Magnetoencephalographic signatures of insular epileptic spikes based on functional connectivity

Failure to recognize insular cortex seizures has recently been identified as a cause of epilepsy surgeries targeting the temporal, parietal, or frontal lobe. Such failures are partly due to the fact that current noninvasive localization techniques fare poorly in recognizing insular epileptic foci. Our group recently demonstrated that magnetoencephalography (MEG) is sensitive to epileptiform spikes generated by the insula. In this study, we assessed the potential of distributed source imaging and functional connectivity analyses to distinguish insular networks underlying the generation of spikes. Nineteen patients with operculo‐insular epilepsy were investigated. Each patient underwent MEG as well as T1‐weighted magnetic resonance imaging (MRI) as part of their standard presurgical evaluation. Cortical sources of MEG spikes were reconstructed with the maximum entropy on the mean algorithm, and their time courses served to analyze source functional connectivity. The results indicate that the anterior and posterior subregions of the insula have specific patterns of functional connectivity mainly involving frontal and parietal regions, respectively. In addition, while their connectivity patterns are qualitatively similar during rest and during spikes, couplings within these networks are much stronger during spikes. These results show that MEG can establish functional connectivity‐based signatures that could help in the diagnosis of different subtypes of insular cortex epilepsy. Hum Brain Mapp 37:3250–3261, 2016. © 2016 Wiley Periodicals, Inc.

[1]  Lionel Carmant,et al.  Revisiting the role of the insula in refractory partial epilepsy , 2009, Epilepsia.

[2]  Cécile Amblard,et al.  Biomagnetic source detection by maximum entropy and graphical models , 2004, IEEE Transactions on Biomedical Engineering.

[3]  Matti S. Hämäläinen,et al.  Clinical value of magnetoencephalographic spike propagation represented by spatiotemporal source analysis: Correlation with surgical outcome , 2014, Epilepsy Research.

[4]  Hiroshi Shibasaki,et al.  Simultaneous Recording of Epileptiform Discharges by MEG and Subdural Electrodes in Temporal Lobe Epilepsy , 1997, NeuroImage.

[5]  Moritz Grosse-Wentrup,et al.  Multisubject Learning for Common Spatial Patterns in Motor-Imagery BCI , 2011, Comput. Intell. Neurosci..

[6]  C. Bénar,et al.  Interictal networks in Magnetoencephalography , 2014, Human brain mapping.

[7]  Rafeed Alkawadri,et al.  Sensitivity of scalp 10–20 EEG and magnetoencephalography , 2013, Epileptic disorders : international epilepsy journal with videotape.

[8]  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.

[9]  Stefan Rampp,et al.  MEG-based identification of the epileptogenic zone in occult peri-insular epilepsy , 2012, Seizure.

[10]  D. Lehmann,et al.  Segmentation of brain electrical activity into microstates: model estimation and validation , 1995, IEEE Transactions on Biomedical Engineering.

[11]  F. Flynn,et al.  Anatomy of the insula functional and clinical correlates , 1999 .

[12]  Patrick Kwan,et al.  Epilepsy after the first drug fails: substitution or add-on? , 2000, Seizure.

[13]  W T Blume,et al.  A randomized, controlled trial of surgery for temporal-lobe epilepsy. , 2001, The New England journal of medicine.

[14]  Christophe Grova,et al.  MEG Source Localization of Spatially Extended Generators of Epileptic Activity: Comparing Entropic and Hierarchical Bayesian Approaches , 2013, PloS one.

[15]  L. Ferini-Strambi,et al.  Nocturnal frontal lobe epilepsy , 1997 .

[16]  C. N. Guy,et al.  Intracerebral propagation of interictal activity in partial epilepsy: implications for source localisation. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[17]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[18]  Daniel S. Margulies,et al.  Mapping the functional connectivity of anterior cingulate cortex , 2007, NeuroImage.

[19]  Jean Gotman,et al.  Spatial correlation of hemodynamic changes related to interictal epileptic discharges with electric and magnetic source imaging , 2014, Human brain mapping.

[20]  M. Mesulam,et al.  Insula of the old world monkey. III: Efferent cortical output and comments on function , 1982, The Journal of comparative neurology.

[21]  F. Mauguière,et al.  Clinical manifestations of insular lobe seizures: a stereo-electroencephalographic study , 2008, Clinical Neurophysiology.

[22]  P. Chauvel,et al.  Epileptogenicity of brain structures in human temporal lobe epilepsy: a quantified study from intracerebral EEG. , 2008, Brain : a journal of neurology.

[23]  C. Michel,et al.  Electric source imaging of interictal activity accurately localises the seizure onset zone , 2013, Journal of Neurology, Neurosurgery & Psychiatry.

[24]  François Dubeau,et al.  Localization Accuracy of Distributed Inverse Solutions for Electric and Magnetic Source Imaging of Interictal Epileptic Discharges in Patients with Focal Epilepsy , 2015, Brain Topography.

[25]  N. Crone,et al.  Network dynamics of the brain and influence of the epileptic seizure onset zone , 2014, Proceedings of the National Academy of Sciences.

[26]  Bin He,et al.  Source Connectivity Analysis from MEG and its Application to Epilepsy Source Localization , 2011, Brain Topography.

[27]  Seppo P. Ahlfors,et al.  Propagation of epileptic spikes reconstructed from spatiotemporal magnetoencephalographic and electroencephalographic source analysis , 2010, NeuroImage.

[28]  S. Spencer.  Neural Networks in Human Epilepsy: Evidence of and Implications for Treatment , 2002, Epilepsia.

[29]  M. Lassonde,et al.  Neuropsychological performance before and after partial or complete insulectomy in patients with epilepsy , 2015, Epilepsy & Behavior.

[30]  Eugen Trinka,et al.  Successful surgical treatment of insular epilepsy with nocturnal hypermotor seizures , 2008, Epilepsia.

[31]  Hideyuki Nakama,et al.  Hypermotor Seizure Arising from Insular Cortex , 2006, Epilepsia.

[32]  Naomi B. Pitskel,et al.  Three Systems of Insular Functional Connectivity Identified with Cluster Analysis , 2010, Cerebral cortex.

[33]  Dang Khoa Nguyen,et al.  Temporal Lobe Epilepsy Surgery Failures: A Review , 2012, Epilepsy research and treatment.

[34]  Jean Gotman,et al.  Evaluation of EEG localization methods using realistic simulations of interictal spikes , 2006, NeuroImage.

[35]  Katiuscia Sacco,et al.  Meta-analytic clustering of the insular cortex Characterizing the meta-analytic connectivity of the insula when involved in active tasks , 2012, NeuroImage.

[36]  D. N. Pandya,et al.  Insular interconnections with the amygdala in the rhesus monkey , 1981, Neuroscience.

[37]  G. R. Barnes,et al.  A Quantitative Assessment of the Sensitivity of Whole-Head MEG to Activity in the Adult Human Cortex , 2002, NeuroImage.

[38]  Christoph Baumgartner,et al.  Magnetoencephalography in presurgical epilepsy evaluation , 2002, Neurosurgical Review.

[39]  J. R. Augustine.  Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.

[40]  András Jakab,et al.  Connectivity-based parcellation reveals interhemispheric differences in the insula , 2011, Brain Topography.

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

[42]  Manon Robert,et al.  The utility of magnetoencephalography in the presurgical evaluation of refractory insular epilepsy , 2013, Epilepsia.

[43]  C D Binnie,et al.  Origin and propagation of interictal discharges in the acute electrocorticogram. Implications for pathophysiology and surgical treatment of temporal lobe epilepsy. , 1997, Brain : a journal of neurology.

[44]  G Lantz,et al.  Space-oriented segmentation and 3-dimensional source reconstruction of ictal EEG patterns , 2001, Clinical Neurophysiology.

[45]  François Dubeau,et al.  Patients with Temporoparietal Ictal Symptoms and Inferomesial EEG Do Not Benefit from Anterior Temporal Resection , 2004, Epilepsia.

[46]  R M Leahy,et al.  A sensor-weighted overlapping-sphere head model and exhaustive head model comparison for MEG. , 1999, Physics in medicine and biology.

[47]  Richard M. Leahy,et al.  Brainstorm: A User-Friendly Application for MEG/EEG Analysis , 2011, Comput. Intell. Neurosci..

[48]  Localization of abnormal discharges causing insular epilepsy by magnetoencephalography. , 2012, The Tohoku journal of experimental medicine.

[49]  Sylvain Rheims,et al.  Functional connectivity of insular efferences , 2014, Human brain mapping.

[50]  C. Keysers,et al.  Probabilistic tractography recovers a rostrocaudal trajectory of connectivity variability in the human insular cortex , 2011, Human brain mapping.

[51]  P Kahane,et al.  Intracranial EEG and human brain mapping , 2003, Journal of Physiology-Paris.

[52]  A. Tucholka,et al.  The Corticocortical Structural Connectivity of the Human Insula , 2017, Cerebral cortex.

[53]  Lauren L. Cloutman,et al.  Connectivity-based structural and functional parcellation of the human cortex using diffusion imaging and tractography , 2012, Front. Neuroanat..