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...

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Veröffentlicht in:	Frontiers in neurology Jg. 9; S. 766
Hauptverfasser:	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
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	Switzerland Frontiers Media 18.09.2018 Frontiers Media S.A
Schlagworte:	Computer Science cortical metabolism cortical thickness Medical Imaging MRI Neurology PET primary progressive aphasias tracts cortical metabolism primary progressive aphasias tracts MRI cortical thickness PET
ISSN:	1664-2295, 1664-2295
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Abstract	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 ( = 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.
AbstractList	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. 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.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. 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 ( = 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.
Author	Routier, Alexandre Moreaud, Olivier Migliaccio, Raphaëlla Colliot, Olivier Bennys, Karim Bertrand, Anne Couratier, Philippe Pasquier, Florence Habert, Marie-Odile Laurent, Bernard Dubois, Bruno Kas, Aurélie Mertz, Justine Martinaud, Olivier Etcharry-Bouyx, Frédérique Sundqvist, Martina Boutoleau-Bretonnière, Claire Bertin, Hugo David, Pierre-Maxime Belliard, Serge Pariente, Jérémie Puel, Michèle Godefroy, Olivier Teichmann, Marc
AuthorAffiliation	13 Department of Neurology, University Hospital of Rouen , Rouen , France 11 Department of Neurology, University Hospital of Lille , Lille , France 1 Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, FrontLab , Paris , France 23 National Reference Center for “PPA and rare dementias”, Institute for Memory and Alzheimer's Disease, AP-HP , Paris , France 19 Department of Neurology, University Hospital of Limoges , Limoges , France 17 CHU Toulouse, Neurology Department , Toulouse , France 25 AP-HP, Departments of Neuroradiology and Neurology, Hôpital de la Pitié-Salpêtrière , Paris , France 8 Department of Nuclear Medicine, European Hospital Georges Pompidou , Paris , France 16 Department of Neurology and Laboratory of Functional Neurosciences (EA 4559), University Hospital of Amiens , Amiens , France 22 Department of Neurology, Institute for Memory and Alzheimer's Disease, Pitié-Salpêtrière Hospital, AP-HP , Paris , France 15 Department of Psychia
AuthorAffiliation_xml	– name: 7 AP-HP, Hôpital Saint Antoine, Department of Radiology , Paris , France – name: 10 Department of Neurology, Memory Research and Resource Center for Alzheimer's Disease, University Hospital Pontchaillou , Rennes , France – name: 3 Laboratoire d'Imagerie Biomédicale, Sorbonne Université, Inserm U 1146, CNRS UMR , Paris , France – name: 20 Department of Neurology, University Hospital of Nantes , Nantes , France – name: 25 AP-HP, Departments of Neuroradiology and Neurology, Hôpital de la Pitié-Salpêtrière , Paris , France – name: 9 Normandie University, UNICAEN, EPHE, INSERM, U1077, Neuropsychologie et Imagerie de la Mémoire Humaine , Caen , France – name: 14 Department of Neurology, Memory Research and Resource Center for Alzheimer's Disease, University Hospital of Angers , Angers , France – name: 23 National Reference Center for “PPA and rare dementias”, Institute for Memory and Alzheimer's Disease, AP-HP , Paris , France – name: 24 Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université , Paris , France – name: 2 Inria, Aramis Project-Team , Paris , France – name: 1 Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, FrontLab , Paris , France – name: 13 Department of Neurology, University Hospital of Rouen , Rouen , France – name: 18 INSERM/UPS, UMR 1214—ToNIC, Toulouse NeuroImaging Center, University of Toulouse III , Toulouse , France – name: 5 Centre Acquisition et Traitement des Images , Paris , France – name: 15 Department of Psychiatry, Neurology and Rehabilitation University Hospital of Grenoble, Memory Research and Resource Center for Alzheimer's Disease , Grenoble , France – name: 8 Department of Nuclear Medicine, European Hospital Georges Pompidou , Paris , France – name: 11 Department of Neurology, University Hospital of Lille , Lille , France – name: 12 Department of Neurology, Memory Research and Resource Center for Alzheimer's Disease, University Hospital of Montpellier , Montpellier , France – name: 21 Department of Neurology, University Hospital of Saint-Etienne , Saint-Etienne , France – name: 4 AP-HP, Hôpital Pitié-Salpêtrière, Department of Nuclear Medicine , Paris , France – name: 19 Department of Neurology, University Hospital of Limoges , Limoges , France – name: 17 CHU Toulouse, Neurology Department , Toulouse , France – name: 6 Institut du Cerveau et de la Moelle épinière, ICM, Inserm U 1127, CNRS UMR 7225, Sorbonne Université, AP-HP , Paris , France – name: 22 Department of Neurology, Institute for Memory and Alzheimer's Disease, Pitié-Salpêtrière Hospital, AP-HP , Paris , France – name: 16 Department of Neurology and Laboratory of Functional Neurosciences (EA 4559), University Hospital of Amiens , Amiens , France
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ContentType	Journal Article
Copyright	Distributed under a Creative Commons Attribution 4.0 International License 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. 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
Copyright_xml	– notice: Distributed under a Creative Commons Attribution 4.0 International License – notice: 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. 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
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Keywords	cortical metabolism primary progressive aphasias tracts MRI cortical thickness PET
Language	English
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 PMCID: PMC6153366 Deceased, March 2nd 2018 Edited by: Freimut Dankwart Juengling, St. Claraspital Basel, Switzerland Reviewed by: Jordi A. Matias-Guiu, Hospital Clínico San Carlos, Spain; Cristian E. Leyton, University of Sydney, Australia This article was submitted to Applied Neuroimaging, a section of the journal Frontiers in Neurology
ORCID	0000-0002-9850-296X 0000-0002-9836-654X 0000-0001-6789-6620 0000-0002-7004-8777 0000-0001-9463-3658 0000-0001-8933-1575 0000-0003-1603-8049 0000-0002-7719-9746 0000-0001-9562-856X
OpenAccessLink	https://doaj.org/article/2f985459a1be4b8b9963df5591073499
PMID	30279675
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PQPubID	23479
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PublicationCentury	2000
PublicationDate	2018-09-18
PublicationDateYYYYMMDD	2018-09-18
PublicationDate_xml	– month: 09 year: 2018 text: 2018-09-18 day: 18
PublicationDecade	2010
PublicationPlace	Switzerland
PublicationPlace_xml	– name: Switzerland
PublicationTitle	Frontiers in neurology
PublicationTitleAlternate	Front Neurol
PublicationYear	2018
Publisher	Frontiers Media Frontiers Media S.A
Publisher_xml	– name: Frontiers Media – name: Frontiers Media S.A
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Snippet	Neuroimaging studies have described the brain alterations in primary progressive aphasia (PPA) variants (semantic, logopenic, nonfluent/agrammatic). However,...
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SubjectTerms	Computer Science cortical metabolism cortical thickness Medical Imaging MRI Neurology PET primary progressive aphasias tracts
Title	Structural, Microstructural, and Metabolic Alterations in Primary Progressive Aphasia Variants
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