BOLD correlates of continuously fluctuating epileptic activity isolated by independent component analysis

Combined EEG/fMRI recordings offer a promising opportunity to detect brain areas with altered BOLD signal during interictal epileptic discharges (IEDs). These areas are likely to represent the irritative zone, which is itself a reflection of the epileptogenic zone. This paper reports on the imaging findings using independent component analysis (ICA) to continuously quantify epileptiform activity in simultaneously acquired EEG and fMRI. Using ICA derived factors coding for the epileptic activity takes into account that epileptic activity is continuously fluctuating with each spike differing in amplitude, duration and maybe topography, including subthreshold epileptic activity besides clear IEDs and may thus increase the sensitivity and statistical power of combined EEG/fMRI in epilepsy. Twenty patients with different types of focal and generalized epilepsy syndromes were investigated. ICA separated epileptiform activity from normal physiological brain activity and artifacts. In 16/20 patients, BOLD correlates of epileptic activity matched the EEG sources, the clinical semiology, and, if present, the structural lesions. In clinically equivocal cases, the BOLD correlates aided to attribute proper diagnosis of the underlying epilepsy syndrome. Furthermore, in one patient with temporal lobe epilepsy, BOLD correlates of rhythmic delta activity could be employed to delineate the affected hippocampus. Compared to BOLD correlates of manually identified IEDs, the sensitivity was improved from 50% (10/20) to 80%. The ICA EEG/fMRI approach is a safe, non-invasive and easily applicable technique, which can be used to identify regions with altered hemodynamic effects related to IEDs as well as intermittent rhythmic discharges in different types of epilepsy.

[1]  P. LeVan,et al.  Independent Component Analysis in the Study of Focal Seizures , 2006, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[2]  C. Jack,et al.  Subtraction ictal SPECT co‐registered to MRI improves clinical usefulness of SPECT in localizing the surgical seizure focus , 1998, Neurology.

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

[4]  E Urrestarazu,et al.  [Independent Components Analysis (ICA) in the study of electroencephalographic signals]. , 2005, Neurologia.

[5]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[6]  Douglas M. Bowden,et al.  NeuroNames Brain Hierarchy , 1995, NeuroImage.

[7]  Marco Carnì,et al.  EEG/fMRI Study of Ictal and Interictal Epileptic Activity: Methodological Issues and Future Perspectives in Clinical Practice , 2006, Epilepsia.

[8]  R. Wennberg,et al.  The contribution of 18F-FDG PET in preoperative epilepsy surgery evaluation for patients with temporal lobe epilepsy A meta-analysis , 2007, Seizure.

[9]  G. Srivastava,et al.  ICA-based procedures for removing ballistocardiogram artifacts from EEG data acquired in the MRI scanner , 2005, NeuroImage.

[10]  Manuel Abbafati,et al.  An independent component analysis-based approach on ballistocardiogram artifact removing. , 2006, Magnetic resonance imaging.

[11]  Terence J O'Brien,et al.  Evaluating the Utility of Inpatient Video‐EEG Monitoring , 2004, Epilepsia.

[12]  H. Lüders,et al.  The epileptogenic zone: general principles. , 2006, Epileptic disorders : international epilepsy journal with videotape.

[13]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[14]  T. Sejnowski,et al.  Removal of eye activity artifacts from visual event-related potentials in normal and clinical subjects , 2000, Clinical Neurophysiology.

[15]  J. Gotman,et al.  Isolation of epileptiform discharges from unaveraged EEG by independent component analysis , 1999, Clinical Neurophysiology.

[16]  C. Michel,et al.  128-Channel EEG Source Imaging in Epilepsy: Clinical Yield and Localization Precision , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[17]  J Gotman,et al.  Separation of spikes from background by independent component analysis with dipole modeling and comparison to intracranial recording , 2001, Clinical Neurophysiology.

[18]  L F Quesney,et al.  Presurgical EEG investigation in frontal lobe epilepsy. , 1992, Epilepsy research. Supplement.

[19]  Karl J. Friston,et al.  EEG–fMRI of idiopathic and secondarily generalized epilepsies , 2006, NeuroImage.

[20]  Jérémie Mattout,et al.  Symmetrical event-related EEG/fMRI information fusion in a variational Bayesian framework , 2007, NeuroImage.

[21]  Hiroshi Shibasaki,et al.  Use of magnetoencephalography in the presurgical evaluation of epilepsy patients , 2007, Clinical Neurophysiology.

[22]  Jean Gotman,et al.  EEG‐fMRI of focal epileptic spikes: Analysis with multiple haemodynamic functions and comparison with gadolinium‐enhanced MR angiograms , 2004, Human brain mapping.

[23]  Bettina Sorger,et al.  Improved quality of auditory event-related potentials recorded simultaneously with 3-T fMRI: Removal of the ballistocardiogram artefact , 2007, NeuroImage.

[24]  Frank Gilliam,et al.  Significance of interictal temporal lobe delta activity for localization of the primary epileptogenic region , 1999, Neurology.

[25]  J. Gotman,et al.  fMRI Activation in Continuous and Spike‐triggered EEG–fMRI Studies of Epileptic Spikes , 2003, Epilepsia.

[26]  C. Elger,et al.  Clinical Relevance of Quantified Intracranial Interictal Spike Activity in Presurgical Evaluation of Epilepsy , 2000, Epilepsia.

[27]  P. G. Larsson,et al.  3T phased array MRI improves the presurgical evaluation in focal epilepsies , 2005, Neurology.

[28]  Terence J O'Brien,et al.  Subtraction ictal single-photon emission computed tomography coregistered to magnetic resonance imaging in evaluating the need for repeated epilepsy surgery. , 2006, Journal of neurosurgery.

[29]  A. Kleinschmidt,et al.  Linking Generalized Spike‐and‐Wave Discharges and Resting State Brain Activity by Using EEG/fMRI in a Patient with Absence Seizures , 2006, Epilepsia.

[30]  Jean Gotman,et al.  Negative BOLD responses to epileptic spikes , 2006, Human brain mapping.

[31]  Jean Gotman,et al.  EEG–fMRI of epileptic spikes: Concordance with EEG source localization and intracranial EEG , 2006, NeuroImage.

[32]  Tzyy-Ping Jung,et al.  Imaging brain dynamics using independent component analysis , 2001, Proc. IEEE.

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

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

[35]  B H Brinkmann,et al.  Subtraction SPECT co-registered to MRI improves postictal SPECT localization of seizure foci , 1999, Neurology.

[36]  P. G. Larsson,et al.  The value of multichannel MEG and EEG in the presurgical evaluation of 70 epilepsy patients , 2006, Epilepsy Research.

[37]  J. Gotman,et al.  Generalized epileptic discharges show thalamocortical activation and suspension of the default state of the brain. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[38]  J. Gotman,et al.  fMRI activation during spike and wave discharges in idiopathic generalized epilepsy. , 2004, Brain : a journal of neurology.

[39]  Anthony B Waites,et al.  fMRI “deactivation” of the posterior cingulate during generalized spike and wave , 2003, NeuroImage.

[40]  L. Lemieux,et al.  Recording of EEG during fMRI experiments: Patient safety , 1997, Magnetic resonance in medicine.

[41]  R. Knowlton,et al.  Multimodality imaging in partial epilepsies , 2004, Current opinion in neurology.

[42]  Karl J. Friston,et al.  Studying spontaneous EEG activity with fMRI , 2003, Brain Research Reviews.

[43]  Rainer Goebel,et al.  Mapping directed influence over the brain using Granger causality and fMRI , 2005, NeuroImage.

[44]  J S Duncan,et al.  Imaging in epilepsy , 2005, Journal of Neurology, Neurosurgery & Psychiatry.

[45]  John S. Duncan,et al.  Analysis of EEG–fMRI data in focal epilepsy based on automated spike classification and Signal Space Projection , 2006, NeuroImage.

[46]  W R Webber,et al.  Practical detection of epileptiform discharges (EDs) in the EEG using an artificial neural network: a comparison of raw and parameterized EEG data. , 1994, Electroencephalography and clinical neurophysiology.

[47]  J. Gotman,et al.  Correspondence between EEG-fMRI and EEG dipole localisation of interictal discharges in focal epilepsy , 2006, NeuroImage.

[48]  G. Glover Deconvolution of Impulse Response in Event-Related BOLD fMRI1 , 1999, NeuroImage.

[49]  D. Lehmann,et al.  Functional imaging with low-resolution brain electromagnetic tomography (LORETA): a review. , 2002, Methods and findings in experimental and clinical pharmacology.

[50]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[51]  Daniel Brandeis,et al.  Synchronization facilitates removal of MRI artefacts from concurrent EEG recordings and increases usable bandwidth , 2006, NeuroImage.

[52]  Terence J. O'Brien,et al.  “Magnetic Resonance Imaging Negative Positron Emission Tomography Positive” Temporal Lobe Epilepsy: FDG-PET Pattern Differs from Mesial Temporal Lobe Epilepsy , 2006, Molecular Imaging and Biology.

[53]  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.

[54]  C.J. James,et al.  Tracking Epileptiform Activity in the Multichannel Ictal EEG using Spatially Constrained Independent Component Analysis , 2005, 2005 IEEE Engineering in Medicine and Biology 27th Annual Conference.

[55]  John S. Duncan,et al.  BOLD and perfusion changes during epileptic generalised spike wave activity , 2008, NeuroImage.

[56]  Louis Lemieux,et al.  Identification of EEG Events in the MR Scanner: The Problem of Pulse Artifact and a Method for Its Subtraction , 1998, NeuroImage.

[57]  Gian Luca Romani,et al.  Complete artifact removal for EEG recorded during continuous fMRI using independent component analysis , 2007, NeuroImage.

[58]  R D Pascual-Marqui,et al.  Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. , 2002, Methods and findings in experimental and clinical pharmacology.

[59]  M R Symms,et al.  EEG-triggered functional MRI of interictal epileptiform activity in patients with partial seizures. , 1999, Brain : a journal of neurology.

[60]  Christopher J James,et al.  Independent component analysis for biomedical signals , 2005, Physiological measurement.

[61]  Ravi S. Menon,et al.  Linear aspects of transformation from interictal epileptic discharges to BOLD fMRI signals in an animal model of occipital epilepsy , 2006, NeuroImage.