Cerebellar and subcortical atrophy contribute to psychiatric symptoms in frontotemporal dementia.
frontotemporal dementia
genetics
magnetic resonance imaging
neuropsychiatry
Journal
Human brain mapping
ISSN: 1097-0193
Titre abrégé: Hum Brain Mapp
Pays: United States
ID NLM: 9419065
Informations de publication
Date de publication:
05 2023
05 2023
Historique:
revised:
18
01
2023
received:
18
08
2022
accepted:
19
01
2023
medline:
13
4
2023
pubmed:
11
3
2023
entrez:
10
3
2023
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 36895129
doi: 10.1002/hbm.26220
pmc: PMC10089095
doi:
Substances chimiques
C9orf72 Protein
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2684-2700Subventions
Organisme : Medical Research Council
ID : MC_UU_00005/12
Pays : United Kingdom
Organisme : Department of Health
ID : BRC149/NS/MH
Pays : United Kingdom
Organisme : Department of Health
ID : BRC-1215-20014
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/K010395/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_U105597119
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M023664/1
Pays : United Kingdom
Organisme : Alzheimer's Society
ID : AS-PG-16-007
Pays : United Kingdom
Organisme : Alzheimer's Society
ID : AS-JF-19a-004-517
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M008525/1
Pays : United Kingdom
Investigateurs
Aitana Sogorb Esteve
(AS)
Annabel Nelson
(A)
Arabella Bouzigues
(A)
Carolin Heller
(C)
Caroline V Greaves
(CV)
David Cash
(D)
David L Thomas
(DL)
Emily Todd
(E)
Hanya Benotmane
(H)
Henrik Zetterberg
(H)
Imogen J Swift
(IJ)
Jennifer Nicholas
(J)
Kiran Samra
(K)
Lucy L Russell
(LL)
Martina Bocchetta
(M)
Rachelle Shafei
(R)
Rhian S Convery
(RS)
Carolyn Timberlake
(C)
Thomas Cope
(T)
Timothy Rittman
(T)
Alberto Benussi
(A)
Enrico Premi
(E)
Roberto Gasparotti
(R)
Silvana Archetti
(S)
Stefano Gazzina
(S)
Valentina Cantoni
(V)
Andrea Arighi
(A)
Chiara Fenoglio
(C)
Elio Scarpini
(E)
Giorgio Fumagalli
(G)
Vittoria Borracci
(V)
Giacomina Rossi
(G)
Giorgio Giaccone
(G)
Giuseppe Di Fede
(G)
Paola Caroppo
(P)
Pietro Tiraboschi
(P)
Sara Prioni
(S)
Veronica Redaelli
(V)
David Tang-Wai
(D)
Ekaterina Rogaeva
(E)
Miguel Castelo-Branco
(M)
Morris Freedman
(M)
Ron Keren
(R)
Sandra Black
(S)
Sara Mitchell
(S)
Christen Shoesmith
(C)
Robart Bartha
(R)
Rosa Rademakers
(R)
Jackie Poos
(J)
Janne M Papma
(JM)
Lucia Giannini
(L)
Rick van Minkelen
(R)
Yolande Pijnenburg
(Y)
Benedetta Nacmias
(B)
Camilla Ferrari
(C)
Cristina Polito
(C)
Gemma Lombardi
(G)
Valentina Bessi
(V)
Michele Veldsman
(M)
Christin Andersson
(C)
Hakan Thonberg
(H)
Linn Öijerstedt
(L)
Vesna Jelic
(V)
Paul Thompson
(P)
Tobias Langheinrich
(T)
Albert Lladó
(A)
Anna Antonell
(A)
Jaume Olives
(J)
Mircea Balasa
(M)
Nuria Bargalló
(N)
Sergi Borrego-Ecija
(S)
Ana Verdelho
(A)
Carolina Maruta
(C)
Catarina B Ferreira
(CB)
Gabriel Miltenberger
(G)
Frederico Simões do Couto
(FS)
Alazne Gabilondo
(A)
Ana Gorostidi
(A)
Jorge Villanua
(J)
Marta Cañada
(M)
Mikel Tainta
(M)
Miren Zulaica
(M)
Myriam Barandiaran
(M)
Patricia Alves
(P)
Benjamin Bender
(B)
Carlo Wilke
(C)
Lisa Graf
(L)
Annick Vogels
(A)
Mathieu Vandenbulcke
(M)
Philip Van Damme
(P)
Rose Bruffaerts
(R)
Koen Poesen
(K)
Pedro Rosa-Neto
(P)
Serge Gauthier
(S)
Agnès Camuzat
(A)
Alexis Brice
(A)
Anne Bertrand
(A)
Aurélie Funkiewiez
(A)
Daisy Rinaldi
(D)
Dario Saracino
(D)
Olivier Colliot
(O)
Sabrina Sayah
(S)
Catharina Prix
(C)
Elisabeth Wlasich
(E)
Olivia Wagemann
(O)
Sandra Loosli
(S)
Sonja Schönecker
(S)
Tobias Hoegen
(T)
Jolina Lombardi
(J)
Sarah Anderl-Straub
(S)
Adeline Rollin
(A)
Gregory Kuchcinski
(G)
Maxime Bertoux
(M)
Thibaud Lebouvier
(T)
Vincent Deramecourt
(V)
Beatriz Santiago
(B)
Diana Duro
(D)
Maria João Leitão
(MJ)
Maria Rosario Almeida
(MR)
Miguel Tábuas-Pereira
(M)
Sónia Afonso
(S)
Annerose Engel
(A)
Maryna Polyakova
(M)
Informations de copyright
© 2023 The Authors. Human Brain Mapping published by Wiley Periodicals LLC.
Références
Neuroimage Clin. 2021;29:102540
pubmed: 33418170
Sci Rep. 2017 Oct 9;7(1):12841
pubmed: 28993670
Neuroimage. 2011 Feb 1;54(3):1786-94
pubmed: 20965257
Nat Neurosci. 2016 Apr;19(4):533-41
pubmed: 27021938
J Neurophysiol. 2011 Nov;106(5):2322-45
pubmed: 21795627
Neuroimage. 2004;23 Suppl 1:S250-63
pubmed: 15501095
Neuroimage. 2011 Feb 1;54(3):2033-44
pubmed: 20851191
Neurology. 2016 May 3;86(18):1736-43
pubmed: 27037234
PLoS One. 2015 Jul 31;10(7):e0133402
pubmed: 26230510
Hum Brain Mapp. 2023 May;44(7):2684-2700
pubmed: 36895129
Brain. 2014 Nov;137(Pt 11):3047-60
pubmed: 25273996
Neuroimage. 2001 Sep;14(3):595-606
pubmed: 11506533
Brain. 2007 Apr;130(Pt 4):1159-66
pubmed: 17353226
Front Public Health. 2015 May 05;3:66
pubmed: 26000269
Ann Neurol. 2018 Jul;84(1):98-109
pubmed: 30014499
Brain Behav. 2017 Sep 14;7(10):e00807
pubmed: 29075567
J Neurol. 2019 Aug;266(8):2075-2086
pubmed: 31119452
Neuroimage Clin. 2016 Feb 21;11:287-290
pubmed: 26977398
J Neuropsychiatry Clin Neurosci. 2017 Summer;29(3):195-205
pubmed: 28238272
J Alzheimers Dis. 2018;65(1):147-163
pubmed: 30010122
Annu Rev Neurosci. 2002;25:563-93
pubmed: 12052921
Neurobiol Stress. 2022 Jan 14;17:100429
pubmed: 35146077
Front Syst Neurosci. 2013 Jul 16;7:32
pubmed: 23882191
Neurobiol Aging. 2018 Feb;62:191-196
pubmed: 29172163
Annu Rev Psychol. 2013;64:499-525
pubmed: 22804773
Neurobiol Aging. 2022 Mar;111:54-63
pubmed: 34968832
Neuroimage. 2009 May 15;46(1):39-46
pubmed: 19457380
Neuroimage Clin. 2021;30:102646
pubmed: 33895632
Neuropsychol Rev. 2019 Dec;29(4):450-464
pubmed: 31428914
Neuroimage. 2020 Feb 15;207:116348
pubmed: 31715254
Elife. 2018 Aug 14;7:
pubmed: 30106371
Brain. 2017 Dec 1;140(12):3357-3377
pubmed: 29112719
Neuroimage. 2019 Apr 15;190:69-78
pubmed: 29277406
Neurobiol Aging. 2021 Oct;106:153-168
pubmed: 34280848
J Neurol Neurosurg Psychiatry. 2020 Sep;91(9):975-984
pubmed: 32769115
J Alzheimers Dis. 2012;30(4):857-74
pubmed: 22466003
JAMA Neurol. 2018 Feb 1;75(2):236-245
pubmed: 29197216
Lancet Neurol. 2015 Mar;14(3):253-62
pubmed: 25662776
JAMA Netw Open. 2021 Jan 4;4(1):e2030194
pubmed: 33404617
Dement Geriatr Cogn Disord. 2008;25(3):206-11
pubmed: 18204254
Neurology. 2009 May 5;72(18):1562-9
pubmed: 19414722
Brain Imaging Behav. 2021 Oct;15(5):2540-2551
pubmed: 33587281
Brain. 2009 Sep;132(Pt 9):2579-92
pubmed: 19439421
Ann Neurol. 2020 Jul;88(1):113-122
pubmed: 32285980
Neuroimage. 2006 Oct 15;33(1):127-38
pubmed: 16904911
Neuroimage. 2018 May 15;172:437-449
pubmed: 29408539
Lancet Neurol. 2020 Feb;19(2):145-156
pubmed: 31810826
J Neurosci. 2007 Aug 1;27(31):8161-5
pubmed: 17670959
Neurology. 2012 Sep 4;79(10):1002-11
pubmed: 22875087