Altered functional connectivity in seizure onset zones revealed by fMRI intrinsic connectivity

Objective: The purpose of this study was to investigate functional connectivity (FC) changes in epileptogenic networks in intractable partial epilepsy obtained from resting-state fMRI by using intrinsic connectivity contrast (ICC), a voxel-based network measure of degree that reflects the number of connections to each voxel. Methods: We measured differences between intrahemispheric- and interhemispheric-ICC (ICCintra−inter) that could reveal localized connectivity abnormalities in epileptogenic zones while more global network changes would be eliminated when subtracting these values. The ICCintra−inter map was compared with the seizure onset zone (SOZ) based on intracranial EEG (icEEG) recordings in 29 patients with at least 1 year of postsurgical follow-up. Two independent reviewers blindly interpreted the icEEG and fMRI data, and the concordance rates were compared for various clinical factors. Results: Concordance between the icEEG SOZ and ICCintra−inter map was observed in 72.4% (21/29) of the patients, which was higher in patients with good surgical outcome, especially in those patients with temporal lobe epilepsy (TLE) or lateral temporal seizure localization. Concordance was also better in the extratemporal lobe epilepsy than the TLE group. In 85.7% (18/21) of the cases, the ICCintra−inter values were negative in the SOZ, indicating decreased FC within the epileptic hemisphere relative to between hemispheres. Conclusions: Assessing alterations in FC using fMRI-ICC map can help localize the SOZ, which has potential as a noninvasive presurgical diagnostic tool to improve surgical outcome. In addition, the method reveals that, in focal epilepsy, both intrahemispheric- and interhemispheric-FC may be altered, in the presence of both regional as well as global network abnormalities.

[1]  Andreas Schulze-Bonhage,et al.  Reduced interhemispheric hippocampal BOLD signal coupling related to early epilepsy onset , 2009, Seizure.

[2]  Dustin Scheinost,et al.  Unified Framework for Development, Deployment and Robust Testing of Neuroimaging Algorithms , 2011, Neuroinformatics.

[3]  E. Bilevicius,et al.  Asymmetrical hippocampal connectivity in mesial temporal lobe epilepsy: evidence from resting state fMRI , 2010, BMC Neuroscience.

[4]  Dustin Scheinost,et al.  Potential Use and Challenges of Functional Connectivity Mapping in Intractable Epilepsy , 2013, Front. Neurol..

[5]  P. Chauvel,et al.  Decreased basal fMRI functional connectivity in epileptogenic networks and contralateral compensatory mechanisms , 2009, Human brain mapping.

[6]  S. Schultz Principles of Neural Science, 4th ed. , 2001 .

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

[8]  M. Kramer,et al.  Epilepsy as a Disorder of Cortical Network Organization , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[9]  Jorge Sepulcre,et al.  Localization of focal epileptic discharges using functional connectivity magnetic resonance imaging. , 2011, Journal of neurosurgery.

[10]  W. Liao,et al.  Impaired perceptual networks in temporal lobe epilepsy revealed by resting fMRI , 2009, Journal of Neurology.

[11]  W T Blume,et al.  Proposal for a New Classification of Outcome with Respect to Epileptic Seizures Following Epilepsy Surgery , 2001, Epilepsia.

[12]  J. R. Landis,et al.  The measurement of observer agreement for categorical data. , 1977, Biometrics.

[13]  Andrew J. Cole,et al.  Surgical Treatment of the Epilepsies, 2nd Ed. , 1994, Neurology.

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

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

[16]  Maolin Qiu,et al.  A whole-brain voxel based measure of intrinsic connectivity contrast reveals local changes in tissue connectivity with anesthetic without a priori assumptions on thresholds or regions of interest , 2011, NeuroImage.

[17]  John C. Gore,et al.  Functional epileptic network in left mesial temporal lobe epilepsy detected using resting fMRI , 2010, Epilepsy Research.

[18]  Jed A. Meltzer,et al.  Effects of Working Memory Load on Oscillatory Power in Human Intracranial EEG , 2007, Cerebral cortex.

[19]  Friedrich G Woermann,et al.  Imaging structure and function in refractory focal epilepsy , 2005, The Lancet Neurology.

[20]  P. Hofman,et al.  Loss of network efficiency associated with cognitive decline in chronic epilepsy , 2011, Neurology.

[21]  Laurent Spelle,et al.  Insular cortex involvement in mesiotemporal lobe epilepsy: A positron emission tomography study , 2002, Annals of neurology.

[22]  Bin He,et al.  Analysis of epileptogenic network properties during ictal activity , 2009, 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[23]  Jerome Engel,et al.  Outcome with respect to epileptic seizures. , 1993 .

[24]  R Todd Constable,et al.  Functional MRI connectivity as a predictor of the surgical outcome of epilepsy , 2011, Epilepsia.

[25]  R. Todd Constable,et al.  Social network theory applied to resting-state fMRI connectivity data in the identification of epilepsy networks with iterative feature selection , 2011, Journal of Neuroscience Methods.

[26]  Xenophon Papademetris,et al.  More accurate Talairach coordinates for neuroimaging using non-linear registration , 2008, NeuroImage.

[27]  Huafu Chen,et al.  Altered Functional Connectivity and Small-World in Mesial Temporal Lobe Epilepsy , 2010, PloS one.

[28]  Robert T. Schultz,et al.  Integrated Intensity and Point-Feature Nonrigid Registration. , 2001 .

[29]  L. Lemieux,et al.  Interictal Functional Connectivity of Human Epileptic Networks Assessed by Intracerebral EEG and BOLD Signal Fluctuations , 2011, PLoS ONE.

[30]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[31]  Kaspar Anton Schindler,et al.  Assessing seizure dynamics by analysing the correlation structure of multichannel intracranial EEG. , 2006, Brain : a journal of neurology.

[32]  Huafu Chen,et al.  fMRI study of mesial temporal lobe epilepsy using amplitude of low‐frequency fluctuation analysis , 2010, Human brain mapping.

[33]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[34]  M. Dichter,et al.  Cellular mechanisms of epilepsy: a status report. , 1987, Science.

[35]  Jean Daunizeau,et al.  Concepts of Connectivity and Human Epileptic Activity , 2011, Front. Syst. Neurosci..

[36]  Max A. Viergever,et al.  Characterization of Functional and Structural Integrity in Experimental Focal Epilepsy: Reduced Network Efficiency Coincides with White Matter Changes , 2012, PloS one.

[37]  John C Gore,et al.  Resting state functional connectivity of the hippocampus associated with neurocognitive function in left temporal lobe epilepsy , 2014, Human brain mapping.

[38]  Bertrand Devaux,et al.  Metabolic changes and electro-clinical patterns in mesio-temporal lobe epilepsy: a correlative study. , 2004, Brain : a journal of neurology.

[39]  Bennett A. Landman,et al.  Functional Networks in Temporal-Lobe Epilepsy: A Voxel-Wise Study of Resting-State Functional Connectivity and Gray-Matter Concentration , 2013, Brain Connect..

[40]  Robert T. Schultz,et al.  Integrated Intensity and Point-Feature Nonrigid Registration , 2004, MICCAI.

[41]  P. Chauvel,et al.  Role of resting state functional connectivity MRI in presurgical investigation of mesial temporal lobe epilepsy , 2010, Journal of Neurology, Neurosurgery & Psychiatry.

[42]  A. Turken,et al.  The Neural Architecture of the Language Comprehension Network: Converging Evidence from Lesion and Connectivity Analyses , 2011, Front. Syst. Neurosci..