Detection of epileptic activity in fMRI without recording the EEG

EEG-fMRI localizes epileptic foci by detecting cerebral hemodynamic changes that are correlated to epileptic events visible in EEG. However, scalp EEG is insensitive to activity restricted to deep structures and recording the EEG in the scanner is complex and results in major artifacts that are difficult to remove. This study presents a new framework for identifying the BOLD manifestations of epileptic discharges without having to record the EEG. The first stage is based on the detection of epileptic events for each voxel by sparse representation in the wavelet domain. The second stage is to gather voxels according to proximity in time and space of detected activities. This technique was evaluated on data generated by superposing artificial responses at different locations and responses amplitude in the brain for 6 control subject runs. The method was able to detect effectively and consistently for responses amplitude of at least 1% above baseline. 46 runs from 15 patients with focal epilepsy were investigated. The results demonstrate that the method detected at least one concordant event in 37/41 runs. The maps of activation obtained from our method were more similar to those obtained by EEG-fMRI than to those obtained by the other method used in this context, 2D-Temporal Cluster Analysis. For 5 runs without event read on scalp EEG, 3 runs showed an activation concordant with the patient's diagnostic. It may therefore be possible, at least when spikes are infrequent, to detect their BOLD manifestations without having to record the EEG.

[1]  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.

[2]  Yves Goussard,et al.  Unsupervised deconvolution of sparse spike trains using stochastic approximation , 1996, IEEE Trans. Signal Process..

[3]  Karl J. Friston,et al.  Nonlinear Responses in fMRI: The Balloon Model, Volterra Kernels, and Other Hemodynamics , 2000, NeuroImage.

[4]  R Baumgartner,et al.  Comparison of two exploratory data analysis methods for fMRI: fuzzy clustering vs. principal component analysis. , 2000, Magnetic resonance imaging.

[5]  Oliver Granert,et al.  Changes in activity of striato–thalamo–cortical network precede generalized spike wave discharges , 2008, NeuroImage.

[6]  J. Gotman,et al.  Temporal and Extratemporal BOLD Responses to Temporal Lobe Interictal Spikes , 2006, Epilepsia.

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

[8]  Sylvain Faisan,et al.  Hidden Markov multiple event sequence models: A paradigm for the spatio-temporal analysis of fMRI data , 2007, Medical Image Anal..

[9]  Yaakov Tsaig,et al.  Fast Solution of $\ell _{1}$ -Norm Minimization Problems When the Solution May Be Sparse , 2008, IEEE Transactions on Information Theory.

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

[11]  B. Rosen,et al.  Evidence of a Cerebrovascular Postarteriole Windkessel with Delayed Compliance , 1999, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[12]  Alan C. Evans,et al.  A general statistical analysis for fMRI data , 2000, NeuroImage.

[13]  Fan Chung,et al.  Spectral Graph Theory , 1996 .

[14]  M. Lindquist,et al.  Validity and power in hemodynamic response modeling: A comparison study and a new approach , 2007, Human brain mapping.

[15]  O Josephs,et al.  Event-related functional magnetic resonance imaging: modelling, inference and optimization. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[16]  Bertrand Thirion,et al.  A fully Bayesian approach to the parcel-based detection-estimation of brain activity in fMRI , 2008, NeuroImage.

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

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

[19]  Mohamed-Jalal Fadili,et al.  Activelets: Wavelets for sparse representation of hemodynamic responses , 2011, Signal Process..

[20]  Habib Benali,et al.  CORSICA: correction of structured noise in fMRI by automatic identification of ICA components. , 2007, Magnetic resonance imaging.

[21]  I. Johnstone,et al.  Ideal spatial adaptation by wavelet shrinkage , 1994 .

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

[23]  Indrayana Rustandi,et al.  Modeling fMRI data generated by overlapping cognitive processes with unknown onsets using Hidden Process Models , 2009, NeuroImage.

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

[25]  Yihong Yang,et al.  Mapping Transient, Randomly Occurring Neuropsychological Events Using Independent Component Analysis , 2001, NeuroImage.

[26]  Jérôme Idier,et al.  Enhanced sampling schemes for MCMC based blind Bernoulli-Gaussian deconvolution , 2009, Signal Process..

[27]  J. Gotman Epileptic networks studied with EEG‐fMRI , 2008, Epilepsia.

[28]  Ildar Khalidov,et al.  Operator-like wavelets with application to functional magnetic resonance imaging , 2009 .

[29]  Yingli Lu,et al.  BOLD changes occur prior to epileptic spikes seen on scalp EEG , 2007, NeuroImage.

[30]  S. Ruan,et al.  A multistep Unsupervised Fuzzy Clustering Analysis of fMRI time series , 2000, Human brain mapping.

[31]  Yingli Lu,et al.  Using voxel-specific hemodynamic response function in EEG-fMRI data analysis , 2006, NeuroImage.

[32]  Yingli Lu,et al.  Using voxel-specific hemodynamic response function in EEG-fMRI data analysis: An estimation and detection model , 2007, NeuroImage.

[33]  Victoria L Morgan,et al.  Resting functional MRI with temporal clustering analysis for localization of epileptic activity without EEG , 2004, NeuroImage.

[34]  Jean Gotman,et al.  Limits of 2D-TCA in detecting BOLD responses to epileptic activity , 2011, Epilepsy Research.

[35]  R. Buxton,et al.  Dynamics of blood flow and oxygenation changes during brain activation: The balloon model , 1998, Magnetic resonance in medicine.

[36]  Xenophon Papademetris,et al.  Graph-theory based parcellation of functional subunits in the brain from resting-state fMRI data , 2010, NeuroImage.

[37]  F. Leijten,et al.  EEG-fMRI in the preoperative work-up for epilepsy surgery. , 2007, Brain : a journal of neurology.

[38]  Jean Gotman,et al.  The BOLD Response to Interictal Epileptiform Discharges , 2002, NeuroImage.

[39]  Robert D. Nowak,et al.  Wavelet-based statistical signal processing using hidden Markov models , 1998, IEEE Trans. Signal Process..

[40]  L. K. Hansen,et al.  Feature‐space clustering for fMRI meta‐analysis , 2001, Human brain mapping.

[41]  Jean-Baptiste Poline,et al.  A group model for stable multi-subject ICA on fMRI datasets , 2010, NeuroImage.

[42]  Yong Li,et al.  Development of 2dTCA for the detection of irregular, transient bold activity , 2008, Human brain mapping.

[43]  Dario Farina,et al.  Spike Sorting by Stochastic Simulation , 2011, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[44]  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.

[45]  John C. Gore,et al.  Cluster analysis detection of functional MRI activity in temporal lobe epilepsy , 2007, Epilepsy Research.

[46]  C. C. Gaudes,et al.  Detection and characterization of single‐trial fMRI bold responses: Paradigm free mapping , 2011, Human brain mapping.

[47]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[48]  J Gotman,et al.  Different structures involved during ictal and interictal epileptic activity in malformations of cortical development: an EEG-fMRI study. , 2008, Brain : a journal of neurology.

[49]  J. Gotman,et al.  Quality of EEG in simultaneous EEG-fMRI for epilepsy , 2003, Clinical Neurophysiology.

[50]  Mark W. Woolrich,et al.  Fully Bayesian spatio-temporal modeling of FMRI data , 2004, IEEE Transactions on Medical Imaging.

[51]  Jitendra Malik,et al.  Normalized cuts and image segmentation , 1997, Proceedings of IEEE Computer Society Conference on Computer Vision and Pattern Recognition.