Functional network resilience to pathology in presymptomatic genetic frontotemporal dementia.


Journal

Neurobiology of aging
ISSN: 1558-1497
Titre abrégé: Neurobiol Aging
Pays: United States
ID NLM: 8100437

Informations de publication

Date de publication:
05 2019
Historique:
received: 22 02 2018
revised: 23 12 2018
accepted: 24 12 2018
pubmed: 5 3 2019
medline: 18 12 2019
entrez: 5 3 2019
Statut: ppublish

Résumé

The presymptomatic phase of neurodegenerative diseases are characterized by structural brain changes without significant clinical features. We set out to investigate the contribution of functional network resilience to preserved cognition in presymptomatic genetic frontotemporal dementia. We studied 172 people from families carrying genetic abnormalities in C9orf72, MAPT, or PGRN. Networks were extracted from functional MRI data and assessed using graph theoretical analysis. We found that despite loss of both brain volume and functional connections, there is maintenance of an efficient topological organization of the brain's functional network in the years leading up to the estimated age of frontotemporal dementia symptom onset. After this point, functional network efficiency declines markedly. Reduction in connectedness was most marked in highly connected hub regions. Measures of topological efficiency of the brain's functional network and organization predicted cognitive dysfunction in domains related to symptomatic frontotemporal dementia and connectivity correlated with brain volume loss in frontotemporal dementia. We propose that maintaining the efficient organization of the brain's functional network supports cognitive health even as atrophy and connectivity decline presymptomatically.

Identifiants

pubmed: 30831384
pii: S0197-4580(18)30447-0
doi: 10.1016/j.neurobiolaging.2018.12.009
pmc: PMC6491498
pii:
doi:

Substances chimiques

C9orf72 Protein 0
C9orf72 protein, human 0
MAPT protein, human 0
tau Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

169-177

Subventions

Organisme : Medical Research Council
ID : MC_UU_00024/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M008525/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : G1100464
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M023664/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M009041/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 103838
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M018288/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/M024873/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/J009482/1
Pays : United Kingdom

Investigateurs

Sónia Afonso (S)
Maria Rosario Almeida (MR)
Sarah Anderl-Straub (S)
Christin Andersson (C)
Anna Antonell (A)
Silvana Archetti (S)
Andrea Arighi (A)
Mircea Balasa (M)
Myriam Barandiaran (M)
Nuria Bargalló (N)
Robart Bartha (R)
Benjamin Bender (B)
Luisa Benussi (L)
Valentina Bessi (V)
Giuliano Binetti (G)
Sandra Black (S)
Martina Bocchetta (M)
Sergi Borrego-Ecija (S)
Jose Bras (J)
Rose Bruffaerts (R)
Paola Caroppo (P)
David Cash (D)
Miguel Castelo-Branco (M)
Rhian Convery (R)
Thomas Cope (T)
Maura Cosseddu (M)
María de Arriba (M)
Giuseppe Di Fede (G)
Zigor Díaz (Z)
Katrina M Dick (KM)
Diana Duro (D)
Chiara Fenoglio (C)
Camilla Ferrari (C)
Catarina B Ferreira (CB)
Toby Flanagana (T)
Nick Fox (N)
Morris Freedman (M)
Giorgio Fumagalli (G)
Alazne Gabilondo (A)
Roberto Gasparotti (R)
Serge Gauthier (S)
Stefano Gazzina (S)
Roberta Ghidoni (R)
Giorgio Giaccone (G)
Ana Gorostidi (A)
Caroline Greaves (C)
Rita Guerreiro (R)
Carolin Heller (C)
Tobias Hoegen (T)
Begoña Indakoetxea (B)
Vesna Jelic (V)
Lize Jiskoot (L)
Hans-Otto Karnath (HO)
Ron Keren (R)
Maria João Leitão (MJ)
Albert Lladó (A)
Gemma Lombardi (G)
Sandra Loosli (S)
Carolina Maruta (C)
Simon Mead (S)
Lieke Meeter (L)
Gabriel Miltenberger (G)
Rick van Minkelen (R)
Sara Mitchell (S)
Benedetta Nacmias (B)
Mollie Neason (M)
Jennifer Nicholas (J)
Linn Öijerstedt (L)
Jaume Olives (J)
Alessandro Padovani (A)
Jessica Panman (J)
Janne Papma (J)
Michela Pievani (M)
Yolande Pijnenburg (Y)
Enrico Premi (E)
Sara Prioni (S)
Catharina Prix (C)
Rosa Rademakers (R)
Veronica Redaelli (V)
Ekaterina Rogaeva (E)
Pedro Rosa-Neto (P)
Giacomina Rossi (G)
Martin Rosser (M)
Beatriz Santiago (B)
Elio Scarpini (E)
Sonja Schönecker (S)
Elisa Semler (E)
Rachelle Shafei (R)
Christen Shoesmith (C)
Miguel Tábuas-Pereira (M)
Mikel Tainta (M)
Ricardo Taipa (R)
David Tang-Wai (D)
David L Thomas (DL)
Hakan Thonberg (H)
Carolyn Timberlake (C)
Pietro Tiraboschi (P)
Philip Vandamme (P)
Mathieu Vandenbulcke (M)
Michele Veldsman (M)
Ana Verdelho (A)
Jorge Villanua (J)
Jason Warren (J)
Carlo Wilke (C)
Ione Woollacott (I)
Elisabeth Wlasich (E)
Henrik Zetterberg (H)
Miren Zulaica (M)

Informations de copyright

Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.

Références

PLoS One. 2007 Oct 17;2(10):e1049
pubmed: 17940613
Neurobiol Aging. 2009 Jul;30(7):1114-24
pubmed: 18053618
Proc Natl Acad Sci U S A. 2012 Apr 10;109(15):5868-73
pubmed: 22467830
Lancet Neurol. 2006 Oct;5(10):828-34
pubmed: 16987729
Neuron. 2009 Apr 16;62(1):42-52
pubmed: 19376066
Lancet Neurol. 2011 Sep;10(9):829-43
pubmed: 21778116
J Neurosci. 2009 Feb 11;29(6):1860-73
pubmed: 19211893
Cortex. 2013 Oct;49(9):2389-401
pubmed: 23164495
Hum Brain Mapp. 2016 Mar;37(3):1026-37
pubmed: 26757216
Hum Brain Mapp. 2015 Jun;36(6):2248-69
pubmed: 25727740
Parkinsonism Relat Disord. 2011 Sep;17(8):599-605
pubmed: 21665514
J Neurosci. 2006 Jan 4;26(1):63-72
pubmed: 16399673
Lancet Neurol. 2010 Jan;9(1):119-28
pubmed: 20083042
Neurobiol Aging. 2016 Dec;48:153-160
pubmed: 27697694
Ann N Y Acad Sci. 2011 Apr;1224:109-125
pubmed: 21251014
Lancet Neurol. 2016 Jun;15(7):673-684
pubmed: 27068280
JAMA Neurol. 2013 Oct;70(10):1249-53
pubmed: 23959214
Brain. 2018 Feb 1;141(2):550-567
pubmed: 29293892
Proc Natl Acad Sci U S A. 2011 Nov 22;108(47):19066-71
pubmed: 22065778
Proc Natl Acad Sci U S A. 2012 Dec 11;109(50):20608-13
pubmed: 23185007
Brain Struct Funct. 2016 Jan;221(1):115-31
pubmed: 25257603
Biol Psychiatry. 2007 Sep 1;62(5):429-37
pubmed: 17210143
Am J Psychiatry. 2011 Jun;168(6):642-8
pubmed: 21362744
Neuron. 2013 Aug 21;79(4):798-813
pubmed: 23972601
Neuroimage. 2012 Oct 1;62(4):2296-314
pubmed: 22387165
Neurology. 2013 Feb 26;80(9):814-23
pubmed: 23390180
Ann Neurol. 2003 Feb;53(2):181-8
pubmed: 12557284
Neurobiol Aging. 2010 Aug;31(8):1375-85
pubmed: 20447732
Alzheimer Dis Assoc Disord. 2007 Oct-Dec;21(4):S50-7
pubmed: 18090425
Brain. 2010 May;133(Pt 5):1352-67
pubmed: 20410145
Brain. 2009 May;132(Pt 5):1355-65
pubmed: 19339253
PLoS Comput Biol. 2007 Feb 2;3(2):e17
pubmed: 17274684
Brain. 2017 Jun 1;140(6):1784-1791
pubmed: 28460069
Lancet Neurol. 2015 Mar;14(3):253-62
pubmed: 25662776
PLoS Comput Biol. 2010 Nov 18;6(11):e1001006
pubmed: 21124954
Nat Rev Neurosci. 2012 Apr 13;13(5):336-49
pubmed: 22498897
Neurobiol Aging. 2014 Feb;35(2):431-41
pubmed: 24074808
Nat Rev Neurosci. 2018 Nov;19(11):701-710
pubmed: 30305711
Proc Natl Acad Sci U S A. 2011 Oct 4;108(40):16783-8
pubmed: 21930901
Neurology. 2004 Feb 24;62(4):591-600
pubmed: 14981176
Neuropsychologia. 2009 Aug;47(10):2015-28
pubmed: 19467352
Neuroimage Clin. 2015 Aug 07;9:140-52
pubmed: 26413477
NMR Biomed. 1997 Jun-Aug;10(4-5):165-70
pubmed: 9430343
Neuroimage. 2011 Aug 1;57(3):908-17
pubmed: 21609769

Auteurs

Timothy Rittman (T)

Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK. Electronic address: tr332@medschl.cam.ac.uk.

Robin Borchert (R)

Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK.

Simon Jones (S)

Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK.

John van Swieten (J)

Alzheimercentrum, Erasmus Medical Center, Rotterdam, the Netherlands.

Barbara Borroni (B)

Department of Clinical and Experimental Sciences, University of Brescia, Italy.

Daniela Galimberti (D)

Department of Pathophysiology and Transplantation, "Dino Ferrari" Center, University of Milan, Fondazione Cà Granda, IRCCS Ospedale Maggiore Policlinico, Milan, Italy.

Mario Masellis (M)

Cognitive Neurology Research Unit, Sunnybrook Health Sciences Centre, Toronto, Canada; Hurvitz Brain Sciences Research Program, Sunnybrook Research Institute, Toronto, Canada; Department of Medicine, University of Toronto, Toronto, Canada.

Maria Carmela Tartaglia (MC)

Tanz Centre for Research in Neurodegenerative Diseases, University of Toronto, Toronto, Canada.

Caroline Graff (C)

Department NVS, Center for Alzheimer Research, Division of Neurogeriatrics, Karolinska Institutet, Stockholm, Sweden; Department of Geriatric Medicine, Karolinska University Hospital, Stockholm, Sweden.

Fabrizio Tagliavini (F)

Istituto Neurologico Carlo Besta, Milan, Italy.

Giovanni B Frisoni (GB)

Department of Psychiatry, University Hospitals and University of Geneva, Geneva, Switzerland; Neuroimaging and Epidemiology Unit, IRCCS San Giovanni di Dio Fatebenefratelli Brescia, Brescia, Italy.

Robert Laforce (R)

Faculty of Medicine, Université Laval, Quebec, Canada.

Elizabeth Finger (E)

Department of Clinical Neurological Sciences, University of Western Ontario, Ontario, Canada.

Alexandre Mendonça (A)

Faculdade de Medicina, Universidade de Lisboa, Lisboa, Portugal.

Sandro Sorbi (S)

Department of Neurosciences, Psychology, Drug Research and Child Health (NEUROFARBA), University of Florence, Florence, Italy; IRCCS Don Gnocchi, Florence, Italy.

Jonathan D Rohrer (JD)

Dementia Research Centre, Department of Neurodegenerative Disease, UCL Institute of Neurology, Queen Square, London, UK.

James B Rowe (JB)

Department of Clinical Neurosciences, University of Cambridge, Cambridge, UK.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH