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Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia

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Resumo:Recent studies have reported early cerebellar and subcortical impact in the disease progression of genetic frontotemporal dementia (FTD) due to microtubule-associated protein tau (MAPT), progranulin (GRN) and chromosome 9 open reading frame 72 (C9orf72). However, the cerebello-subcortical circuitry in FTD has been understudied despite its essential role in cognition and behaviors related to FTD symptomatology. The present study aims to investigate the association between cerebellar and subcortical atrophy, and neuropsychiatric symptoms across genetic mutations. Our study included 983 participants from the Genetic Frontotemporal dementia Initiative including mutation carriers and noncarrier first-degree relatives of known symptomatic carriers. Voxel-wise analysis of the thalamus, striatum, globus pallidus, amygdala, and the cerebellum was performed, and partial least squares analyses (PLS) were used to link morphometry and behavior. In presymptomatic C9orf72 expansion carriers, thalamic atrophy was found compared to noncarriers, suggesting the importance of this structure in FTD prodromes. PLS analyses demonstrated that the cerebello-subcortical circuitry is related to neuropsychiatric symptoms, with significant overlap in brain/behavior patterns, but also specificity for each genetic mutation group. The largest differences were in the cerebellar atrophy (larger extent in C9orf72 expansion group) and more prominent amygdalar volume reduction in the MAPT group. Brain scores in the C9orf72 expansion carriers and MAPT carriers demonstrated covariation patterns concordant with atrophy patterns detectable up to 20 years before expected symptom onset. Overall, these results demonstrated the important role of the subcortical structures in genetic FTD symptom expression, particularly the cerebellum in C9orf72 and the amygdala in MAPT carriers.
Autores principais:Bussy, Aurélie
Outros Autores:Levy, Jake P.; Best, Tristin; Patel, Raihaan; Cupo, Lani; Van Langenhove, Tim; Nielsen, Jørgen E.; Pijnenburg, Yolande; Waldö, Maria Landqvist; Remes, Anne M.; Schroeter, Matthias L.; Santana, Isabel; Pasquier, Florence; Otto, Markus; Danek, Adrian; Levin, Johannes; Le Ber, Isabelle; Vandenberghe, Rik; Synofzik, Matthis; Moreno, Fermin; De Mendonça, Alexandre; Sanchez‐Valle, Raquel; Laforce, Robert; Langheinrich, Tobias; Gerhard, Alexander; Graff, Caroline; Butler, Chris R.; Sorbi, Sandro; Jiskoot, Lize; Seelaar, Harro; van Swieten, John C.; Finger, Elizabeth; Tartaglia, Maria Carmela; Masellis, Mario; Tiraboschi, Pietro; Galimberti, Daniela; Borroni, Barbara; Rowe, James B.; Bocchetta, Martina; Rohrer, Jonathan D.; Devenyi, Gabriel A.; Chakravarty, M. Mallar; Ducharme, Simon
Assunto:Frontotemporal dementia Genetics Magnetic resonance imaging Neuropsychiatry
Ano:2023
País:Portugal
Tipo de documento:artigo
Tipo de acesso:acesso aberto
Instituição associada:Universidade de Lisboa
Idioma:inglês
Origem:Repositório da Universidade de Lisboa
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author Bussy, Aurélie
author2 Levy, Jake P.
Best, Tristin
Patel, Raihaan
Cupo, Lani
Van Langenhove, Tim
Nielsen, Jørgen E.
Pijnenburg, Yolande
Waldö, Maria Landqvist
Remes, Anne M.
Schroeter, Matthias L.
Santana, Isabel
Pasquier, Florence
Otto, Markus
Danek, Adrian
Levin, Johannes
Le Ber, Isabelle
Vandenberghe, Rik
Synofzik, Matthis
Moreno, Fermin
De Mendonça, Alexandre
Sanchez‐Valle, Raquel
Laforce, Robert
Langheinrich, Tobias
Gerhard, Alexander
Graff, Caroline
Butler, Chris R.
Sorbi, Sandro
Jiskoot, Lize
Seelaar, Harro
van Swieten, John C.
Finger, Elizabeth
Tartaglia, Maria Carmela
Masellis, Mario
Tiraboschi, Pietro
Galimberti, Daniela
Borroni, Barbara
Rowe, James B.
Bocchetta, Martina
Rohrer, Jonathan D.
Devenyi, Gabriel A.
Chakravarty, M. Mallar
Ducharme, Simon
author2_role author
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author
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author
author
author_facet Bussy, Aurélie
Levy, Jake P.
Best, Tristin
Patel, Raihaan
Cupo, Lani
Van Langenhove, Tim
Nielsen, Jørgen E.
Pijnenburg, Yolande
Waldö, Maria Landqvist
Remes, Anne M.
Schroeter, Matthias L.
Santana, Isabel
Pasquier, Florence
Otto, Markus
Danek, Adrian
Levin, Johannes
Le Ber, Isabelle
Vandenberghe, Rik
Synofzik, Matthis
Moreno, Fermin
De Mendonça, Alexandre
Sanchez‐Valle, Raquel
Laforce, Robert
Langheinrich, Tobias
Gerhard, Alexander
Graff, Caroline
Butler, Chris R.
Sorbi, Sandro
Jiskoot, Lize
Seelaar, Harro
van Swieten, John C.
Finger, Elizabeth
Tartaglia, Maria Carmela
Masellis, Mario
Tiraboschi, Pietro
Galimberti, Daniela
Borroni, Barbara
Rowe, James B.
Bocchetta, Martina
Rohrer, Jonathan D.
Devenyi, Gabriel A.
Chakravarty, M. Mallar
Ducharme, Simon
author_role author
contributor_name_str_mv Repositório Científico de Acesso Aberto da ULisboa
country_str PT
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datacite.contributors.contributor.contributorName.fl_str_mv Repositório Científico de Acesso Aberto da ULisboa
datacite.creators.creator.creatorName.fl_str_mv Bussy, Aurélie
Levy, Jake P.
Best, Tristin
Patel, Raihaan
Cupo, Lani
Van Langenhove, Tim
Nielsen, Jørgen E.
Pijnenburg, Yolande
Waldö, Maria Landqvist
Remes, Anne M.
Schroeter, Matthias L.
Santana, Isabel
Pasquier, Florence
Otto, Markus
Danek, Adrian
Levin, Johannes
Le Ber, Isabelle
Vandenberghe, Rik
Synofzik, Matthis
Moreno, Fermin
De Mendonça, Alexandre
Sanchez‐Valle, Raquel
Laforce, Robert
Langheinrich, Tobias
Gerhard, Alexander
Graff, Caroline
Butler, Chris R.
Sorbi, Sandro
Jiskoot, Lize
Seelaar, Harro
van Swieten, John C.
Finger, Elizabeth
Tartaglia, Maria Carmela
Masellis, Mario
Tiraboschi, Pietro
Galimberti, Daniela
Borroni, Barbara
Rowe, James B.
Bocchetta, Martina
Rohrer, Jonathan D.
Devenyi, Gabriel A.
Chakravarty, M. Mallar
Ducharme, Simon
datacite.date.Accepted.fl_str_mv 2023-01-01T00:00:00Z
datacite.date.available.fl_str_mv 2023-03-14T14:21:30Z
datacite.date.embargoed.fl_str_mv 2023-03-14T14:21:30Z
datacite.rights.fl_str_mv http://purl.org/coar/access_right/c_abf2
datacite.subjects.subject.fl_str_mv Frontotemporal dementia
Genetics
Magnetic resonance imaging
Neuropsychiatry
datacite.titles.title.fl_str_mv Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia
dc.contributor.none.fl_str_mv Repositório Científico de Acesso Aberto da ULisboa
dc.creator.none.fl_str_mv Bussy, Aurélie
Levy, Jake P.
Best, Tristin
Patel, Raihaan
Cupo, Lani
Van Langenhove, Tim
Nielsen, Jørgen E.
Pijnenburg, Yolande
Waldö, Maria Landqvist
Remes, Anne M.
Schroeter, Matthias L.
Santana, Isabel
Pasquier, Florence
Otto, Markus
Danek, Adrian
Levin, Johannes
Le Ber, Isabelle
Vandenberghe, Rik
Synofzik, Matthis
Moreno, Fermin
De Mendonça, Alexandre
Sanchez‐Valle, Raquel
Laforce, Robert
Langheinrich, Tobias
Gerhard, Alexander
Graff, Caroline
Butler, Chris R.
Sorbi, Sandro
Jiskoot, Lize
Seelaar, Harro
van Swieten, John C.
Finger, Elizabeth
Tartaglia, Maria Carmela
Masellis, Mario
Tiraboschi, Pietro
Galimberti, Daniela
Borroni, Barbara
Rowe, James B.
Bocchetta, Martina
Rohrer, Jonathan D.
Devenyi, Gabriel A.
Chakravarty, M. Mallar
Ducharme, Simon
dc.date.Accepted.fl_str_mv 2023-01-01T00:00:00Z
dc.date.available.fl_str_mv 2023-03-14T14:21:30Z
dc.date.embargoed.fl_str_mv 2023-03-14T14:21:30Z
dc.format.none.fl_str_mv application/pdf
dc.identifier.none.fl_str_mv http://hdl.handle.net/10451/56655
dc.language.none.fl_str_mv eng
dc.publisher.none.fl_str_mv Wiley
dc.rights.cclincense.fl_str_mv http://creativecommons.org/licenses/by-nc-nd/4.0/
dc.rights.none.fl_str_mv http://purl.org/coar/access_right/c_abf2
dc.subject.none.fl_str_mv Frontotemporal dementia
Genetics
Magnetic resonance imaging
Neuropsychiatry
dc.title.fl_str_mv Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia
dc.type.none.fl_str_mv http://purl.org/coar/resource_type/c_6501
description Recent studies have reported early cerebellar and subcortical impact in the disease progression of genetic frontotemporal dementia (FTD) due to microtubule-associated protein tau (MAPT), progranulin (GRN) and chromosome 9 open reading frame 72 (C9orf72). However, the cerebello-subcortical circuitry in FTD has been understudied despite its essential role in cognition and behaviors related to FTD symptomatology. The present study aims to investigate the association between cerebellar and subcortical atrophy, and neuropsychiatric symptoms across genetic mutations. Our study included 983 participants from the Genetic Frontotemporal dementia Initiative including mutation carriers and noncarrier first-degree relatives of known symptomatic carriers. Voxel-wise analysis of the thalamus, striatum, globus pallidus, amygdala, and the cerebellum was performed, and partial least squares analyses (PLS) were used to link morphometry and behavior. In presymptomatic C9orf72 expansion carriers, thalamic atrophy was found compared to noncarriers, suggesting the importance of this structure in FTD prodromes. PLS analyses demonstrated that the cerebello-subcortical circuitry is related to neuropsychiatric symptoms, with significant overlap in brain/behavior patterns, but also specificity for each genetic mutation group. The largest differences were in the cerebellar atrophy (larger extent in C9orf72 expansion group) and more prominent amygdalar volume reduction in the MAPT group. Brain scores in the C9orf72 expansion carriers and MAPT carriers demonstrated covariation patterns concordant with atrophy patterns detectable up to 20 years before expected symptom onset. Overall, these results demonstrated the important role of the subcortical structures in genetic FTD symptom expression, particularly the cerebellum in C9orf72 and the amygdala in MAPT carriers.
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eu_rights_str_mv openAccess
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fulltext.url.fl_str_mv https://repositorio.ulisboa.pt/bitstreams/f762bb27-9c47-4cb4-9ffd-a2287a7d0e93/download
id ul_e155df86747ebd2a367d6033a862ff6c
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institution Universidade de Lisboa
instname_str Universidade de Lisboa
language eng
network_acronym_str ul
network_name_str Repositório da Universidade de Lisboa
oai_identifier_str oai:repositorio.ulisboa.pt:10451/56655
organization_str_mv urn:organizationAcronym:ul
person_str_mv Bussy, Aurélie
Levy, Jake P.
Best, Tristin
Patel, Raihaan
Cupo, Lani
Van Langenhove, Tim
Nielsen, Jørgen E.
Pijnenburg, Yolande
Waldö, Maria Landqvist
Remes, Anne M.
Schroeter, Matthias L.
Santana, Isabel
Pasquier, Florence
Otto, Markus
Danek, Adrian
Levin, Johannes
Le Ber, Isabelle
Vandenberghe, Rik
Synofzik, Matthis
Moreno, Fermin
De Mendonça, Alexandre
De Mendonça, Alexandre
https://www.ciencia-id.pt/1615-41B4-0848
1615-41B4-0848
http://orcid.org/0000-0002-0488-1453
0000-0002-0488-1453
Sanchez‐Valle, Raquel
Laforce, Robert
Langheinrich, Tobias
Gerhard, Alexander
Graff, Caroline
Butler, Chris R.
Sorbi, Sandro
Jiskoot, Lize
Seelaar, Harro
van Swieten, John C.
Finger, Elizabeth
Tartaglia, Maria Carmela
Masellis, Mario
Tiraboschi, Pietro
Galimberti, Daniela
Borroni, Barbara
Rowe, James B.
Bocchetta, Martina
Rohrer, Jonathan D.
Devenyi, Gabriel A.
Chakravarty, M. Mallar
Ducharme, Simon
publishDate 2023
publisher.none.fl_str_mv Wiley
reponame_str Repositório da Universidade de Lisboa
repository_id_str urn:repositoryAcronym:ul
service_str_mv urn:repositoryAcronym:ul
spelling engWileypt_PTRecent studies have reported early cerebellar and subcortical impact in the disease progression of genetic frontotemporal dementia (FTD) due to microtubule-associated protein tau (MAPT), progranulin (GRN) and chromosome 9 open reading frame 72 (C9orf72). However, the cerebello-subcortical circuitry in FTD has been understudied despite its essential role in cognition and behaviors related to FTD symptomatology. The present study aims to investigate the association between cerebellar and subcortical atrophy, and neuropsychiatric symptoms across genetic mutations. Our study included 983 participants from the Genetic Frontotemporal dementia Initiative including mutation carriers and noncarrier first-degree relatives of known symptomatic carriers. Voxel-wise analysis of the thalamus, striatum, globus pallidus, amygdala, and the cerebellum was performed, and partial least squares analyses (PLS) were used to link morphometry and behavior. In presymptomatic C9orf72 expansion carriers, thalamic atrophy was found compared to noncarriers, suggesting the importance of this structure in FTD prodromes. PLS analyses demonstrated that the cerebello-subcortical circuitry is related to neuropsychiatric symptoms, with significant overlap in brain/behavior patterns, but also specificity for each genetic mutation group. The largest differences were in the cerebellar atrophy (larger extent in C9orf72 expansion group) and more prominent amygdalar volume reduction in the MAPT group. Brain scores in the C9orf72 expansion carriers and MAPT carriers demonstrated covariation patterns concordant with atrophy patterns detectable up to 20 years before expected symptom onset. Overall, these results demonstrated the important role of the subcortical structures in genetic FTD symptom expression, particularly the cerebellum in C9orf72 and the amygdala in MAPT carriers.application/pdfpt_PTCerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementiaBussy, AurélieLevy, Jake P.Best, TristinPatel, RaihaanCupo, LaniVan Langenhove, TimNielsen, Jørgen E.Pijnenburg, YolandeWaldö, Maria LandqvistRemes, Anne M.Schroeter, Matthias L.Santana, IsabelPasquier, FlorenceOtto, MarkusDanek, AdrianLevin, JohannesLe Ber, IsabelleVandenberghe, RikSynofzik, MatthisMoreno, FerminPersonalDe Mendonça, AlexandreDSpacehttp://dspace.org/items/53ca3547-99ce-4b68-9330-7879a54c47b7DSpacehttp://dspace.org/items/53ca3547-99ce-4b68-9330-7879a54c47b7de MendonçaAlexandreCiência IDhttps://www.ciencia-id.pt1615-41B4-0848ORCIDhttp://orcid.org0000-0002-0488-1453Scopus Author IDhttps://www.scopus.com7003320823Scopus Author IDhttps://www.scopus.com55307490700Sanchez‐Valle, RaquelLaforce, RobertLangheinrich, TobiasGerhard, AlexanderGraff, CarolineButler, Chris R.Sorbi, SandroJiskoot, LizeSeelaar, Harrovan Swieten, John C.Finger, ElizabethTartaglia, Maria CarmelaMasellis, MarioTiraboschi, PietroGalimberti, DanielaBorroni, BarbaraRowe, James B.Bocchetta, MartinaRohrer, Jonathan D.Devenyi, Gabriel A.Chakravarty, M. MallarDucharme, SimonHostingInstitutionOrganizationalRepositório Científico de Acesso Aberto da ULisboae-mailmailto:repositorio@reitoria.ulisboa.ptrepositorio@reitoria.ulisboa.ptISSNIsPartOf1065-9471DOIIsPartOf10.1002/hbm.262202023-03-14T14:21:30Z20232023-01-01T00:00:00ZHandlehttp://hdl.handle.net/10451/56655http://purl.org/coar/access_right/c_abf2open accessFrontotemporal dementiaGeneticsMagnetic resonance imagingNeuropsychiatry11069069 bytesliteraturehttp://purl.org/coar/resource_type/c_6501journal article2023http://creativecommons.org/licenses/by-nc-nd/4.0/http://purl.org/coar/access_right/c_abf2application/pdffulltexthttps://repositorio.ulisboa.pt/bitstreams/f762bb27-9c47-4cb4-9ffd-a2287a7d0e93/downloadHuman Brain Mapping
spellingShingle Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia
Bussy, Aurélie
Frontotemporal dementia
Genetics
Magnetic resonance imaging
Neuropsychiatry
status SINGLETON
subject.fl_str_mv Frontotemporal dementia
Genetics
Magnetic resonance imaging
Neuropsychiatry
title Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia
title_full Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia
title_fullStr Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia
title_full_unstemmed Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia
title_short Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia
title_sort Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia
topic Frontotemporal dementia
Genetics
Magnetic resonance imaging
Neuropsychiatry
topic_facet Frontotemporal dementia
Genetics
Magnetic resonance imaging
Neuropsychiatry
url http://hdl.handle.net/10451/56655
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