Cortical gray matter progression in idiopathic REM sleep behavior disorder and its relation to cognitive decline.


Journal

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

Informations de publication

Date de publication:
2020
Historique:
received: 10 05 2020
revised: 04 09 2020
accepted: 06 09 2020
pubmed: 22 9 2020
medline: 29 6 2021
entrez: 21 9 2020
Statut: ppublish

Résumé

Idiopathic Rapid eye movement sleep behavior disorder (IRBD) is recognized as the prodromal stage of the alpha-Synucleinopathies. Although some studies have addressed the characterization of brain structure in IRBD, little is known about its progression. The present work aims at further characterizing gray matter progression throughout IRBD relative to normal aging and investigating how these changes are associated with cognitive decline. Fourteen patients with polysomnography-confirmed IRBD and 18 age-matched healthy controls (HC) underwent neuropsychological, olfactory, motor, and T1-weighted MRI evaluation at baseline and follow-up. We compared the evolution of cortical thickness (CTh), subcortical volumes, smell, motor and cognitive performance in IRBD and HC after a mean of 1.6 years. FreeSurfer was used for CTh and volumetry preprocessing and analyses. The symmetrized percent of change (SPC) of the CTh was correlated with the SPC of motor and neuropsychological performance. IRBD and HC differed significantly in the cortical thinning progression in regions encompassing bilateral superior parietal and precuneus, the right cuneus, the left occipital pole and lateral orbitofrontal gyri (FWE corrected, p < 0.05). The Visual form discrimination test showed worse progression in the IRBD relative to HC, that was associated with gray matter loss in the right superior parietal and the left precuneus. Increasing motor signs in IRBD were related to cortical thinning mainly involving frontal regions, and late-onset IRBD was associated with cortical thinning involving posterior areas (FWE corrected, p < 0.05). Despite finding olfactory identification deficits in IRBD, results did not show decline over the disease course. Progression in IRBD patients is characterized by parieto-occipital and orbitofrontal thinning and visuospatial loss. The cognitive decline in IRBD is associated with degeneration in parietal regions.

Sections du résumé

BACKGROUND
Idiopathic Rapid eye movement sleep behavior disorder (IRBD) is recognized as the prodromal stage of the alpha-Synucleinopathies. Although some studies have addressed the characterization of brain structure in IRBD, little is known about its progression.
OBJECTIVE
The present work aims at further characterizing gray matter progression throughout IRBD relative to normal aging and investigating how these changes are associated with cognitive decline.
METHODS
Fourteen patients with polysomnography-confirmed IRBD and 18 age-matched healthy controls (HC) underwent neuropsychological, olfactory, motor, and T1-weighted MRI evaluation at baseline and follow-up. We compared the evolution of cortical thickness (CTh), subcortical volumes, smell, motor and cognitive performance in IRBD and HC after a mean of 1.6 years. FreeSurfer was used for CTh and volumetry preprocessing and analyses. The symmetrized percent of change (SPC) of the CTh was correlated with the SPC of motor and neuropsychological performance.
RESULTS
IRBD and HC differed significantly in the cortical thinning progression in regions encompassing bilateral superior parietal and precuneus, the right cuneus, the left occipital pole and lateral orbitofrontal gyri (FWE corrected, p < 0.05). The Visual form discrimination test showed worse progression in the IRBD relative to HC, that was associated with gray matter loss in the right superior parietal and the left precuneus. Increasing motor signs in IRBD were related to cortical thinning mainly involving frontal regions, and late-onset IRBD was associated with cortical thinning involving posterior areas (FWE corrected, p < 0.05). Despite finding olfactory identification deficits in IRBD, results did not show decline over the disease course.
CONCLUSION
Progression in IRBD patients is characterized by parieto-occipital and orbitofrontal thinning and visuospatial loss. The cognitive decline in IRBD is associated with degeneration in parietal regions.

Identifiants

pubmed: 32957013
pii: S2213-1582(20)30258-8
doi: 10.1016/j.nicl.2020.102421
pmc: PMC7509231
pii:
doi:

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

102421

Informations de copyright

Copyright © 2020 The Authors. Published by Elsevier Inc. All rights reserved.

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Auteurs

A Campabadal (A)

Medical Psychology Unit, Department of Medicine, Institute of Neuroscience, University of Barcelona, Barcelona, Catalonia, Spain; Institute of Biomedical Research August Pi i Sunyer (IDIBAPS), Barcelona, Catalonia, Spain.

A Inguanzo (A)

Medical Psychology Unit, Department of Medicine, Institute of Neuroscience, University of Barcelona, Barcelona, Catalonia, Spain; Institute of Biomedical Research August Pi i Sunyer (IDIBAPS), Barcelona, Catalonia, Spain.

B Segura (B)

Medical Psychology Unit, Department of Medicine, Institute of Neuroscience, University of Barcelona, Barcelona, Catalonia, Spain; Institute of Biomedical Research August Pi i Sunyer (IDIBAPS), Barcelona, Catalonia, Spain; Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED:CB06/05/0018-ISCIII), Barcelona, Spain.

M Serradell (M)

Institute of Biomedical Research August Pi i Sunyer (IDIBAPS), Barcelona, Catalonia, Spain; Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED:CB06/05/0018-ISCIII), Barcelona, Spain; Sleep Disorders Center, Neurology Service, Hospital Clínic, Barcelona, Catalonia, Spain.

A Abos (A)

Medical Psychology Unit, Department of Medicine, Institute of Neuroscience, University of Barcelona, Barcelona, Catalonia, Spain.

C Uribe (C)

Medical Psychology Unit, Department of Medicine, Institute of Neuroscience, University of Barcelona, Barcelona, Catalonia, Spain.

C Gaig (C)

Institute of Biomedical Research August Pi i Sunyer (IDIBAPS), Barcelona, Catalonia, Spain; Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED:CB06/05/0018-ISCIII), Barcelona, Spain; Sleep Disorders Center, Neurology Service, Hospital Clínic, Barcelona, Catalonia, Spain.

J Santamaria (J)

Institute of Biomedical Research August Pi i Sunyer (IDIBAPS), Barcelona, Catalonia, Spain; Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED:CB06/05/0018-ISCIII), Barcelona, Spain; Sleep Disorders Center, Neurology Service, Hospital Clínic, Barcelona, Catalonia, Spain.

Y Compta (Y)

Institute of Biomedical Research August Pi i Sunyer (IDIBAPS), Barcelona, Catalonia, Spain; Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED:CB06/05/0018-ISCIII), Barcelona, Spain; Parkinson's Disease & Movement Disorders Unit, Neurology Service, Hospital Clínic de Barcelona, Institute of Neuroscience, University of Barcelona, Barcelona, Catalonia, Spain.

N Bargallo (N)

Centre de Diagnòstic per la Imatge, Hospital Clínic, Barcelona, Catalonia, Spain.

C Junque (C)

Medical Psychology Unit, Department of Medicine, Institute of Neuroscience, University of Barcelona, Barcelona, Catalonia, Spain; Institute of Biomedical Research August Pi i Sunyer (IDIBAPS), Barcelona, Catalonia, Spain; Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED:CB06/05/0018-ISCIII), Barcelona, Spain. Electronic address: cjunque@ub.edu.

A Iranzo (A)

Institute of Biomedical Research August Pi i Sunyer (IDIBAPS), Barcelona, Catalonia, Spain; Centro de Investigación Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED:CB06/05/0018-ISCIII), Barcelona, Spain; Sleep Disorders Center, Neurology Service, Hospital Clínic, Barcelona, Catalonia, Spain.

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