yoko Yamaguchi,et al.  Long-range EEG phase synchronization during an arithmetic task indexes a coherent cortical network simultaneously measured by fMRI , 2005, NeuroImage.

[56]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[57]  L. R. Dice.  Measures of the Amount of Ecologic Association Between Species , 1945 .

[58]  Catie Chang,et al.  Effects of model-based physiological noise correction on default mode network anti-correlations and correlations , 2009, NeuroImage.

[59]  Willis J. Tompkins,et al.  A Real-Time QRS Detection Algorithm , 1985, IEEE Transactions on Biomedical Engineering.

[60]  Rodolfo Abreu,et al.  Physiological noise correction using ECG-derived respiratory signals for enhanced mapping of spontaneous neuronal activity with simultaneous EEG-fMRI , 2017, NeuroImage.

[61]  L. Lemieux,et al.  With or without spikes: localization of focal epileptic activity by simultaneous electroencephalography and functional magnetic resonance imaging. , 2011, Brain : a journal of neurology.

[62]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[63]  Antígona Martínez,et al.  Nonlinear temporal dynamics of the cerebral blood flow response , 2001, Human brain mapping.

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

[65]  Thomas Dierks,et al.  BOLD correlates of EEG alpha phase-locking and the fMRI default mode network , 2009, NeuroImage.

[66]  Christoph M. Michel,et al.  Continuous EEG source imaging enhances analysis of EEG-fMRI in focal epilepsy , 2010, NeuroImage.

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

[68]  Claudio Pollo,et al.  Electroencephalographic source imaging: a prospective study of 152 operated epileptic patients , 2011, Brain : a journal of neurology.

[69]  Helmut Laufs,et al.  A personalized history of EEG–fMRI integration , 2012, NeuroImage.

[70]  Dante Mantini,et al.  Adaptive optimal basis set for BCG artifact removal in simultaneous EEG-fMRI , 2018, Scientific Reports.

[71]  Afraim Salek-Haddadi,et al.  Event-Related fMRI with Simultaneous and Continuous EEG: Description of the Method and Initial Case Report , 2001, NeuroImage.

[72]  Marco Leite,et al.  Transfer Function between EEG and BOLD Signals of Epileptic Activity , 2013, Front. Neur..

[73]  João Jorge,et al.  Towards high-quality simultaneous EEG-fMRI at 7T: Detection and reduction of EEG artifacts due to head motion , 2015, NeuroImage.

[74]  Vangelis Sakkalis,et al.  Review of advanced techniques for the estimation of brain connectivity measured with EEG/MEG , 2011, Comput. Biol. Medicine.

[75]  Arno Villringer,et al.  Evaluating gradient artifact correction of EEG data acquired simultaneously with fMRI. , 2007, Magnetic resonance imaging.

[76]  Elizabeth A. Peck,et al.  Introduction to Linear Regression Analysis , 2001 .

[77]  J. Gotman,et al.  Independent component analysis as a model‐free approach for the detection of BOLD changes related to epileptic spikes: A simulation study , 2009, Human brain mapping.

[78]  Yann LeCun,et al.  Classification of patterns of EEG synchronization for seizure prediction , 2009, Clinical Neurophysiology.

[79]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[80]  Stephen M. Smith,et al.  Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm , 2001, IEEE Transactions on Medical Imaging.

[81]  Rodolfo Abreu,et al.  Ballistocardiogram artifact correction taking into account physiological signal preservation in simultaneous EEG-fMRI , 2016, NeuroImage.

[82]  Mark S. Cohen,et al.  Simultaneous EEG and fMRI of the alpha rhythm , 2002, Neuroreport.

[83]  Jeffery A. Hall,et al.  Electroencephalography/functional magnetic resonance imaging responses help predict surgical outcome in focal epilepsy , 2013, Epilepsia.

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

[85]  Marco Leite,et al.  Phase–amplitude coupling and the BOLD signal: A simultaneous intracranial EEG (icEEG) - fMRI study in humans performing a finger-tapping task , 2017, NeuroImage.

[86]  Alessandra Bertoldo,et al.  Integrating EEG and fMRI in epilepsy , 2011, NeuroImage.

[87]  L. Senhadji,et al.  From EEG signals to brain connectivity: A model-based evaluation of interdependence measures , 2009, Journal of Neuroscience Methods.

[88]  C. Michel,et al.  Noninvasive Localization of Electromagnetic Epileptic Activity. I. Method Descriptions and Simulations , 2004, Brain Topography.

[89]  Cheng Luo,et al.  BOLD-fMRI activity informed by network variation of scalp EEG in juvenile myoclonic epilepsy , 2019, NeuroImage: Clinical.

[90]  Alberto Leal,et al.  Characterisation and Reduction of the EEG Artefact Caused by the Helium Cooling Pump in the MR Environment: Validation in Epilepsy Patient Data , 2014, Brain Topography.

[91]  C. Michel,et al.  Propagation of Interictal Epileptiform Activity Can Lead to Erroneous Source Localizations: A 128-Channel EEG Mapping Study , 2003, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[92]  João Jorge,et al.  EEG–fMRI integration for the study of human brain function , 2014, NeuroImage.