Identifying the neural basis of a language‐impaired phenotype of temporal lobe epilepsy
Objective To identify neuroimaging and clinical biomarkers associated with a language‐impaired phenotype in refractory temporal lobe epilepsy (TLE). Methods Eighty‐five patients with TLE were characterized as language‐impaired (TLE‐LI) or non–language‐impaired (TLE‐NLI) based on comprehensive neurop...
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| Published in | Epilepsia (Copenhagen) Vol. 60; no. 8; pp. 1627 - 1638 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Wiley Subscription Services, Inc
01.08.2019
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| Online Access | Get full text |
| ISSN | 0013-9580 1528-1167 1528-1167 |
| DOI | 10.1111/epi.16283 |
Cover
| Abstract | Objective
To identify neuroimaging and clinical biomarkers associated with a language‐impaired phenotype in refractory temporal lobe epilepsy (TLE).
Methods
Eighty‐five patients with TLE were characterized as language‐impaired (TLE‐LI) or non–language‐impaired (TLE‐NLI) based on comprehensive neuropsychological testing. Structural magnetic resonance imaging (MRI), diffusion tensor imaging, and functional MRI (fMRI) were obtained in patients and 47 healthy controls (HC). fMRI activations and cortical thickness were calculated within language regions of interest, and fractional anisotropy (FA) was calculated within deep white matter tracts associated with language. Analyses of variance were performed to test for differences among the groups in imaging measures. Receiver operator characteristic curves were used to determine how well different clinical versus imaging measures discriminated TLE‐LI from TLE‐NLI.
Results
TLE‐LI patients showed significantly less activation within left superior temporal cortex compared to HC and TLE‐NLI, regardless of side of seizure onset. TLE‐LI also showed decreased FA in the inferior longitudinal fasciculus and arcuate fasciculus compared to HC. Cortical thickness did not differ between groups in any region. A model that included language‐related fMRI activations within the superior temporal gyrus, age at onset, and demographic variables was the most predictive of language impairment (area under the curve = 0.80).
Significance
These findings demonstrate a unique imaging signature associated with a language‐impaired phenotype in TLE, characterized by functional and microstructural alterations within the language network. Reduced left superior temporal activation combined with compromise to language association tracts underlies this phenotype, extending our previous work on cognitive phenotypes that could have implications for treatment‐planning or cognitive progression in TLE. |
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| AbstractList | To identify neuroimaging and clinical biomarkers associated with a language-impaired phenotype in refractory temporal lobe epilepsy (TLE).OBJECTIVETo identify neuroimaging and clinical biomarkers associated with a language-impaired phenotype in refractory temporal lobe epilepsy (TLE).Eighty-five patients with TLE were characterized as language-impaired (TLE-LI) or non-language-impaired (TLE-NLI) based on comprehensive neuropsychological testing. Structural magnetic resonance imaging (MRI), diffusion tensor imaging, and functional MRI (fMRI) were obtained in patients and 47 healthy controls (HC). fMRI activations and cortical thickness were calculated within language regions of interest, and fractional anisotropy (FA) was calculated within deep white matter tracts associated with language. Analyses of variance were performed to test for differences among the groups in imaging measures. Receiver operator characteristic curves were used to determine how well different clinical versus imaging measures discriminated TLE-LI from TLE-NLI.METHODSEighty-five patients with TLE were characterized as language-impaired (TLE-LI) or non-language-impaired (TLE-NLI) based on comprehensive neuropsychological testing. Structural magnetic resonance imaging (MRI), diffusion tensor imaging, and functional MRI (fMRI) were obtained in patients and 47 healthy controls (HC). fMRI activations and cortical thickness were calculated within language regions of interest, and fractional anisotropy (FA) was calculated within deep white matter tracts associated with language. Analyses of variance were performed to test for differences among the groups in imaging measures. Receiver operator characteristic curves were used to determine how well different clinical versus imaging measures discriminated TLE-LI from TLE-NLI.TLE-LI patients showed significantly less activation within left superior temporal cortex compared to HC and TLE-NLI, regardless of side of seizure onset. TLE-LI also showed decreased FA in the inferior longitudinal fasciculus and arcuate fasciculus compared to HC. Cortical thickness did not differ between groups in any region. A model that included language-related fMRI activations within the superior temporal gyrus, age at onset, and demographic variables was the most predictive of language impairment (area under the curve = 0.80).RESULTSTLE-LI patients showed significantly less activation within left superior temporal cortex compared to HC and TLE-NLI, regardless of side of seizure onset. TLE-LI also showed decreased FA in the inferior longitudinal fasciculus and arcuate fasciculus compared to HC. Cortical thickness did not differ between groups in any region. A model that included language-related fMRI activations within the superior temporal gyrus, age at onset, and demographic variables was the most predictive of language impairment (area under the curve = 0.80).These findings demonstrate a unique imaging signature associated with a language-impaired phenotype in TLE, characterized by functional and microstructural alterations within the language network. Reduced left superior temporal activation combined with compromise to language association tracts underlies this phenotype, extending our previous work on cognitive phenotypes that could have implications for treatment-planning or cognitive progression in TLE.SIGNIFICANCEThese findings demonstrate a unique imaging signature associated with a language-impaired phenotype in TLE, characterized by functional and microstructural alterations within the language network. Reduced left superior temporal activation combined with compromise to language association tracts underlies this phenotype, extending our previous work on cognitive phenotypes that could have implications for treatment-planning or cognitive progression in TLE. Objective To identify neuroimaging and clinical biomarkers associated with a language‐impaired phenotype in refractory temporal lobe epilepsy (TLE). Methods Eighty‐five patients with TLE were characterized as language‐impaired (TLE‐LI) or non–language‐impaired (TLE‐NLI) based on comprehensive neuropsychological testing. Structural magnetic resonance imaging (MRI), diffusion tensor imaging, and functional MRI (fMRI) were obtained in patients and 47 healthy controls (HC). fMRI activations and cortical thickness were calculated within language regions of interest, and fractional anisotropy (FA) was calculated within deep white matter tracts associated with language. Analyses of variance were performed to test for differences among the groups in imaging measures. Receiver operator characteristic curves were used to determine how well different clinical versus imaging measures discriminated TLE‐LI from TLE‐NLI. Results TLE‐LI patients showed significantly less activation within left superior temporal cortex compared to HC and TLE‐NLI, regardless of side of seizure onset. TLE‐LI also showed decreased FA in the inferior longitudinal fasciculus and arcuate fasciculus compared to HC. Cortical thickness did not differ between groups in any region. A model that included language‐related fMRI activations within the superior temporal gyrus, age at onset, and demographic variables was the most predictive of language impairment (area under the curve = 0.80). Significance These findings demonstrate a unique imaging signature associated with a language‐impaired phenotype in TLE, characterized by functional and microstructural alterations within the language network. Reduced left superior temporal activation combined with compromise to language association tracts underlies this phenotype, extending our previous work on cognitive phenotypes that could have implications for treatment‐planning or cognitive progression in TLE. To identify neuroimaging and clinical biomarkers associated with a language-impaired phenotype in refractory temporal lobe epilepsy (TLE). Eighty-five patients with TLE were characterized as language-impaired (TLE-LI) or non-language-impaired (TLE-NLI) based on comprehensive neuropsychological testing. Structural magnetic resonance imaging (MRI), diffusion tensor imaging, and functional MRI (fMRI) were obtained in patients and 47 healthy controls (HC). fMRI activations and cortical thickness were calculated within language regions of interest, and fractional anisotropy (FA) was calculated within deep white matter tracts associated with language. Analyses of variance were performed to test for differences among the groups in imaging measures. Receiver operator characteristic curves were used to determine how well different clinical versus imaging measures discriminated TLE-LI from TLE-NLI. TLE-LI patients showed significantly less activation within left superior temporal cortex compared to HC and TLE-NLI, regardless of side of seizure onset. TLE-LI also showed decreased FA in the inferior longitudinal fasciculus and arcuate fasciculus compared to HC. Cortical thickness did not differ between groups in any region. A model that included language-related fMRI activations within the superior temporal gyrus, age at onset, and demographic variables was the most predictive of language impairment (area under the curve = 0.80). These findings demonstrate a unique imaging signature associated with a language-impaired phenotype in TLE, characterized by functional and microstructural alterations within the language network. Reduced left superior temporal activation combined with compromise to language association tracts underlies this phenotype, extending our previous work on cognitive phenotypes that could have implications for treatment-planning or cognitive progression in TLE. ObjectiveTo identify neuroimaging and clinical biomarkers associated with a language‐impaired phenotype in refractory temporal lobe epilepsy (TLE).MethodsEighty‐five patients with TLE were characterized as language‐impaired (TLE‐LI) or non–language‐impaired (TLE‐NLI) based on comprehensive neuropsychological testing. Structural magnetic resonance imaging (MRI), diffusion tensor imaging, and functional MRI (fMRI) were obtained in patients and 47 healthy controls (HC). fMRI activations and cortical thickness were calculated within language regions of interest, and fractional anisotropy (FA) was calculated within deep white matter tracts associated with language. Analyses of variance were performed to test for differences among the groups in imaging measures. Receiver operator characteristic curves were used to determine how well different clinical versus imaging measures discriminated TLE‐LI from TLE‐NLI.ResultsTLE‐LI patients showed significantly less activation within left superior temporal cortex compared to HC and TLE‐NLI, regardless of side of seizure onset. TLE‐LI also showed decreased FA in the inferior longitudinal fasciculus and arcuate fasciculus compared to HC. Cortical thickness did not differ between groups in any region. A model that included language‐related fMRI activations within the superior temporal gyrus, age at onset, and demographic variables was the most predictive of language impairment (area under the curve = 0.80).SignificanceThese findings demonstrate a unique imaging signature associated with a language‐impaired phenotype in TLE, characterized by functional and microstructural alterations within the language network. Reduced left superior temporal activation combined with compromise to language association tracts underlies this phenotype, extending our previous work on cognitive phenotypes that could have implications for treatment‐planning or cognitive progression in TLE. |
| Author | Macari, Anna Christina McDonald, Carrie R. Hermann, Bruce P. Kaestner, Erik Reyes, Anny Chang, Yu‐Hsuan Paul, Brianna M. |
| AuthorAffiliation | 6 UCSD Comprehensive Epilepsy Center, San Diego 1 Center for Multimodal Imaging and Genetics, University of California, San Diego 3 Department of Neurology, University of California – San Francisco, San Francisco 5 Matthews Neuropsychology Section, University of Wisconsin 7 Department of Psychiatry, University of California, San Diego 4 UCSF Comprehensive Epilepsy Center, San Francisco 2 San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology, San Diego |
| AuthorAffiliation_xml | – name: 1 Center for Multimodal Imaging and Genetics, University of California, San Diego – name: 5 Matthews Neuropsychology Section, University of Wisconsin – name: 2 San Diego State University/University of California San Diego Joint Doctoral Program in Clinical Psychology, San Diego – name: 6 UCSD Comprehensive Epilepsy Center, San Diego – name: 7 Department of Psychiatry, University of California, San Diego – name: 3 Department of Neurology, University of California – San Francisco, San Francisco – name: 4 UCSF Comprehensive Epilepsy Center, San Francisco |
| Author_xml | – sequence: 1 givenname: Erik orcidid: 0000-0003-3252-5365 surname: Kaestner fullname: Kaestner, Erik organization: University of California, San Diego – sequence: 2 givenname: Anny surname: Reyes fullname: Reyes, Anny organization: San Diego State University–University of California, San Diego Joint Doctoral Program in Clinical Psychology – sequence: 3 givenname: Anna Christina surname: Macari fullname: Macari, Anna Christina organization: University of California, San Diego – sequence: 4 givenname: Yu‐Hsuan surname: Chang fullname: Chang, Yu‐Hsuan organization: University of California, San Diego – sequence: 5 givenname: Brianna M. surname: Paul fullname: Paul, Brianna M. organization: University of California, San Francisco Comprehensive Epilepsy Center – sequence: 6 givenname: Bruce P. surname: Hermann fullname: Hermann, Bruce P. organization: University of Wisconsin – sequence: 7 givenname: Carrie R. surname: McDonald fullname: McDonald, Carrie R. email: camcdonald@ucsd.edu organization: University of California |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31297795$$D View this record in MEDLINE/PubMed |
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| Snippet | Objective
To identify neuroimaging and clinical biomarkers associated with a language‐impaired phenotype in refractory temporal lobe epilepsy (TLE).
Methods... To identify neuroimaging and clinical biomarkers associated with a language-impaired phenotype in refractory temporal lobe epilepsy (TLE). Eighty-five patients... ObjectiveTo identify neuroimaging and clinical biomarkers associated with a language‐impaired phenotype in refractory temporal lobe epilepsy... To identify neuroimaging and clinical biomarkers associated with a language-impaired phenotype in refractory temporal lobe epilepsy (TLE).OBJECTIVETo identify... |
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| SubjectTerms | Adult Anisotropy Brain - diagnostic imaging Brain - physiopathology Case-Control Studies clinical biomarkers Cognitive ability cognitive phenotype Cortex (temporal) Diffusion Tensor Imaging Drug Resistant Epilepsy - complications Drug Resistant Epilepsy - diagnostic imaging Drug Resistant Epilepsy - physiopathology Epilepsy Epilepsy, Temporal Lobe - complications Epilepsy, Temporal Lobe - diagnostic imaging Epilepsy, Temporal Lobe - physiopathology Female Functional magnetic resonance imaging Functional Neuroimaging Genotype & phenotype Humans Language Language Disorders - diagnostic imaging Language Disorders - etiology Language Disorders - physiopathology Language Tests Magnetic Resonance Imaging Male Measuring techniques neural substrate Neuroimaging NMR Nuclear magnetic resonance Patients Phenotype Phenotypes Psychology Seizures Substantia alba Superior temporal gyrus Temporal gyrus Temporal lobe |
| Title | Identifying the neural basis of a language‐impaired phenotype of temporal lobe epilepsy |
| URI | https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fepi.16283 https://www.ncbi.nlm.nih.gov/pubmed/31297795 https://www.proquest.com/docview/2269069225 https://www.proquest.com/docview/2257714158 https://pubmed.ncbi.nlm.nih.gov/PMC6687533 |
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