Limitations to plasticity of language network reorganization in localization related epilepsy.

Neural networks for processing language often are reorganized in patients with epilepsy. However, the extent and location of within and between hemisphere re-organization are not established. We studied 45 patients, all with a left hemisphere seizure focus (mean age 22.8, seizure onset 13.3), and 19 normal controls (mean age 24.8) with an fMRI word definition language paradigm to assess the location of language processing regions. Individual patient SPM maps were compared to the normal group in a voxel-wise comparison; a voxel was considered to be significant if its z-value exceeded mid R:2mid R:. Subsequently, we used principal component analysis with hierarchical clustering of variance patterns from individual difference maps to identify four patient sub-groups. One did not differ from normal controls; one had increased left temporal activation on the margin of regions activated in controls; two others had recruitment in right inferior frontal gyrus, middle frontal gyrus and temporal cortex. Right hemisphere activation in these two groups occurred in homologues of left hemisphere regions that sustained task activation. Our study used novel data driven methods to find evidence for constraints on inter-hemispheric reorganization of language in recruitment of right homologues, and, in a subpopulation of patients, evidence for intra-hemispheric reorganization of language limited to the margins of typical left temporal regional activation. These methods may be applied to investigate both normal and pathological variance in other developmental disorders and cognitive domains.

[1]  D. Le Bihan,et al.  Noninvasive assessment of language dominance in children and adolescents with functional MRI , 1997, Neurology.

[2]  Dong Soo Lee,et al.  Differential features of metabolic abnormalities between medial and lateral temporal lobe epilepsy: quantitative analysis of (18)F-FDG PET using SPM. , 2003, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[3]  K P George,et al.  Cortical language activation in stroke patients recovering from aphasia with functional MRI. , 1999, Stroke.

[4]  J. A. Frost,et al.  Determination of language dominance using functional MRI: A comparison with the Wada test , 2011, Neurology.

[5]  Christine Delmaire,et al.  Productive and perceptive language reorganization in temporal lobe epilepsy , 2005, NeuroImage.

[6]  Siddheswar Ray,et al.  Determination of Number of Clusters in K-Means Clustering and Application in Colour Image Segmentation , 2000 .

[7]  Guillén Fernández,et al.  Language Mapping in Less Than 15 Minutes: Real-Time Functional MRI during Routine Clinical Investigation , 2001, NeuroImage.

[8]  Chandan J. Vaidya,et al.  Functional imaging of developmental and adaptive changes in neurocognition , 2006, NeuroImage.

[9]  J. E Adcock,et al.  Quantitative fMRI assessment of the differences in lateralization of language-related brain activation in patients with temporal lobe epilepsy , 2003, NeuroImage.

[10]  Margaret S. McGill,et al.  Subject Index Vol. 57, Suppl. 1, 2001 , 2004, Hormone Research in Paediatrics.

[11]  J. Petrella,et al.  Cortical localization of reading in normal children: An fMRI language study , 2001 .

[12]  B Milner,et al.  THE ROLE OF EARLY LEFT‐BRAIN INJURY IN DETERMINING LATERALIZATION OF CEREBRAL SPEECH FUNCTIONS , 1977, Annals of the New York Academy of Sciences.

[13]  E. T. Possing,et al.  Language lateralization in left-handed and ambidextrous people: fMRI data , 2002, Neurology.

[14]  W H Theodore,et al.  Seizure focus affects regional language networks assessed by fMRI , 2005, Neurology.

[15]  Mitchel S Berger,et al.  Functional outcome after language mapping for glioma resection. , 2008, The New England journal of medicine.

[16]  D. Hinkley Annals of Statistics , 2006 .

[17]  G J Barker,et al.  Magnetization transfer imaging in focal epilepsy , 2003, Neurology.

[18]  G McCarthy,et al.  Comparative localization of auditory comprehension by using functional magnetic resonance imaging and cortical stimulation. , 1999, Journal of neurosurgery.

[19]  J. Pujol,et al.  Cerebral lateralization of language in normal left-handed people studied by functional MRI , 1999, Neurology.

[20]  V. Schmithorst,et al.  Normal fMRI Brain Activation Patterns in Children Performing a Verb Generation Task , 2001, NeuroImage.

[21]  M Erb,et al.  Early left periventricular brain lesions induce right hemispheric organization of speech , 2001, Neurology.

[22]  R J Wise,et al.  Separate neural subsystems within 'Wernicke's area'. , 2001, Brain : a journal of neurology.

[23]  R W Cox,et al.  Language processing is strongly left lateralized in both sexes. Evidence from functional MRI. , 1999, Brain : a journal of neurology.

[24]  Orrin Devinsky,et al.  Evidence for cortical reorganization of language in patients with hippocampal sclerosis. , 2007, Brain : a journal of neurology.

[25]  J. Winn,et al.  Brain , 1878, The Lancet.

[26]  K. Nolte Management of stroke : a practical guide for the prevention , evaluation and treatment of acute stroke , 2022 .

[27]  C. Elger,et al.  Shift-back of right into left hemisphere language dominance after control of epileptic seizures: Evidence for epilepsy driven functional cerebral organization , 2006, Epilepsy Research.

[28]  R. Goodman,et al.  Distribution of Auditory and Visual Naming Sites in Nonlesional Temporal Lobe Epilepsy Patients and Patients with Space‐Occupying Temporal Lobe Lesions , 2007, Epilepsia.

[29]  F Andermann,et al.  Entorhinal cortex atrophy in epilepsy patients exhibiting normal hippocampal volumes , 2001, Neurology.

[30]  S. Bookheimer,et al.  Regional cerebral blood flow during object naming and word reading , 1995 .

[31]  S. Sato,et al.  Language dominance in partial epilepsy patients identified with an fMRI reading task , 2002, Neurology.

[32]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

[33]  Dong Soo Lee,et al.  (18)F-FDG PET in localization of frontal lobe epilepsy: comparison of visual and SPM analysis. , 2002, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[34]  D J Mikulis,et al.  Functional MRI of phonological and semantic processing in temporal lobe epilepsy. , 2001, Brain : a journal of neurology.

[35]  M. Just,et al.  Brain Activation Modulated by Sentence Comprehension , 1996, Science.

[36]  G. Jackson,et al.  A Neurocognitive Account of Frontal Lobe Involvement in Orthographic Lexical Retrieval: An fMRI Study , 2001, NeuroImage.

[37]  W H Theodore,et al.  Cortical Stimulation Elicits Regional Distinctions in Auditory and Visual Naming , 1996, Epilepsia.

[38]  Steven E Petersen,et al.  fMRI reveals novel functional neuroanatomy in a child with perinatal stroke , 2006, Neurology.

[39]  S. Sato,et al.  fMRI language task panel improves determination of language dominance , 2004, Neurology.

[40]  E. Courchesne,et al.  Abnormal variability and distribution of functional maps in autism: an FMRI study of visuomotor learning. , 2003, The American journal of psychiatry.

[41]  L. Katz,et al.  Sex differences in the functional organization of the brain for language , 1995, Nature.

[42]  C. DeCarli,et al.  Use of positron emission tomography for the evaluation of epilepsy. , 1995, Neuroimaging clinics of North America.

[43]  O. Devinsky,et al.  Anterior temporal language areas in patients with early onset of temporal lobe epilepsy , 1993, Annals of neurology.

[44]  Kenneth Perrine,et al.  Brain stimulation reveals critical auditory naming cortex. , 2005, Brain : a journal of neurology.

[45]  Wolfgang Grodd,et al.  Right-Hemispheric Organization of Language Following Early Left-Sided Brain Lesions: Functional MRI Topography , 2002, NeuroImage.

[46]  J. A. Frost,et al.  Language dominance in neurologically normal and epilepsy subjects , 1999 .

[47]  Karl J. Friston,et al.  Design and analysis of fMRI studies with neurologically impaired patients , 2006, Journal of magnetic resonance imaging : JMRI.

[48]  I. Janszky,et al.  Left‐sided Interictal Epileptic Activity Induces Shift of Language Lateralization in Temporal Lobe Epilepsy: An fMRI Study , 2006, Epilepsia.

[49]  M. Symms,et al.  Diffusion tensor imaging in patients with epilepsy and malformations of cortical development. , 2001, Brain : a journal of neurology.

[50]  F. Woermann,et al.  Language lateralization by Wada test and fMRI in 100 patients with epilepsy , 2003, Neurology.

[51]  D Le Bihan,et al.  Functional MR evaluation of temporal and frontal language dominance compared with the Wada test , 2000, Neurology.

[52]  J. A. López del Val,et al.  Principal Components Analysis , 2018, Applied Univariate, Bivariate, and Multivariate Statistics Using Python.

[53]  D. LeBihan,et al.  Functional anatomy of cognitive development , 2000, Neurology.

[54]  G. Ojemann,et al.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. , 1989, Journal of neurosurgery.

[55]  H. Karbe,et al.  Differential capacity of left and right hemispheric areas for compensation of poststroke aphasia , 1999, Annals of neurology.

[56]  Timothy Edward John Behrens,et al.  Distinct right frontal lobe activation in language processing following left hemisphere injury. , 2006, Brain : a journal of neurology.

[57]  K. Thomas,et al.  MR quantitation of volume and diffusion changes in the developing brain. , 2005, AJNR. American journal of neuroradiology.

[58]  Robert Minahan,et al.  Language recovery after left hemispherectomy in children with late‐onset seizures , 1999, Annals of neurology.

[59]  Elizabeth Bates,et al.  LANGUAGE DEVELOPMENT IN CHILDREN WITH UNILATERAL BRAIN INJURY , 2000 .

[60]  Scott K. Holland,et al.  Sex differences in the activation of language cortex during childhood , 2006, Neuropsychologia.

[61]  A. Thiel,et al.  Direct Demonstration of Transcallosal Disinhibition in Language Networks , 2006, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[62]  Sharlene D. Newman,et al.  Imagery in sentence comprehension: an fMRI study , 2004, NeuroImage.

[63]  J. Xiong,et al.  Intersubject Variability in Cortical Activations during a Complex Language Task , 2000, NeuroImage.

[64]  C. Nelson,et al.  Handbook of Developmental Cognitive Neuroscience , 2001 .

[65]  Marko Wilke,et al.  LI-tool: A new toolbox to assess lateralization in functional MR-data , 2007, Journal of Neuroscience Methods.

[66]  J C Mazziotta,et al.  The functional anatomy of frontal lobe epilepsy studied with PET. , 1992, Advances in neurology.

[67]  W H Theodore,et al.  Antiepileptic Drugs and Cerebral Glucose Metabolism , 1988, Epilepsia.

[68]  G J Barker,et al.  Diffusion tensor imaging of cryptogenic and acquired partial epilepsies. , 2001, Brain : a journal of neurology.

[69]  Nader Pouratian,et al.  Utility of preoperative functional magnetic resonance imaging for identifying language cortices in patients with vascular malformations. , 2002, Journal of neurosurgery.

[70]  N. F. Ramsey,et al.  Combined Analysis of Language Tasks in fMRI Improves Assessment of Hemispheric Dominance for Language Functions in Individual Subjects , 2001, NeuroImage.

[71]  G. Raboyeau,et al.  Right hemisphere activation in recovery from aphasia , 2008, Neurology.

[72]  Asaid Khateb,et al.  Group analysis and the subject factor in functional magnetic resonance imaging: Analysis of fifty right‐handed healthy subjects in a semantic language task , 2008, Human brain mapping.

[73]  A Jesmanowicz,et al.  Lateralized human brain language systems demonstrated by task subtraction functional magnetic resonance imaging. , 1995, Archives of neurology.

[74]  S. Bookheimer Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. , 2002, Annual review of neuroscience.

[75]  W H Theodore,et al.  A direct comparison of PET activation and electrocortical stimulation mapping for language localization , 1997, Neurology.

[76]  Tai-Li Chou,et al.  Developmental and skill effects on the neural correlates of semantic processing to visually presented words , 2006, Human brain mapping.

[77]  James R. Booth,et al.  Developmental changes in the neural correlates of semantic processing , 2006, NeuroImage.

[78]  J. S. Duncan,et al.  A Longitudinal Quantitative MRI Study of Community-Based Patients with Chronic Epilepsy and Newly Diagnosed Seizures: Methodology and Preliminary Findings , 2001, NeuroImage.

[79]  Thomas Elbert,et al.  Functional re-recruitment of dysfunctional brain areas predicts language recovery in chronic aphasia , 2008, NeuroImage.

[80]  Guillén Fernández,et al.  Left hippocampal pathology is associated with atypical language lateralization in patients with focal epilepsy. , 2006, Brain : a journal of neurology.

[81]  Colin Humphries,et al.  Time course of semantic processes during sentence comprehension: An fMRI study , 2007, NeuroImage.

[82]  Iraj Derakhshan,et al.  ATYPICAL LANGUAGE IN LESIONAL AND NONLESIONAL COMPLEX PARTIAL EPILEPSY , 2008, Neurology.

[83]  D. Arnold,et al.  Mesial temporal damage in temporal lobe epilepsy: a volumetric MRI study of the hippocampus, amygdala and parahippocampal region. , 2003, Brain : a journal of neurology.

[84]  V. Haughton,et al.  Functional MR of frontal lobe activation: comparison with Wada language results. , 1998, AJNR. American journal of neuroradiology.

[85]  C. Weiller,et al.  Dynamics of language reorganization after stroke. , 2006, Brain : a journal of neurology.

[86]  G. Eden,et al.  The Neural Basis of Hyperlexic Reading An fMRI Case Study , 2004, Neuron.

[87]  R T Constable,et al.  Functional MRI of Language Processing: Dependence on Input Modality and Temporal Lobe Epilepsy , 2001, Epilepsia.