Atypical language in lesional and nonlesional complex partial epilepsy

Objective: We investigated the relationship between partial epilepsy, MRI findings, and atypical language representation. Methods: A total of 102 patients (4 to 55 years) with left hemisphere epileptogenic zones were evaluated using three fMRI language tasks obtained at 1.5 or 3T with EPI BOLD techniques: verbal fluency, reading comprehension, and auditory comprehension. fMRI maps were visually interpreted at a standard threshold and rated as left or atypical language. Results: Atypical language dominance occurred in 30 patients (29%) and varied with MRI type (p < 0.01). Atypical language representation occurred in 36% (13/36) with normal MRI, 21% (6/29) with mesial temporal sclerosis, 14% (4/28) with focal cortical lesions (dysplasia, tumor, vascular malformation), and all (6/6) with a history of stroke. Multivariate logistic regression analysis found handedness, seizure onset, and MRI type accounted for much of the variance in language activation patterns (χ2 = 24.09, p < 0.01). Atypical language was more prevalent in patients with early seizure onset (43.2%, p < 0.05) and atypical handedness (60%, p < 0.01). None of the three clinical factors were correlated with each other (p > 0.40). Patients with atypical language had lower verbal abilities (F = 6.96, p = 0.01) and a trend toward lower nonverbal abilities (F = 3.58, p = 0.06). There were no differences in rates of atypical language across time, age groups, or MRI scanner. Conclusion: Early seizure onset and atypical handedness, as well as the location and nature of pathologic substrate, are important factors in language reorganization. GLOSSARY: FOV = field of view; MTS = mesial temporal sclerosis; RRN = read response naming; TE = echo time; TR = repetition time; WAIS = Wechsler Adult Intelligence Scale; WISC = Wechsler Intelligence Scale for Children.

[1]  Eugen Trinka,et al.  Language Lateralization in Temporal Lobe Epilepsy: A Comparison between fMRI and the Wada Test , 2006, Epilepsia.

[2]  William D Gaillard,et al.  A functional magnetic resonance imaging study of left hemisphere language dominance in children. , 2002, Archives of neurology.

[3]  S. Dehaene,et al.  Anatomical variability in the cortical representation of first and second language , 1997, Neuroreport.

[4]  A. Wagner,et al.  Prefrontal and hippocampal contributions to visual associative recognition: Interactions between cognitive control and episodic retrieval , 2004, Brain and Cognition.

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

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

[7]  A. Duhaime,et al.  Recovery of Language after Left Hemispherectomy in a Sixteen-Year-Old Girl with Late-Onset Seizures , 2002, Pediatric Neurosurgery.

[8]  D. Caplan,et al.  Processing of Visually Presented Sentences in Mandarin and English Studied with fMRI , 1999, Neuron.

[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]  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.

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

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

[14]  D. Francis,et al.  Longitudinal neuropsychological outcome in infants and preschoolers with traumatic brain injury , 1997, Journal of the International Neuropsychological Society.

[15]  D. Thal,et al.  Language and gesture in late talkers: a 1-year follow-up. , 1991, Journal of speech and hearing research.

[16]  Angelo Labate,et al.  Is Language Lateralization in Temporal Lobe Epilepsy Patients Related to the Nature of the Epileptogenic Lesion? , 2006, Epilepsia.

[17]  D. Gadian,et al.  Language reorganization in children with early-onset lesions of the left hemisphere: an fMRI study. , 2004, Brain : a journal of neurology.

[18]  Aesop.  The Aesop for Children , 1928 .

[19]  J B Poline,et al.  Episodic memory in left temporal lobe epilepsy: a functional MRI study. , 2000, Brain : a journal of neurology.

[20]  Kristina M. Visscher,et al.  Functional Neuroanatomical Differences Between Adults and School-Age Children in the Processing of Single Words , 2002, Science.

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

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

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

[24]  James R. Booth,et al.  Functional organization of activation patterns in children: Whole brain fMRI imaging during three different cognitive tasks , 1999, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[25]  Functional MRI Study of Verbal Fluency in a Patient with Subcortical Laminar Heterotopia , 2004, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[26]  W D Gaillard,et al.  fMRI identifies regional specialization of neural networks for reading in young children , 2003, Neurology.

[27]  G. Vingerhoets.  Cognitive effects of seizures , 2006, Seizure.

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

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

[30]  M. Salih,et al.  Outcome of stroke in Saudi children. , 2006, Saudi medical journal.

[31]  Stéphane Lehéricy,et al.  Arteriovenous brain malformations: is functional MR imaging reliable for studying language reorganization in patients? Initial observations. , 2002, Radiology.

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

[33]  Byron Bernal,et al.  False lateralization of language cortex on functional MRI after a cluster of focal seizures. , 2002, Neurology.

[34]  L.M. Balsamo,et al.  Language lateralization and the role of the fusiform gyrus in semantic processing in young children , 2006, NeuroImage.

[35]  J. Gotman,et al.  Temporal and Extratemporal BOLD Responses to Temporal Lobe Interictal Spikes , 2006, Epilepsia.

[36]  Byron Bernal,et al.  Seizure disorders: functional MR imaging for diagnostic evaluation and surgical treatment--prospective study. , 2005, Radiology.

[37]  M. Mishkin,et al.  Onset of speech after left hemispherectomy in a nine-year-old boy. , 1997, Brain : a journal of neurology.

[38]  R. Mattson,et al.  Selective memory improvement and impairment in temporal lobectomy for epilepsy , 1984, Annals of neurology.

[39]  F. Vargha-Khadem,et al.  Clinical outcomes of hemispherectomy for epilepsy in childhood and adolescence. , 2003, Brain : a journal of neurology.

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

[41]  William Davis Gaillard,et al.  Functional MR imaging of language, memory, and sensorimotor cortex. , 2004, Neuroimaging clinics of North America.

[42]  B. MacWhinney,et al.  Developmental and Lesion Effects in Brain Activation During Sentence Comprehension and Mental Rotation , 2000, Developmental neuropsychology.

[43]  J. Kassubek,et al.  Determination of hemisphere dominance for language: comparison of frontal and temporal fMRI activation with intracarotid amytal testing , 2002, Neuroradiology.

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

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

[46]  J. Jameson,et al.  SF1 in the Development of the Adrenal Gland and Gonads , 2003, Hormone Research in Paediatrics.

[47]  G. Jackson,et al.  fMRI Lateralization of Expressive Language in Children with Cerebral Lesions , 2006, Epilepsia.

[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]  Dorothy M. Aram,et al.  Intellectual stability in children with unilateral brain lesions , 1994, Neuropsychologia.

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

[53]  D. Spencer,et al.  Characteristics of medial temporal lobe epilepsy: I. Results of history and physical examination , 1993, Annals of neurology.

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

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

[56]  J. Petrella,et al.  Developmental aspects of language processing: fMRI of verbal fluency in children and adults , 2003, Human brain mapping.

[57]  G. Hynd,et al.  The Role of the Corpus Callosum in Interhemispheric Transfer of Information: Excitation or Inhibition? , 2005, Neuropsychology Review.

[58]  P. G. Larsson,et al.  3T phased array MRI improves the presurgical evaluation in focal epilepsies , 2005, Neurology.

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

[60]  W. Gaillard,et al.  Auditory comprehension of language in young children , 2003, Neurology.

[61]  John B. Dillon.  Left Handedness , 1914, Science.

[62]  H. Whitaker,et al.  Verbal and cognitive sequelae following unilateral lesions acquired in early childhood. , 1985, Journal of clinical and experimental neuropsychology.

[63]  B. Levin,et al.  Language cortex representation: Effects of developmental versus acquired pathology , 1996, Annals of neurology.

[64]  F. Vargha-Khadem,et al.  Development of language in six hemispherectomized patients. , 1991, Brain : a journal of neurology.

[65]  J. Petrella,et al.  Cortical localization of reading in normal children , 2001, Neurology.

[66]  Stefan Knecht,et al.  Does language lateralization depend on the hippocampus? , 2004, Brain : a journal of neurology.

[67]  Friedrich G Woermann,et al.  Functional organization of the brain with malformations of cortical development , 2003, Annals of neurology.

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

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

[70]  S Sarkari,et al.  Reorganization of language-specific cortex in patients with lesions or mesial temporal epilepsy , 2004, Neurology.

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

[72]  René Westerhausen,et al.  The association of macro- and microstructure of the corpus callosum and language lateralisation , 2006, Brain and Language.

[73]  Lucie Hertz-Pannier,et al.  Late plasticity for language in a child's non-dominant hemisphere: a pre- and post-surgery fMRI study. , 2002, Brain : a journal of neurology.

[74]  E. Bates,et al.  EARLY COGNITION, COMMUNICATION AND LANGUAGE IN CHILDREN WITH FOCAL BRAIN INJURY , 1994, Developmental medicine and child neurology.

[75]  G. McCarthy,et al.  Human Brain Mapping 6:1–13(1998) � Functional MRI Studies of Auditory Comprehension , 2022 .

[76]  F. Woermann,et al.  Epileptic activity influences the speech organization in medial temporal lobe epilepsy. , 2003, Brain : a journal of neurology.