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Journal Articles Human Brain Mapping Year : 2023

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 (1, 2) , Markus Otto , Adrian Danek , Johannes Levin , Isabelle Le Ber (3) , 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 (3) , Brice Alexis (3) , Bertrand Anne (3) , Funkiewiez Aurélie (3) , Rinaldi Daisy (3) , Saracino Dario (3) , Colliot Olivier (3) , Sayah Sabrina (3) , 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
Aurélie Bussy
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
Yolande Pijnenburg
  • Function : Author
Maria Landqvist Waldö
  • Function : Author
Anne M Remes
  • Function : Author
Matthias L Schroeter
  • Function : Author
Isabel Santana
  • Function : Author
Markus Otto
  • Function : Author
Adrian Danek
  • Function : Author
Johannes Levin
  • Function : Author
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
James B Rowe
  • Function : Author
Martina Bocchetta
Jonathan D Rohrer
  • Function : Author
Gabriel A Devenyi
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
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.
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hal-04523731 , version 1 (27-03-2024)

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Attribution - NonCommercial - NoDerivatives

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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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