Whole-brain MRI phenotyping in dysplasia-related frontal lobe epilepsy

Objective: To perform whole-brain morphometry in patients with frontal lobe epilepsy and evaluate the utility of group-level patterns for individualized diagnosis and prognosis. Methods: We compared MRI-based cortical thickness and folding complexity between 2 frontal lobe epilepsy cohorts with histologically verified focal cortical dysplasia (FCD) (13 type I; 28 type II) and 41 closely matched controls. Pattern learning algorithms evaluated the utility of group-level findings to predict histologic FCD subtype, the side of the seizure focus, and postsurgical seizure outcome in single individuals. Results: Relative to controls, FCD type I displayed multilobar cortical thinning that was most marked in ipsilateral frontal cortices. Conversely, type II showed thickening in temporal and postcentral cortices. Cortical folding also diverged, with increased complexity in prefrontal cortices in type I and decreases in type II. Group-level findings successfully guided automated FCD subtype classification (type I: 100%; type II: 96%), seizure focus lateralization (type I: 92%; type II: 86%), and outcome prediction (type I: 92%; type II: 82%). Conclusion: FCD subtypes relate to diverse whole-brain structural phenotypes. While cortical thickening in type II may indicate delayed pruning, a thin cortex in type I likely results from combined effects of seizure excitotoxicity and the primary malformation. Group-level patterns have a high translational value in guiding individualized diagnostics.

[1]  D. V. van Essen,et al.  Mapping Human Cortical Areas In Vivo Based on Myelin Content as Revealed by T1- and T2-Weighted MRI , 2011, The Journal of Neuroscience.

[2]  Itzhak Fried,et al.  Assessment and surgical outcomes for mild type I and severe type II cortical dysplasia: A critical review and the UCLA experience , 2009, Epilepsia.

[3]  Li Min Li,et al.  Voxel‐based Morphometry Reveals Excess Gray Matter Concentration in Patients with Focal Cortical Dysplasia , 2006, Epilepsia.

[4]  Maria Thom,et al.  Focal cortical dysplasia type II: biological features and clinical perspectives , 2009, The Lancet Neurology.

[5]  Seokjun Hong,et al.  Magnetic resonance imaging pattern learning in temporal lobe epilepsy: Classification and prognostics , 2015, Annals of neurology.

[6]  Seokjun Hong,et al.  Imaging structural and functional brain networks in temporal lobe epilepsy , 2013, Front. Hum. Neurosci..

[7]  A. Bleasel,et al.  Clinical, EEG, and quantitative MRI differences in pediatric frontal and temporal lobe epilepsy , 2002, Neurology.

[8]  Maria Thom,et al.  Multi-focal occurrence of cortical dysplasia in epilepsy patients. , 2009, Brain : a journal of neurology.

[9]  Pavel Krsek,et al.  Diagnostic methods and treatment options for focal cortical dysplasia , 2015, Epilepsia.

[10]  John G. Parnavelas,et al.  Modes of neuronal migration in the developing cerebral cortex , 2002, Nature Reviews Neuroscience.

[11]  Alan C. Evans,et al.  Automated 3-D extraction and evaluation of the inner and outer cortical surfaces using a Laplacian map and partial volume effect classification , 2005, NeuroImage.

[12]  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.

[13]  Andrea Bernasconi,et al.  Small focal cortical dysplasia lesions are located at the bottom of a deep sulcus. , 2008, Brain : a journal of neurology.

[14]  Li Min Li,et al.  Gray matter atrophy associated with duration of temporal lobe epilepsy , 2006, NeuroImage.

[15]  Neda Bernasconi,et al.  Cortical thickness analysis in temporal lobe epilepsy , 2010, Neurology.

[16]  H. Vinters,et al.  Incomplete resection of focal cortical dysplasia is the main predictor of poor postsurgical outcome , 2009, Neurology.

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

[18]  Alan C. Evans,et al.  Brain size and cortical structure in the adult human brain. , 2008, Cerebral cortex.

[19]  Patric Hagmann,et al.  Mapping the human connectome at multiple scales with diffusion spectrum MRI , 2012, Journal of Neuroscience Methods.

[20]  Gustavo Rey,et al.  Different features of histopathological subtypes of pediatric focal cortical dysplasia , 2008, Annals of neurology.

[21]  B. Peterson,et al.  Normal Development of Brain Circuits , 2010, Neuropsychopharmacology.

[22]  M. Koepp,et al.  PET: central benzodiazepine neuroreceptor mapping in localization-related epilepsies. , 2000, Advances in neurology.

[23]  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.

[24]  R. Kuzniecky,et al.  A developmental and genetic classification for malformations of cortical development: update 2012 , 2012, Brain : a journal of neurology.

[25]  Neda Bernasconi,et al.  Automated detection of cortical dysplasia type II in MRI-negative epilepsy , 2014, Neurology.

[26]  N. Voets,et al.  Increased temporolimbic cortical folding complexity in temporal lobe epilepsy , 2010, Neurology.

[27]  Hal Blumenfeld,et al.  From Molecules to Networks: Cortical/Subcortical Interactions in the Pathophysiology of Idiopathic Generalized Epilepsy , 2003, Epilepsia.

[28]  Luiz Eduardo Betting,et al.  White Matter Abnormalities in Patients with Focal Cortical Dysplasia Revealed by Diffusion Tensor Imaging Analysis in a Voxelwise Approach , 2012, Front. Neur..

[29]  S. Sathiya Keerthi,et al.  Which Is the Best Multiclass SVM Method? An Empirical Study , 2005, Multiple Classifier Systems.

[30]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Steven Robbins,et al.  An unbiased iterative group registration template for cortical surface analysis , 2007, NeuroImage.

[32]  Maria Thom,et al.  The clinicopathologic spectrum of focal cortical dysplasias: A consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission 1 , 2011, Epilepsia.

[33]  O. Marín,et al.  Cell migration in the forebrain. , 2003, Annual review of neuroscience.

[34]  KJ Worsley,et al.  SurfStat: A Matlab toolbox for the statistical analysis of univariate and multivariate surface and volumetric data using linear mixed effects models and random field theory , 2009, NeuroImage.

[35]  J. Lerch,et al.  Patterns of Coordinated Anatomical Change in Human Cortical Development: A Longitudinal Neuroimaging Study of Maturational Coupling , 2011, Neuron.

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

[37]  Pablo M. Casillas-Espinosa,et al.  Regulators of synaptic transmission: Roles in the pathogenesis and treatment of epilepsy , 2012, Epilepsia.

[38]  I. Blümcke,et al.  Neuropathologic measurements in focal cortical dysplasias: validation of the ILAE 2011 classification system and diagnostic implications for MRI , 2012, Acta Neuropathologica.

[39]  Boris C. Bernhardt,et al.  Thalamo–cortical network pathology in idiopathic generalized epilepsy: Insights from MRI-based morphometric correlation analysis , 2009, NeuroImage.

[40]  Alan C. Evans,et al.  Detecting changes in nonisotropic images , 1999, Human brain mapping.

[41]  Alan C. Evans,et al.  Longitudinal and cross-sectional analysis of atrophy in pharmacoresistant temporal lobe epilepsy , 2009, Neurology.