The Role of Hub and Spoke Regions in Theory of Mind in Early Alzheimer's Disease and Frontotemporal Dementia.

18F-FDG-PET Alzheimer’s disease brain network dementia frontotemporal dementia mild cognitive impairment neurodegenerative diseases neuroimaging social cognition theory of mind

Journal

Biomedicines
ISSN: 2227-9059
Titre abrégé: Biomedicines
Pays: Switzerland
ID NLM: 101691304

Informations de publication

Date de publication:
24 Feb 2022
Historique:
received: 11 10 2021
revised: 04 02 2022
accepted: 20 02 2022
entrez: 25 3 2022
pubmed: 26 3 2022
medline: 26 3 2022
Statut: epublish

Résumé

Theory of mind (ToM, the ability to attribute mental states to others) deficit is a frequent finding in neurodegenerative conditions, mediated by a diffuse brain network confirmed by 18F-FDG-PET and MR imaging, involving frontal, temporal and parietal areas. However, the role of hubs and spokes network regions in ToM performance, and their respective damage, is still unclear. To study this mechanism, we combined ToM testing with brain 18F-FDG-PET imaging in 25 subjects with mild cognitive impairment due to Alzheimer’s disease (MCI−AD), 24 subjects with the behavioral variant of frontotemporal dementia (bvFTD) and 40 controls. Regions included in the ToM network were divided into hubs and spokes based on their structural connectivity and distribution of hypometabolism. The hubs of the ToM network were identified in frontal regions in both bvFTD and MCI−AD patients. A mediation analysis revealed that the impact of spokes damage on ToM performance was mediated by the integrity of hubs (p < 0.001), while the impact of hubs damage on ToM performance was independent from the integrity of spokes (p < 0.001). Our findings support the theory that a key role is played by the hubs in ToM deficits, suggesting that hubs could represent a final common pathway leading from the damage of spoke regions to clinical deficits.

Identifiants

pubmed: 35327346
pii: biomedicines10030544
doi: 10.3390/biomedicines10030544
pmc: PMC8945345
pii:
doi:

Types de publication

Journal Article

Langues

eng

Subventions

Organisme : Italian Ministry of Health Fondi per la Ricerca corrente
ID : 2019/2020

Références

Eur J Nucl Med Mol Imaging. 2009 Dec;36(12):2103-10
pubmed: 19838705
J Neuropsychol. 2020 Sep;14(3):399-415
pubmed: 32212244
Biomedicines. 2021 Jan 16;9(1):
pubmed: 33467174
Trends Cogn Sci. 2013 Dec;17(12):683-96
pubmed: 24231140
Neurology. 2015 Sep 29;85(13):1115-22
pubmed: 26320199
Cogn Neuropsychiatry. 2004 Nov;9(4):301-13
pubmed: 16571588
Mov Disord. 2010 Jan 15;25(1):13-27
pubmed: 19908307
Soc Neurosci. 2020 Oct;15(5):544-557
pubmed: 32378482
Biomedicines. 2021 May 06;9(5):
pubmed: 34066395
Alzheimers Dement. 2018 Apr;14(4):535-562
pubmed: 29653606
Brain. 2012 Oct;135(Pt 10):3026-38
pubmed: 23065791
Exp Aging Res. 2009 Jan-Mar;35(1):98-106
pubmed: 19173104
Mol Psychiatry. 2021 Oct 20;:
pubmed: 34667263
Curr Alzheimer Res. 2017;14(9):937-950
pubmed: 28290245
Hum Brain Mapp. 2008 Jul;29(7):802-9
pubmed: 18438885
Biomedicines. 2021 Apr 01;9(4):
pubmed: 33916324
Neuroinformatics. 2014 Oct;12(4):575-93
pubmed: 24952892
Exp Brain Res. 2020 Sep;238(9):2009-2018
pubmed: 32617883
Alzheimers Dement. 2011 May;7(3):270-9
pubmed: 21514249
Cortex. 2020 Sep;130:401-412
pubmed: 32755727
Brain. 2001 Mar;124(Pt 3):600-16
pubmed: 11222459
Neuropsychologia. 2011 Sep;49(11):2971-84
pubmed: 21803062
Nature. 2000 Jul 27;406(6794):378-82
pubmed: 10935628
Front Psychol. 2015 Oct 31;6:1610
pubmed: 26582995
Am J Geriatr Psychiatry. 2020 Jul;28(7):755-763
pubmed: 31928846
PeerJ. 2019 Nov 29;7:e8170
pubmed: 31803543
Neurosci Biobehav Rev. 2016 Jun;65:276-91
pubmed: 27073047
Neuropsychologia. 2003;41(12):1574-82
pubmed: 12887982
Brain Res. 2018 Jan 1;1678:262-272
pubmed: 29079506
Stroke. 2019 Oct;50(10):2768-2774
pubmed: 31743084
J Neurol Neurosurg Psychiatry. 2013 Jul;84(7):818-21
pubmed: 23117487
J Clin Exp Neuropsychol. 2020 Apr;42(3):223-239
pubmed: 31902277
Biomedicines. 2021 Mar 26;9(4):
pubmed: 33810484
Cereb Cortex. 2013 Oct;23(10):2380-93
pubmed: 22875861
Brain Res Brain Res Rev. 2003 Sep;43(1):29-40
pubmed: 14499460
Brain. 2014 Apr;137(Pt 4):1241-53
pubmed: 24523434
J Geriatr Psychiatry Neurol. 2017 May;30(3):140-150
pubmed: 28355945
J Child Psychol Psychiatry. 2001 Feb;42(2):241-51
pubmed: 11280420
J Neurosci. 2009 Jun 10;29(23):7619-24
pubmed: 19515930
Biomedicines. 2021 Mar 27;9(4):
pubmed: 33801765
Neurosci Biobehav Rev. 2014 May;42:9-34
pubmed: 24486722
Biomedicines. 2021 Apr 10;9(4):
pubmed: 33920310
Schizophr Res. 2008 Oct;105(1-3):165-74
pubmed: 18774263
Gigascience. 2018 Mar 1;7(3):1-17
pubmed: 29432527
Neurosci Biobehav Rev. 2018 Jan;84:92-99
pubmed: 29175518
J Neurosci. 2019 Dec 11;39(50):9878-9882
pubmed: 31676604
Neuroimage. 2020 Aug 15;217:116929
pubmed: 32413461
Cortex. 2014 Sep;58:9-17
pubmed: 24946302
Ann N Y Acad Sci. 2008 Mar;1124:1-38
pubmed: 18400922
Soc Cogn Affect Neurosci. 2015 May;10(5):619-27
pubmed: 25062837
Alzheimer Dis Assoc Disord. 2007 Oct-Dec;21(4):S14-8
pubmed: 18090417
Brain Sci. 2021 Sep 13;11(9):
pubmed: 34573224
Brain Res. 2018 Jan 1;1678:116-122
pubmed: 29066367
Front Neurorobot. 2020 Aug 28;14:60
pubmed: 32982714
Int J Mol Sci. 2021 Nov 30;22(23):
pubmed: 34884804

Auteurs

Beatrice Orso (B)

Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI), University of Genoa, Largo Daneo 3, 16132 Genoa, Italy.
Department of Radiology and Nuclear Medicine, Amsterdam UMC Location VuMC, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, The Netherlands.

Luigi Lorenzini (L)

Department of Radiology and Nuclear Medicine, Amsterdam UMC Location VuMC, Amsterdam Neuroscience, Vrije Universiteit Amsterdam, 1081 HV Amsterdam, The Netherlands.

Dario Arnaldi (D)

Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI), University of Genoa, Largo Daneo 3, 16132 Genoa, Italy.
IRCCS Ospedale Policlinico S. Martino, Largo Rosanna Benzi 10, 16132 Genoa, Italy.

Nicola Girtler (N)

Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI), University of Genoa, Largo Daneo 3, 16132 Genoa, Italy.
IRCCS Ospedale Policlinico S. Martino, Largo Rosanna Benzi 10, 16132 Genoa, Italy.

Andrea Brugnolo (A)

Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI), University of Genoa, Largo Daneo 3, 16132 Genoa, Italy.
IRCCS Ospedale Policlinico S. Martino, Largo Rosanna Benzi 10, 16132 Genoa, Italy.

Elisa Doglione (E)

IRCCS Ospedale Policlinico S. Martino, Largo Rosanna Benzi 10, 16132 Genoa, Italy.

Pietro Mattioli (P)

Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI), University of Genoa, Largo Daneo 3, 16132 Genoa, Italy.

Erica Biassoni (E)

Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI), University of Genoa, Largo Daneo 3, 16132 Genoa, Italy.

Federico Massa (F)

Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI), University of Genoa, Largo Daneo 3, 16132 Genoa, Italy.

Enrico Peira (E)

National Institute of Nuclear Physics (INFN), Genoa Section, Via Dodecaneso 33, 16146 Genoa, Italy.

Matteo Bauckneht (M)

IRCCS Ospedale Policlinico S. Martino, Largo Rosanna Benzi 10, 16132 Genoa, Italy.
Department of Health Science (DISSAL), University of Genoa, Via Antonio Pastore 1, 16132 Genoa, Italy.

Maria I Donegani (MI)

IRCCS Ospedale Policlinico S. Martino, Largo Rosanna Benzi 10, 16132 Genoa, Italy.
Department of Health Science (DISSAL), University of Genoa, Via Antonio Pastore 1, 16132 Genoa, Italy.

Silvia Morbelli (S)

IRCCS Ospedale Policlinico S. Martino, Largo Rosanna Benzi 10, 16132 Genoa, Italy.
Department of Health Science (DISSAL), University of Genoa, Via Antonio Pastore 1, 16132 Genoa, Italy.

Flavio Nobili (F)

Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI), University of Genoa, Largo Daneo 3, 16132 Genoa, Italy.
IRCCS Ospedale Policlinico S. Martino, Largo Rosanna Benzi 10, 16132 Genoa, Italy.

Matteo Pardini (M)

Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics, Maternal and Child Health (DINOGMI), University of Genoa, Largo Daneo 3, 16132 Genoa, Italy.
IRCCS Ospedale Policlinico S. Martino, Largo Rosanna Benzi 10, 16132 Genoa, Italy.

Classifications MeSH