Specific structuro-metabolic pattern of thalamic subnuclei in fatal familial insomnia: A PET/MRI imaging study.

18F-Fluorodeoxyglucose Fatal familial insomnia Magnetic resonance imaging Positron-Emission Tomography Thalamic nuclei

Journal

NeuroImage. Clinical
ISSN: 2213-1582
Titre abrégé: Neuroimage Clin
Pays: Netherlands
ID NLM: 101597070

Informations de publication

Date de publication:
2022
Historique:
received: 04 01 2022
revised: 31 03 2022
accepted: 24 04 2022
pubmed: 4 5 2022
medline: 20 5 2022
entrez: 3 5 2022
Statut: ppublish

Résumé

Dysfunction of the thalamus has been proposed as a core mechanism of fatal familial insomnia. However, detailed metabolic and structural alterations in thalamic subnuclei are not well documented. We aimed to address the multimodal structuro-metabolic pattern at the level of the thalamic nuclei in fatal familial insomnia patients, and investigated the clinical presentation of primary thalamic alterations. Five fatal familial insomnia patients and 10 healthy controls were enrolled in this study. All participants underwent neuropsychological assessments, polysomnography, electroencephalogram, and cerebrospinal fluid tests. MRI and fluorodeoxyglucose PET were acquired on a hybrid PET/MRI system. Structural and metabolic changes were compared using voxel-based morphometry analyses and standardized uptake value ratio analyses, focusing on thalamic subnuclei region of interest analyses. Correlation analysis was conducted between gray matter volume and metabolic decrease ratios, and clinical features. The whole-brain analysis showed that gray matter volume decline was confined to the bilateral thalamus and right middle temporal pole in fatal familial insomnia patients, whereas hypometabolism was observed in the bilateral thalamus, basal ganglia, and widespread cortices, mainly in the forebrain. In the regions of interest analysis, gray matter volume and metabolism decreases were prominent in bilateral medial dorsal nuclei, anterior nuclei, and the pulvinar, which is consistent with neuropathological and clinical findings. A positive correlation was found between gray matter volume and metabolic decrease ratios. Our study revealed specific structuro-metabolic pattern of fatal familial insomnia that demonstrated the essential roles of medial dorsal nuclei, anterior nuclei, and pulvinar, which may be a potential biomarker in diagnosis. Also, primary thalamic subnuclei alterations may be correlated with insomnia, neuropsychiatric, and autonomic symptoms sparing primary cortical involvement.

Sections du résumé

BACKGROUND
Dysfunction of the thalamus has been proposed as a core mechanism of fatal familial insomnia. However, detailed metabolic and structural alterations in thalamic subnuclei are not well documented. We aimed to address the multimodal structuro-metabolic pattern at the level of the thalamic nuclei in fatal familial insomnia patients, and investigated the clinical presentation of primary thalamic alterations.
MATERIALS AND METHODS
Five fatal familial insomnia patients and 10 healthy controls were enrolled in this study. All participants underwent neuropsychological assessments, polysomnography, electroencephalogram, and cerebrospinal fluid tests. MRI and fluorodeoxyglucose PET were acquired on a hybrid PET/MRI system. Structural and metabolic changes were compared using voxel-based morphometry analyses and standardized uptake value ratio analyses, focusing on thalamic subnuclei region of interest analyses. Correlation analysis was conducted between gray matter volume and metabolic decrease ratios, and clinical features.
RESULTS
The whole-brain analysis showed that gray matter volume decline was confined to the bilateral thalamus and right middle temporal pole in fatal familial insomnia patients, whereas hypometabolism was observed in the bilateral thalamus, basal ganglia, and widespread cortices, mainly in the forebrain. In the regions of interest analysis, gray matter volume and metabolism decreases were prominent in bilateral medial dorsal nuclei, anterior nuclei, and the pulvinar, which is consistent with neuropathological and clinical findings. A positive correlation was found between gray matter volume and metabolic decrease ratios.
CONCLUSIONS
Our study revealed specific structuro-metabolic pattern of fatal familial insomnia that demonstrated the essential roles of medial dorsal nuclei, anterior nuclei, and pulvinar, which may be a potential biomarker in diagnosis. Also, primary thalamic subnuclei alterations may be correlated with insomnia, neuropsychiatric, and autonomic symptoms sparing primary cortical involvement.

Identifiants

pubmed: 35504222
pii: S2213-1582(22)00091-2
doi: 10.1016/j.nicl.2022.103026
pmc: PMC9065920
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

103026

Informations de copyright

Copyright © 2022 The Author(s). Published by Elsevier Inc. All rights reserved.

Références

Infect Genet Evol. 2010 Mar;10(2):292-7
pubmed: 20096809
J Clin Sleep Med. 2013 Dec 15;9(12):1343-5
pubmed: 24340298
Neurology. 1997 Jul;49(1):126-33
pubmed: 9222180
Lancet Neurol. 2017 Jun;16(6):435-444
pubmed: 28456479
Curr Neurol Neurosci Rep. 2017 Apr;17(4):30
pubmed: 28324299
Int J Clin Exp Pathol. 2015 Sep 01;8(9):10171-7
pubmed: 26617725
Neuropsychologia. 2000;38(5):613-27
pubmed: 10689038
Neurology. 1992 Feb;42(2):312-9
pubmed: 1736158
Brain Pathol. 1995 Jan;5(1):43-51
pubmed: 7767490
Acta Neurol Scand. 2018 Aug;138(2):151-155
pubmed: 29569252
Handb Clin Neurol. 2011;99:981-96
pubmed: 21056239
Ann Neurol. 2008 May;63(5):658-61
pubmed: 18360821
Brain. 2019 Apr 1;142(4):1148-1160
pubmed: 30759182
J Alzheimers Dis. 2016 Nov 1;55(1):431-443
pubmed: 27662320
Neuroimage. 2007 Oct 15;38(1):95-113
pubmed: 17761438
Brain. 2006 Mar;129(Pt 3):668-75
pubmed: 16399807
Arch Neurol. 2008 Apr;65(4):545-9
pubmed: 18413481
Chin Med J (Engl). 2018 Jul 5;131(13):1613-1617
pubmed: 29941716
Prion. 2019 Jan;13(1):116-123
pubmed: 31122137
J Pineal Res. 2009 Jan;46(1):1-7
pubmed: 18761566
Seizure. 2012 Apr;21(3):183-7
pubmed: 22209542
Sleep Med. 2010 May;11(5):498-9
pubmed: 20133192
Brain Res Brain Res Rev. 2002 Sep;39(2-3):107-40
pubmed: 12423763
Medicine (Baltimore). 2017 Dec;96(49):e8951
pubmed: 29245265
Neurosci Lett. 1988 Feb 29;85(2):223-7
pubmed: 3374838
Neurosci Biobehav Rev. 2012 Jan;36(1):134-42
pubmed: 21605592
Neuropathol Appl Neurobiol. 2011 Aug;37(5):549-53
pubmed: 20874730
Exp Neurol. 2010 Sep;225(1):154-62
pubmed: 20558163
Sleep Med. 2017 May;33:165-166
pubmed: 28449898
Neurosci Biobehav Rev. 1982 Fall;6(3):351-80
pubmed: 6757808
Clin Nucl Med. 2018 Aug;43(8):e274-e275
pubmed: 29877883
Curr Neurol Neurosci Rep. 2013 Apr;13(4):341
pubmed: 23423537
J Neurophysiol. 2009 Feb;101(2):917-25
pubmed: 19073806

Auteurs

Kexin Xie (K)

Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing 100053, China.

Yaojing Chen (Y)

State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China.

Min Chu (M)

Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing 100053, China.

Yue Cui (Y)

Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing 100053, China.

Zhongyun Chen (Z)

Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing 100053, China.

Jing Zhang (J)

Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing 100053, China.

Li Liu (L)

Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing 100053, China; Department of Neurology, Shenyang Fifth People Hospital, Shenyang, Liaoning 110023, China.

Donglai Jing (D)

Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing 100053, China; Department of Neurology, Rongcheng People's Hospital, Baoding, Hebei 071700, China.

Chunlei Cui (C)

Department of Nuclear Medicine, Xuanwu Hospital, Capital Medical University, Beijing 100053, China.

Zhigang Liang (Z)

Department of Nuclear Medicine, Xuanwu Hospital, Capital Medical University, Beijing 100053, China.

Liankun Ren (L)

Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing 100053, China.

Pedro Rosa-Neto (P)

McGill University Research Centre for Studies in Aging, Montreal, QC H3G 1Y6, Canada.

Imad Ghorayeb (I)

Université de Bordeaux, Institut de Neurosciences Cognitives et Intégratives d'Aquitaine, UMR 5287, F-33076 Bordeaux, France; CNRS, Institut de Neurosciences Cognitives et Intégratives d'Aquitaine, UMR 5287, F-33076 Bordeaux, France; Département de Neurophysiologie Clinique, Pôle Neurosciences Cliniques, CHU de Bordeaux, F-33076 Bordeaux, France.

Zhanjun Zhang (Z)

State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing 100875, China. Electronic address: zhang_rzs@bnu.edu.cn.

Liyong Wu (L)

Department of Neurology, Xuanwu Hospital, Capital Medical University, Beijing 100053, China; National Clinical Research Center for Geriatric Diseases, Beijing 100053, China. Electronic address: wmywly@hotmail.com.

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