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Structural, Microstructural, and Metabolic Alterations in Primary Progressive Aphasia Variants
Neuroimaging studies have described the brain alterations in primary progressive aphasia (PPA) variants (semantic, logopenic, nonfluent/agrammatic). However, few studies combined T1, FDG-PET, and diffusion MRI techniques to study atrophy, hypometabolism, and tract alterations across the three PPA ma...
Autores principales: | , , , , , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Frontiers Media S.A.
2018
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6153366/ https://www.ncbi.nlm.nih.gov/pubmed/30279675 http://dx.doi.org/10.3389/fneur.2018.00766 |
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author | Routier, Alexandre Habert, Marie-Odile Bertrand, Anne Kas, Aurélie Sundqvist, Martina Mertz, Justine David, Pierre-Maxime Bertin, Hugo Belliard, Serge Pasquier, Florence Bennys, Karim Martinaud, Olivier Etcharry-Bouyx, Frédérique Moreaud, Olivier Godefroy, Olivier Pariente, Jérémie Puel, Michèle Couratier, Philippe Boutoleau-Bretonnière, Claire Laurent, Bernard Migliaccio, Raphaëlla Dubois, Bruno Colliot, Olivier Teichmann, Marc |
author_facet | Routier, Alexandre Habert, Marie-Odile Bertrand, Anne Kas, Aurélie Sundqvist, Martina Mertz, Justine David, Pierre-Maxime Bertin, Hugo Belliard, Serge Pasquier, Florence Bennys, Karim Martinaud, Olivier Etcharry-Bouyx, Frédérique Moreaud, Olivier Godefroy, Olivier Pariente, Jérémie Puel, Michèle Couratier, Philippe Boutoleau-Bretonnière, Claire Laurent, Bernard Migliaccio, Raphaëlla Dubois, Bruno Colliot, Olivier Teichmann, Marc |
author_sort | Routier, Alexandre |
collection | PubMed |
description | Neuroimaging studies have described the brain alterations in primary progressive aphasia (PPA) variants (semantic, logopenic, nonfluent/agrammatic). However, few studies combined T1, FDG-PET, and diffusion MRI techniques to study atrophy, hypometabolism, and tract alterations across the three PPA main variants. We therefore explored a large early-stage cohort of semantic, logopenic and nonfluent/agrammatic variants (N = 86) and of 23 matched healthy controls with anatomical MRI (cortical thickness), FDG PET (metabolism) and diffusion MRI (white matter tracts analyses), aiming at identifying cortical and sub-cortical brain alterations, and confronting these alterations across imaging modalities and aphasia variants. In the semantic variant, there was cortical thinning and hypometabolism in anterior temporal cortices, with left-hemisphere predominance, extending toward posterior temporal regions, and affecting tracts projecting to the anterior temporal lobes (inferior longitudinal fasciculus, uncinate fasciculus) and tracts projecting to or running nearby posterior temporal cortices: (superior longitudinal fasciculus, inferior frontal-occipital fasciculus). In the logopenic variant metabolic alterations were more extensive than atrophy affecting mainly the left temporal-parietal junction and extending toward more anterior temporal cortices. Metabolic and tract data were coherent given the alterations of the left superior and inferior longitudinal fasciculus and the left inferior frontal-occipital fasciculus. In the nonfluent/agrammatic variant cortical thinning and hypometabolism were located in the left frontal cortex but Broca's area was only affected on metabolic measures. Metabolic and tract alterations were coherent as reflected by damage to the left uncinate fasciculus connecting with Broca's area. Our findings provide a full-blown statistically robust picture of brain alterations in early-stage variants of primary progressive aphasia which has implications for diagnosis, classification and future therapeutic strategies. They demonstrate that in logopenic and semantic variants patterns of brain damage display a non-negligible overlap in temporal regions whereas they are substantially distinct in the nonfluent/agrammatic variant (frontal regions). These results also indicate that frontal networks (combinatorial syntax/phonology) and temporal networks (lexical/semantic representations) constitute distinct anatomo-functional entities with differential vulnerability to degenerative processes in aphasia variants. Finally, the identification of the specific damage patterns could open an avenue for trans-cranial stimulation approaches by indicating the appropriate target-entry into the damaged language system. |
format | Online Article Text |
id | pubmed-6153366 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2018 |
publisher | Frontiers Media S.A. |
record_format | MEDLINE/PubMed |
spelling | pubmed-61533662018-10-02 Structural, Microstructural, and Metabolic Alterations in Primary Progressive Aphasia Variants Routier, Alexandre Habert, Marie-Odile Bertrand, Anne Kas, Aurélie Sundqvist, Martina Mertz, Justine David, Pierre-Maxime Bertin, Hugo Belliard, Serge Pasquier, Florence Bennys, Karim Martinaud, Olivier Etcharry-Bouyx, Frédérique Moreaud, Olivier Godefroy, Olivier Pariente, Jérémie Puel, Michèle Couratier, Philippe Boutoleau-Bretonnière, Claire Laurent, Bernard Migliaccio, Raphaëlla Dubois, Bruno Colliot, Olivier Teichmann, Marc Front Neurol Neurology Neuroimaging studies have described the brain alterations in primary progressive aphasia (PPA) variants (semantic, logopenic, nonfluent/agrammatic). However, few studies combined T1, FDG-PET, and diffusion MRI techniques to study atrophy, hypometabolism, and tract alterations across the three PPA main variants. We therefore explored a large early-stage cohort of semantic, logopenic and nonfluent/agrammatic variants (N = 86) and of 23 matched healthy controls with anatomical MRI (cortical thickness), FDG PET (metabolism) and diffusion MRI (white matter tracts analyses), aiming at identifying cortical and sub-cortical brain alterations, and confronting these alterations across imaging modalities and aphasia variants. In the semantic variant, there was cortical thinning and hypometabolism in anterior temporal cortices, with left-hemisphere predominance, extending toward posterior temporal regions, and affecting tracts projecting to the anterior temporal lobes (inferior longitudinal fasciculus, uncinate fasciculus) and tracts projecting to or running nearby posterior temporal cortices: (superior longitudinal fasciculus, inferior frontal-occipital fasciculus). In the logopenic variant metabolic alterations were more extensive than atrophy affecting mainly the left temporal-parietal junction and extending toward more anterior temporal cortices. Metabolic and tract data were coherent given the alterations of the left superior and inferior longitudinal fasciculus and the left inferior frontal-occipital fasciculus. In the nonfluent/agrammatic variant cortical thinning and hypometabolism were located in the left frontal cortex but Broca's area was only affected on metabolic measures. Metabolic and tract alterations were coherent as reflected by damage to the left uncinate fasciculus connecting with Broca's area. Our findings provide a full-blown statistically robust picture of brain alterations in early-stage variants of primary progressive aphasia which has implications for diagnosis, classification and future therapeutic strategies. They demonstrate that in logopenic and semantic variants patterns of brain damage display a non-negligible overlap in temporal regions whereas they are substantially distinct in the nonfluent/agrammatic variant (frontal regions). These results also indicate that frontal networks (combinatorial syntax/phonology) and temporal networks (lexical/semantic representations) constitute distinct anatomo-functional entities with differential vulnerability to degenerative processes in aphasia variants. Finally, the identification of the specific damage patterns could open an avenue for trans-cranial stimulation approaches by indicating the appropriate target-entry into the damaged language system. Frontiers Media S.A. 2018-09-18 /pmc/articles/PMC6153366/ /pubmed/30279675 http://dx.doi.org/10.3389/fneur.2018.00766 Text en Copyright © 2018 Routier, Habert, Bertrand, Kas, Sundqvist, Mertz, David, Bertin, Belliard, Pasquier, Bennys, Martinaud, Etcharry-Bouyx, Moreaud, Godefroy, Pariente, Puel, Couratier, Boutoleau-Bretonnière, Laurent, Migliaccio, Dubois, Colliot and Teichmann. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
spellingShingle | Neurology Routier, Alexandre Habert, Marie-Odile Bertrand, Anne Kas, Aurélie Sundqvist, Martina Mertz, Justine David, Pierre-Maxime Bertin, Hugo Belliard, Serge Pasquier, Florence Bennys, Karim Martinaud, Olivier Etcharry-Bouyx, Frédérique Moreaud, Olivier Godefroy, Olivier Pariente, Jérémie Puel, Michèle Couratier, Philippe Boutoleau-Bretonnière, Claire Laurent, Bernard Migliaccio, Raphaëlla Dubois, Bruno Colliot, Olivier Teichmann, Marc Structural, Microstructural, and Metabolic Alterations in Primary Progressive Aphasia Variants |
title | Structural, Microstructural, and Metabolic Alterations in Primary Progressive Aphasia Variants |
title_full | Structural, Microstructural, and Metabolic Alterations in Primary Progressive Aphasia Variants |
title_fullStr | Structural, Microstructural, and Metabolic Alterations in Primary Progressive Aphasia Variants |
title_full_unstemmed | Structural, Microstructural, and Metabolic Alterations in Primary Progressive Aphasia Variants |
title_short | Structural, Microstructural, and Metabolic Alterations in Primary Progressive Aphasia Variants |
title_sort | structural, microstructural, and metabolic alterations in primary progressive aphasia variants |
topic | Neurology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6153366/ https://www.ncbi.nlm.nih.gov/pubmed/30279675 http://dx.doi.org/10.3389/fneur.2018.00766 |
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