Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia

Aurélie Bussy; Jake P Levy; Tristin Best; Raihaan Patel; Lani Cupo; Tim van Langenhove; Jørgen E Nielsen; Yolande Pijnenburg; Maria Landqvist Waldö; Anne M Remes; Matthias L Schroeter; Isabel Santana; Florence Pasquier; Markus Otto; Adrian Danek; Johannes Levin; Isabelle Le Ber; Rik Vandenberghe; Matthis Synofzik; Fermin Moreno; Alexandre de Mendonça; Raquel Sanchez‐valle; Robert Laforce; Tobias Langheinrich; Alexander Gerhard; Caroline Graff; Chris R Butler; Sandro Sorbi; Lize Jiskoot; Harro Seelaar; John C van Swieten; Elizabeth Finger; Maria Carmela Tartaglia; Mario Masellis; Pietro Tiraboschi; Daniela Galimberti; Barbara Borroni; James B Rowe; Martina Bocchetta; Jonathan D Rohrer; Gabriel A Devenyi; M Mallar Chakravarty; Simon Ducharme; Esteve Aitana Sogorb; Nelson Annabel; Bouzigues Arabella; Heller Carolin; Greaves Caroline V; Cash David; Thomas David L; Todd Emily; Benotmane Hanya; Zetterberg Henrik; Swift Imogen J; Nicholas Jennifer; Samra Kiran; Russell Lucy L; Bocchetta Martina; Shafei Rachelle; Convery Rhian S; Timberlake Carolyn; Cope Thomas; Rittman Timothy; Benussi Alberto; Premi Enrico; Gasparotti Roberto; Archetti Silvana; Gazzina Stefano; Cantoni Valentina; Arighi Andrea; Fenoglio Chiara; Scarpini Elio; Fumagalli Giorgio; Borracci Vittoria; Rossi Giacomina; Giaccone Giorgio; Fede Giuseppe Di; Caroppo Paola; Tiraboschi Pietro; Prioni Sara; Redaelli Veronica; Tang-Wai David; Rogaeva Ekaterina; Castelo-Branco Miguel; Freedman Morris; Keren Ron; Black Sandra; Mitchell Sara; Shoesmith Christen; Bartha Robart; Rademakers Rosa; Poos Jackie; Papma Janne M; Giannini Lucia; Minkelen Rick Van; Pijnenburg Yolande; Nacmias Benedetta; Ferrari Camilla; Polito Cristina; Lombardi Gemma; Bessi Valentina; Veldsman Michele; Andersson Christin; Thonberg Hakan; Öijerstedt Linn; Jelic Vesna; Thompson Paul; Langheinrich Tobias; Lladó Albert; Antonell Anna; Olives Jaume; Balasa Mircea; Bargalló Nuria; Borrego-Ecija Sergi; Verdelho Ana; Maruta Carolina; Ferreira Catarina B; Miltenberger Gabriel; Couto Frederico Simões Do; Gabilondo Alazne; Gorostidi Ana; Villanua Jorge; Cañada Marta; Tainta Mikel; Zulaica Miren; Barandiaran Myriam; Alves Patricia; Bender Benjamin; Wilke Carlo; Graf Lisa; Vogels Annick; Vandenbulcke Mathieu; Damme Philip Van; Bruffaerts Rose; Poesen Koen; Rosa-Neto Pedro; Gauthier Serge; Camuzat Agnès; Brice Alexis; Bertrand Anne; Funkiewiez Aurélie; Rinaldi Daisy; Saracino Dario; Colliot Olivier; Sayah Sabrina; Prix Catharina; Wlasich Elisabeth; Wagemann Olivia; Loosli Sandra; Schönecker Sonja; Hoegen Tobias; Lombardi Jolina; Anderl-Straub Sarah; Rollin Adeline; Kuchcinski Gregory; Bertoux Maxime; Lebouvier Thibaud; Deramecourt Vincent; Santiago Beatriz; Duro Diana; Leitão Maria João; Almeida Maria Rosario; Tábuas-Pereira Miguel; Afonso Sónia; Engel Annerose; Polyakova Maryna

doi:10.1002/hbm.26220

Journal Articles Human Brain Mapping Year : 2023

Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia

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Aurélie Bussy

Function : Author
PersonId : 1368611
ORCID : 0000-0001-6695-9941

Jake P Levy

Function : Author

Tristin Best

Function : Author

Raihaan Patel

Function : Author

Lani Cupo

Function : Author

Tim van Langenhove

Function : Author

Jørgen E Nielsen

Function : Author
PersonId : 1368612
ORCID : 0000-0003-0453-5582

Yolande Pijnenburg

Function : Author

Maria Landqvist Waldö

Function : Author

Anne M Remes

Function : Author

Matthias L Schroeter

Function : Author

Isabel Santana

Function : Author

Florence Pasquier

Function : Author

Equipe Alzheimer and Tauopathies - LilNCog

Excellence Laboratory LabEx DISTALZ

Markus Otto

Function : Author

Adrian Danek

Function : Author

Johannes Levin

Function : Author

Isabelle Le Ber

Function : Author

Institut du Cerveau = Paris Brain Institute

Rik Vandenberghe

Function : Author

Matthis Synofzik

Function : Author

Fermin Moreno

Function : Author

Alexandre de Mendonça

Function : Author

Raquel Sanchez‐valle

Function : Author

Robert Laforce

Function : Author

Tobias Langheinrich

Function : Author

Alexander Gerhard

Function : Author

Caroline Graff

Function : Author

Chris R Butler

Function : Author

Sandro Sorbi

Function : Author

Lize Jiskoot

Function : Author

Harro Seelaar

Function : Author

John C van Swieten

Function : Author

Elizabeth Finger

Function : Author

Maria Carmela Tartaglia

Function : Author

Mario Masellis

Function : Author

Pietro Tiraboschi

Function : Author

Daniela Galimberti

Function : Author

Barbara Borroni

Function : Author
PersonId : 1336812
ORCID : 0000-0001-9340-9814

James B Rowe

Function : Author

Martina Bocchetta

Function : Author
PersonId : 1363148
ORCID : 0000-0003-1814-5024

Jonathan D Rohrer

Function : Author

Gabriel A Devenyi

Function : Author
PersonId : 1302853
ORCID : 0000-0002-7766-1187

M Mallar Chakravarty

Function : Author

Simon Ducharme

Function : Author
PersonId : 1368613

Esteve Aitana Sogorb

Function : Author

Nelson Annabel

Function : Author

Bouzigues Arabella

Function : Author

Heller Carolin

Function : Author

Greaves Caroline V

Function : Author

Cash David

Function : Author

Thomas David L

Function : Author

Todd Emily

Function : Author

Benotmane Hanya

Function : Author

Zetterberg Henrik

Function : Author

Swift Imogen J

Function : Author

Nicholas Jennifer

Function : Author

Samra Kiran

Function : Author

Russell Lucy L

Function : Author

Bocchetta Martina

Function : Author

Shafei Rachelle

Function : Author

Convery Rhian S

Function : Author

Timberlake Carolyn

Function : Author

Cope Thomas

Function : Author

Rittman Timothy

Function : Author

Benussi Alberto

Function : Author

Premi Enrico

Function : Author

Gasparotti Roberto

Function : Author

Archetti Silvana

Function : Author

Gazzina Stefano

Function : Author

Cantoni Valentina

Function : Author

Arighi Andrea

Function : Author

Fenoglio Chiara

Function : Author

Scarpini Elio

Function : Author

Fumagalli Giorgio

Function : Author

Borracci Vittoria

Function : Author

Rossi Giacomina

Function : Author

Giaccone Giorgio

Function : Author

Fede Giuseppe Di

Function : Author

Caroppo Paola

Function : Author

Tiraboschi Pietro

Function : Author

Prioni Sara

Function : Author

Redaelli Veronica

Function : Author

Tang-Wai David

Function : Author

Rogaeva Ekaterina

Function : Author

Castelo-Branco Miguel

Function : Author

Freedman Morris

Function : Author

Keren Ron

Function : Author

Black Sandra

Function : Author

Mitchell Sara

Function : Author

Shoesmith Christen

Function : Author

Bartha Robart

Function : Author

Rademakers Rosa

Function : Author

Poos Jackie

Function : Author

Papma Janne M

Function : Author

Giannini Lucia

Function : Author

Minkelen Rick Van

Function : Author

Pijnenburg Yolande

Function : Author

Nacmias Benedetta

Function : Author

Ferrari Camilla

Function : Author

Polito Cristina

Function : Author

Lombardi Gemma

Function : Author

Bessi Valentina

Function : Author

Veldsman Michele

Function : Author

Andersson Christin

Function : Author

Thonberg Hakan

Function : Author

Öijerstedt Linn

Function : Author

Jelic Vesna

Function : Author

Thompson Paul

Function : Author

Langheinrich Tobias

Function : Author

Lladó Albert

Function : Author

Antonell Anna

Function : Author

Olives Jaume

Function : Author

Balasa Mircea

Function : Author

Bargalló Nuria

Function : Author

Borrego-Ecija Sergi

Function : Author

Verdelho Ana

Function : Author

Maruta Carolina

Function : Author

Ferreira Catarina B

Function : Author

Miltenberger Gabriel

Function : Author

Couto Frederico Simões Do

Function : Author

Gabilondo Alazne

Function : Author

Gorostidi Ana

Function : Author

Villanua Jorge

Function : Author

Cañada Marta

Function : Author

Tainta Mikel

Function : Author

Zulaica Miren

Function : Author

Barandiaran Myriam

Function : Author

Alves Patricia

Function : Author

Bender Benjamin

Function : Author

Wilke Carlo

Function : Author

Graf Lisa

Function : Author

Vogels Annick

Function : Author

Vandenbulcke Mathieu

Function : Author

Damme Philip Van

Function : Author

Bruffaerts Rose

Function : Author

Poesen Koen

Function : Author

Rosa-Neto Pedro

Function : Author

Gauthier Serge

Function : Author

Camuzat Agnès

Function : Author

Institut du Cerveau = Paris Brain Institute

Brice Alexis

Function : Author

Institut du Cerveau = Paris Brain Institute

Bertrand Anne

Function : Author

Institut du Cerveau = Paris Brain Institute

Funkiewiez Aurélie

Function : Author

Institut du Cerveau = Paris Brain Institute

Rinaldi Daisy

Function : Author

Institut du Cerveau = Paris Brain Institute

Saracino Dario

Function : Author

Institut du Cerveau = Paris Brain Institute

Colliot Olivier

Function : Author

Institut du Cerveau = Paris Brain Institute

Sayah Sabrina

Function : Author

Institut du Cerveau = Paris Brain Institute

Prix Catharina

Function : Author

Wlasich Elisabeth

Function : Author

Wagemann Olivia

Function : Author

Loosli Sandra

Function : Author

Schönecker Sonja

Function : Author

Hoegen Tobias

Function : Author

Lombardi Jolina

Function : Author

Anderl-Straub Sarah

Function : Author

Rollin Adeline

Function : Author

Kuchcinski Gregory

Function : Author

Bertoux Maxime

Function : Author

Lebouvier Thibaud

Function : Author

Deramecourt Vincent

Function : Author

Santiago Beatriz

Function : Author

Duro Diana

Function : Author

Leitão Maria João

Function : Author

Almeida Maria Rosario

Function : Author

Tábuas-Pereira Miguel

Function : Author

Afonso Sónia

Function : Author

Engel Annerose

Function : Author

Polyakova Maryna

Function : Author

Abstract

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.

Keywords

frontotemporal dementia genetics magnetic resonance imaging neuropsychiatry

Domains

Neurons and Cognition [q-bio.NC] Human genetics

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Human Brain Mapping - 2023 - Bussy - Cerebellar and subcortical atrophy contribute to psychiatric symptoms in.pdf (10.57 Mo)

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https://hal.sorbonne-universite.fr/hal-04523731

Submitted on : Wednesday, March 27, 2024-4:02:03 PM

Last modification on : Monday, June 3, 2024-4:24:03 PM

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hal-04523731 , version 1 (27-03-2024)

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Attribution - NonCommercial - NoDerivatives

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HAL Id : hal-04523731 , version 1
DOI : 10.1002/hbm.26220
PUBMED : 36895129

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Aurélie Bussy, Jake P Levy, Tristin Best, Raihaan Patel, Lani Cupo, et al.. Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia. Human Brain Mapping, 2023, 44, pp.2684 - 2700. ⟨10.1002/hbm.26220⟩. ⟨hal-04523731⟩

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Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia

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