Characterization of atypical language activation patterns in focal epilepsy
Madison M. Berl PhD
Pediatric Imaging and Tissue Sciences Section on Tissue Biophysics and Biomimetics, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD
Center for Neuroscience Research, Children's National Medical Center, George Washington University, Washington, DC
Search for more papers by this authorLauren A. Zimmaro BA
Center for Neuroscience Research, Children's National Medical Center, George Washington University, Washington, DC
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorOmar I. Khan MD
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorIrene Dustin CNP
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorEva Ritzl MD
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Department of Neurology, Johns Hopkins Hospital, Baltimore, MD
Search for more papers by this authorElizabeth S. Duke BS
Center for Neuroscience Research, Children's National Medical Center, George Washington University, Washington, DC
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorLeigh N. Sepeta PhD
Center for Neuroscience Research, Children's National Medical Center, George Washington University, Washington, DC
Search for more papers by this authorSusumu Sato MD
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorCorresponding Author
William H. Theodore MD
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Address correspondence to Dr Theodore, Clinical Epilepsy Section, NINDS, Building 10, Room 7D-43, 10 Center Drive, MSC 1408, Bethesda, MD 20892-1408. E-mail: [email protected]Search for more papers by this authorWilliam D. Gaillard MD
Center for Neuroscience Research, Children's National Medical Center, George Washington University, Washington, DC
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorMadison M. Berl PhD
Pediatric Imaging and Tissue Sciences Section on Tissue Biophysics and Biomimetics, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD
Center for Neuroscience Research, Children's National Medical Center, George Washington University, Washington, DC
Search for more papers by this authorLauren A. Zimmaro BA
Center for Neuroscience Research, Children's National Medical Center, George Washington University, Washington, DC
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorOmar I. Khan MD
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorIrene Dustin CNP
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorEva Ritzl MD
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Department of Neurology, Johns Hopkins Hospital, Baltimore, MD
Search for more papers by this authorElizabeth S. Duke BS
Center for Neuroscience Research, Children's National Medical Center, George Washington University, Washington, DC
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorLeigh N. Sepeta PhD
Center for Neuroscience Research, Children's National Medical Center, George Washington University, Washington, DC
Search for more papers by this authorSusumu Sato MD
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorCorresponding Author
William H. Theodore MD
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Address correspondence to Dr Theodore, Clinical Epilepsy Section, NINDS, Building 10, Room 7D-43, 10 Center Drive, MSC 1408, Bethesda, MD 20892-1408. E-mail: [email protected]Search for more papers by this authorWilliam D. Gaillard MD
Center for Neuroscience Research, Children's National Medical Center, George Washington University, Washington, DC
Clinical Epilepsy Section, National Institutes of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD
Search for more papers by this authorAbstract
Objective
Functional magnetic resonance imaging is sensitive to the variation in language network patterns. Large populations are needed to rigorously assess atypical patterns, which, even in neurological populations, are a minority.
Methods
We studied 220 patients with focal epilepsy and 118 healthy volunteers who performed an auditory description decision task. We compared a data-driven hierarchical clustering approach to the commonly used a priori laterality index (LI) threshold (LI < 0.20 as atypical) to classify language patterns within frontal and temporal regions of interest. We explored (n = 128) whether IQ varied with different language activation patterns.
Results
The rate of atypical language among healthy volunteers (2.5%) and patients (24.5%) agreed with previous studies; however, we found 6 patterns of atypical language: a symmetrically bilateral, 2 unilaterally crossed, and 3 right dominant patterns. There was high agreement between classification methods, yet the cluster analysis revealed novel correlations with clinical features. Beyond the established association of left-handedness, early seizure onset, and vascular pathology with atypical language, cluster analysis identified an association of handedness with frontal lateralization, early seizure onset with temporal lateralization, and left hemisphere focus with a unilateral right pattern. Intelligence quotient was not significantly different among patterns.
Interpretation
Language dominance is a continuum; however, our results demonstrate meaningful thresholds in classifying laterality. Atypical language patterns are less frequent but more variable than typical language patterns, posing challenges for accurate presurgical planning. Language dominance should be assessed on a regional rather than hemispheric basis, and clinical characteristics should inform evaluation of atypical language dominance. Reorganization of language is not uniformly detrimental to language functioning. ANN NEUROL 2014;75:33–42
Supporting Information
Additional supporting information can be found in the online version of this article.
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