Neuroimaging of Epilepsy: Lesions, Networks, Oscillations

While analysis and interpretation of structural epileptogenic lesion is an essential task for the neuroradiologist in clinical practice, a substantial body of epilepsy research has shown that focal lesions influence brain areas beyond the epileptogenic lesion, across ensembles of functionally and anatomically connected brain areas. In this review article, we aim to provide an overview about altered network compositions in epilepsy, as measured with current advanced neuroimaging techniques to characterize the initiation and spread of epileptic activity in the brain with multimodal noninvasive imaging techniques. We focus on resting-state functional magnetic resonance imaging (MRI) and simultaneous electroencephalography/fMRI, and oppose the findings in idiopathic generalized versus focal epilepsies. These data indicate that circumscribed epileptogenic lesions can have extended effects on many brain systems. Although epileptic seizures may involve various brain areas, seizure activity does not spread diffusely throughout the brain but propagates along specific anatomic pathways that characterize the underlying epilepsy syndrome. Such a functionally oriented approach may help to better understand a range of clinical phenomena such as the type of cognitive impairment, the development of pharmacoresistance, the propagation pathways of seizures, or the success of epilepsy surgery.

[1]  D. Spencer,et al.  Refractory epilepsy: comparison of MR imaging, CT, and histopathologic findings in 117 patients. , 1996, Radiology.

[2]  M. Rushworth,et al.  Connectivity-based subdivisions of the human right "temporoparietal junction area": evidence for different areas participating in different cortical networks. , 2012, Cerebral cortex.

[3]  Marta I. Garrido,et al.  Dynamic Causal Modelling of epileptic seizure propagation pathways: A combined EEG–fMRI study , 2012, NeuroImage.

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

[5]  L Lemieux,et al.  Converging PET and fMRI evidence for a common area involved in human focal epilepsies , 2011, Neurology.

[6]  Josemir W Sander,et al.  The mortality of epilepsy revisited. , 2004, Epileptic disorders : international epilepsy journal with videotape.

[7]  Keith A. Johnson,et al.  Cortical Hubs Revealed by Intrinsic Functional Connectivity: Mapping, Assessment of Stability, and Relation to Alzheimer's Disease , 2009, The Journal of Neuroscience.

[8]  Jean Gotman,et al.  Widespread epileptic networks in focal epilepsies: EEG‐fMRI study , 2012, Epilepsia.

[9]  Terrence J. Sejnowski,et al.  Enhanced detection of artifacts in EEG data using higher-order statistics and independent component analysis , 2007, NeuroImage.

[10]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[11]  Louis Lemieux,et al.  EEG-fMRI; Physiological Basis, Technique, and Applications , 2010 .

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

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

[14]  H. Siebner,et al.  Simultaneous EEG‐fMRI in drug‐naive children with newly diagnosed absence epilepsy , 2008, Epilepsia.

[15]  Thomas Dierks,et al.  BOLD correlates of continuously fluctuating epileptic activity isolated by independent component analysis , 2008, NeuroImage.

[16]  René J. Huster,et al.  Methods for Simultaneous EEG-fMRI: An Introductory Review , 2012, The Journal of Neuroscience.

[17]  P. Griffiths,et al.  3.0 T MRI of 2000 consecutive patients with localisation-related epilepsy. , 2012, The British journal of radiology.

[18]  Marc Joliot,et al.  Brain activity at rest: a multiscale hierarchical functional organization. , 2011, Journal of neurophysiology.

[19]  F. H. Lopes da Silva,et al.  Evolving concepts on the pathophysiology of absence seizures: the cortical focus theory. , 2005, Archives of neurology.

[20]  Rao P. Gullapalli,et al.  Default mode network interference in mild traumatic brain injury – A pilot resting state study , 2013, Brain Research.

[21]  John M Stern,et al.  Connectomics and epilepsy. , 2013, Current opinion in neurology.

[22]  Neda Bernasconi,et al.  Surface-Based Texture and Morphological Analysis Detects Subtle Cortical Dysplasia , 2008, MICCAI.

[23]  Stephan Wolff,et al.  EEG-fMRI study of generalized spike and wave discharges without transitory cognitive impairment , 2010, Epilepsy & Behavior.

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

[25]  Cornelis J Stam,et al.  Graph theoretical analysis of complex networks in the brain , 2007, Nonlinear biomedical physics.

[26]  G. Edelman,et al.  A measure for brain complexity: relating functional segregation and integration in the nervous system. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[27]  V Latora,et al.  Efficient behavior of small-world networks. , 2001, Physical review letters.

[28]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[29]  Jean Gotman,et al.  Independent component analysis reveals dynamic ictal BOLD responses in EEG-fMRI data from focal epilepsy patients , 2010, NeuroImage.

[30]  M. V. D. Heuvel,et al.  Exploring the brain network: A review on resting-state fMRI functional connectivity , 2010, European Neuropsychopharmacology.

[31]  P Gloor,et al.  Generalized Cortico‐Reticular Epilepsies Some Considerations on the Pathophysiology of Generalized Bilaterally Synchronous Spike and Wave Discharge , 1968, Epilepsia.

[32]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[33]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[34]  Josemir W Sander,et al.  The somatic comorbidity of epilepsy: A weighty but often unrecognized burden , 2012, Epilepsia.

[35]  Scott Makeig,et al.  Information-based modeling of event-related brain dynamics. , 2006, Progress in brain research.

[36]  Kaspar Anton Schindler,et al.  Localizing Seizure-Onset Zones in Presurgical Evaluation of Drug-Resistant Epilepsy by Electroencephalography/fMRI: Effectiveness of Alternative Thresholding Strategies , 2012, American Journal of Neuroradiology.

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

[38]  Edward T. Bullmore,et al.  Whole-brain anatomical networks: Does the choice of nodes matter? , 2010, NeuroImage.

[39]  A. Villringer,et al.  Simultaneous EEG–fMRI , 2006, Neuroscience & Biobehavioral Reviews.

[40]  W. Cai,et al.  64Cu-Labeled tetrameric and octameric RGD peptides for microPET imaging of tumor {alpha}v{beta}3 integrin expression , 2007 .

[41]  Abraham Z. Snyder,et al.  A default mode of brain function: A brief history of an evolving idea , 2007, NeuroImage.

[42]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

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

[44]  S. Shorvon,et al.  Presurgical evaluation of patients with epilepsy and normal MRI: role of scalp video-EEG telemetry , 1999, Journal of neurology, neurosurgery, and psychiatry.

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

[46]  Asla Pitkänen,et al.  Epilepsy biomarkers , 2013, Epilepsia.

[47]  Christian E Elger,et al.  Morphometric MRI analysis improves detection of focal cortical dysplasia type II. , 2011, Brain : a journal of neurology.

[48]  Mark Richardson,et al.  Current themes in neuroimaging of epilepsy: Brain networks, dynamic phenomena, and clinical relevance , 2010, Clinical Neurophysiology.

[49]  Olaf Sporns,et al.  Network attributes for segregation and integration in the human brain , 2013, Current Opinion in Neurobiology.

[50]  Josemir W Sander,et al.  CPD — Education and self-assessment The epidemiology of epilepsy: the size of the problem , 2001, Seizure.

[51]  W. Cai,et al.  64Cu-Labeled Tetrameric and Octameric RGD Peptides for Small-Animal PET of Tumor αvβ3 Integrin Expression , 2007, Journal of Nuclear Medicine.

[52]  G. Holmes,et al.  Absence seizures in children: Clinical and electroencephalographic features , 1987, Annals of neurology.

[53]  Kaspar Anton Schindler,et al.  Brain areas involved in medial temporal lobe seizures: A principal component analysis of ictal SPECT data , 2006, Human brain mapping.

[54]  S. Sandrone,et al.  Learning from Default Mode Network: The Predictive Value of Resting State in Traumatic Brain Injury , 2012, The Journal of Neuroscience.

[55]  Karl J. Friston,et al.  Effective connectivity: Influence, causality and biophysical modeling , 2011, NeuroImage.

[56]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[57]  Timothy O. Laumann,et al.  Methods to detect, characterize, and remove motion artifact in resting state fMRI , 2014, NeuroImage.

[58]  Daniel K Sodickson,et al.  Default-mode network disruption in mild traumatic brain injury. , 2012, Radiology.

[59]  Josemir W Sander,et al.  The epidemiology of epilepsy: the size of the problem. , 2001, Seizure.

[60]  G. B. Pike,et al.  Texture analysis and morphological processing of magnetic resonance imaging assist detection of focal cortical dysplasia in extra‐temporal partial epilepsy , 2001, Annals of neurology.

[61]  B. Weir,et al.  The morphology of the spike-wave complex. , 1965, Electroencephalography and clinical neurophysiology.

[62]  J. Pekar,et al.  A method for making group inferences from functional MRI data using independent component analysis , 2001, Human brain mapping.

[63]  Hasan H. Sonmezturk,et al.  Cross hippocampal influence in mesial temporal lobe epilepsy measured with high temporal resolution functional magnetic resonance imaging , 2011, Epilepsia.

[64]  D. Gadian,et al.  Recommendations for Neuroimaging of Patients with Epilepsy , 1997, Epilepsia.

[65]  G. Cascino Temporal lobe epilepsy is a progressive neurologic disorder , 2009, Neurology.

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

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

[68]  C. Panayiotopoulos,et al.  Typical absence seizures in adults: clinical, EEG, video-EEG findings and diagnostic/syndromic considerations. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[69]  Abraham Z. Snyder,et al.  Steps toward optimizing motion artifact removal in functional connectivity MRI; a reply to Carp , 2013, NeuroImage.

[70]  M. Sperling,et al.  Functional connectivity evidence of cortico–cortico inhibition in temporal lobe epilepsy , 2014, Human brain mapping.

[71]  D. McCormick,et al.  Corticothalamic Inputs Control the Pattern of Activity Generated in Thalamocortical Networks , 2000, The Journal of Neuroscience.

[72]  N. Voets,et al.  Structural substrates for resting network disruption in temporal lobe epilepsy. , 2012, Brain : a journal of neurology.

[73]  Kaspar Anton Schindler,et al.  Uniform approach to linear and nonlinear interrelation patterns in multivariate time series. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[74]  J. Pekar,et al.  Different activation dynamics in multiple neural systems during simulated driving , 2002, Human brain mapping.

[75]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[76]  N. Roberts,et al.  Voxel‐based morphometry of temporal lobe epilepsy: An introduction and review of the literature , 2008, Epilepsia.

[77]  Boris C. Bernhardt,et al.  Mapping limbic network organization in temporal lobe epilepsy using morphometric correlations: Insights on the relation between mesiotemporal connectivity and cortical atrophy , 2008, NeuroImage.

[78]  J. Gotman,et al.  EEG-fMRI , 2009, Neurology.

[79]  Mark P Richardson,et al.  Large scale brain models of epilepsy: dynamics meets connectomics , 2012, Journal of Neurology, Neurosurgery & Psychiatry.

[80]  Beatriz Luna,et al.  The nuisance of nuisance regression: Spectral misspecification in a common approach to resting-state fMRI preprocessing reintroduces noise and obscures functional connectivity , 2013, NeuroImage.

[81]  J. H. Cross,et al.  Revised terminology and concepts for organization of seizures and epilepsies: Report of the ILAE Commission on Classification and Terminology, 2005–2009 , 2010, Epilepsia.

[82]  Alan Connelly,et al.  EEG‐fMRI in Children with Pharmacoresistant Focal Epilepsy , 2007, Epilepsia.

[83]  Karl J. Friston Functional and Effective Connectivity: A Review , 2011, Brain Connect..

[84]  M. Corbetta,et al.  Resting interhemispheric functional magnetic resonance imaging connectivity predicts performance after stroke , 2009, Annals of neurology.

[85]  Asla Pitkänen,et al.  Quantitative MRI volumetry of the entorhinal cortex in temporal lobe epilepsy , 2000, Seizure.

[86]  Kaspar Anton Schindler,et al.  Widespread grey matter changes and hemodynamic correlates to interictal epileptiform discharges in pharmacoresistant mesial temporal epilepsy , 2013, Journal of Neurology.

[87]  Neda Bernasconi,et al.  Graph-theoretical analysis reveals disrupted small-world organization of cortical thickness correlation networks in temporal lobe epilepsy. , 2011, Cerebral cortex.

[88]  Bruce Hermann,et al.  Ipsilateral and Contralateral MRI Volumetric Abnormalities in Chronic Unilateral Temporal Lobe Epilepsy and their Clinical Correlates , 2005, Epilepsia.

[89]  Robert Leech,et al.  Salience network integrity predicts default mode network function after traumatic brain injury , 2012, Proceedings of the National Academy of Sciences.

[90]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[91]  Mark Jenkinson,et al.  Optimizing RetroICor and RetroKCor corrections for multi-shot 3D FMRI acquisitions , 2014, NeuroImage.

[92]  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.

[93]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[94]  Karl J. Friston,et al.  Causal Hierarchy within the Thalamo-Cortical Network in Spike and Wave Discharges , 2009, PloS one.

[95]  Felix Rosenow,et al.  Invasive EEG studies in tumor‐related epilepsy: When are they indicated and with what kind of electrodes? , 2013, Epilepsia.

[96]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[97]  Francesca Benuzzi,et al.  Increased cortical BOLD signal anticipates generalized spike and wave discharges in adolescents and adults with idiopathic generalized epilepsies , 2012, Epilepsia.

[98]  Matthew N. DeSalvo,et al.  Dynamic Time Course of Typical Childhood Absence Seizures: EEG, Behavior, and Functional Magnetic Resonance Imaging , 2010, The Journal of Neuroscience.

[99]  J. Gotman,et al.  Absence seizures: Individual patterns revealed by EEG‐fMRI , 2010, Epilepsia.

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

[101]  Olaf Sporns,et al.  From simple graphs to the connectome: Networks in neuroimaging , 2012, NeuroImage.

[102]  R. Wiest,et al.  Time Course Based Artifact Identification for Independent Components of Resting-State fMRI , 2013, Front. Hum. Neurosci..

[103]  C Baumgartner,et al.  Network atrophy in temporal lobe epilepsy , 2008, Neurology.

[104]  David F Abbott,et al.  Absence epilepsy subnetworks revealed by event‐related independent components analysis of functional magnetic resonance imaging , 2013, Epilepsia.

[105]  E. So,et al.  The Cost of Epilepsy in the United States: An Estimate from Population‐Based Clinical and Survey Data , 2000, Epilepsia.

[106]  Godfrey D Pearlson,et al.  Disruptions in functional network connectivity during alcohol intoxicated driving. , 2010, Alcoholism, clinical and experimental research.

[107]  Y. Sheline,et al.  Psychiatric comorbidity, health, and function in epilepsy , 2003, Epilepsy & Behavior.

[108]  Vince D. Calhoun,et al.  A review of group ICA for fMRI data and ICA for joint inference of imaging, genetic, and ERP data , 2009, NeuroImage.