Association between insomnia and cognitive performance, gray matter volume, and white matter microstructure in cognitively unimpaired adults

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  • dc.contributor.author Grau-Rivera, Oriol
  • dc.contributor.author Operto, Grégory
  • dc.contributor.author Falcón, Carles
  • dc.contributor.author Sánchez Benavides, Gonzalo
  • dc.contributor.author Cacciaglia, Raffaele
  • dc.contributor.author Brugulat Serrat, Anna, 1986-
  • dc.contributor.author Gramunt Fombuena, Nina
  • dc.contributor.author Salvadó, Gemma
  • dc.contributor.author Suárez-Calvet, Marc
  • dc.contributor.author Minguillón, Carolina
  • dc.contributor.author Iranzo, Alex
  • dc.contributor.author Gispert López, Juan Domingo
  • dc.contributor.author Molinuevo, José Luis
  • dc.contributor.author ALFA Study
  • dc.date.accessioned 2020-04-15T07:21:33Z
  • dc.date.available 2020-04-15T07:21:33Z
  • dc.date.issued 2020
  • dc.description.abstract Background: Mounting evidence links poor sleep quality with a higher risk of late-life dementia. However, the structural and cognitive correlates of insomnia are still not well understood. The study aims were to characterize the cognitive performance and brain structural pattern of cognitively unimpaired adults at increased risk for Alzheimer’s disease (AD) with insomnia. Methods: This cross-sectional study included 1683 cognitively unimpaired middle/late-middle-aged adults from the ALFA (ALzheimer and FAmilies) study who underwent neuropsychological assessment, T1-weighted structural imaging (n = 366), and diffusion-weighted imaging (n = 334). The World Health Organization’s World Mental Health Survey Initiative version of the Composite International Diagnostic Interview was used to define the presence or absence of insomnia. Multivariable regression models were used to evaluate differences in cognitive performance between individuals with and without insomnia, as well as potential interactions between insomnia and the APOE genotype. Voxel-based morphometry and tract-based spatial statistics were used to assess between-group differences and potential interactions between insomnia and the APOE genotype in gray matter volume and white matter diffusion metrics. Results: Insomnia was reported by 615 out of 1683 participants (36.5%), including 137 out of 366 (37.4%) with T1-weighted structural imaging available and 119 out of 334 (35.6%) with diffusion-weighted imaging. Individuals with insomnia (n = 615) performed worse in executive function tests than non-insomniacs and displayed lower gray matter volume in left orbitofrontal and right middle temporal cortex, bilateral precuneus, posterior cingulate cortex and thalamus, higher gray matter volume in the left caudate nucleus, and widespread reduction of mean and axial diffusivity in right hemisphere white matter tracts. Insomnia interacted with the APOE genotype, with APOE-ε4 carriers displaying lower gray matter volumes when insomnia was present, but higher volumes when insomnia was not present, in several gray matter regions, including the left angular gyrus, the bilateral superior frontal gyri, the thalami, and the right hippocampus. Conclusions: Insomnia in cognitively unimpaired adults at increased risk for AD is associated to poorer performance in some executive functions and volume changes in cortical and subcortical gray matter, including key areas involved in Alzheimer’s disease, as well as decreased white matter diffusivity.
  • dc.description.sponsorship The research leading to these results has received funding from “la Caixa” Foundation (LCF/PR/GN17/10300004). OG-R is supported by the Spanish Ministry of Science, Innovation and Universities (FJCI-2017-33437). MS-C receives funding from the European Union’s Horizon 2020 Research and Innovation Program under the Marie Sklodowska-Curie action grant agreement No 752310. CM was supported by the Spanish Ministry of Economy and Competitiveness (grant no. IEDI-2016-00690). Juan D. Gispert holds a “Ramón y Cajal” fellowship (RYC-2013-13054).
  • dc.format.mimetype application/pdf
  • dc.identifier.citation Grau-Rivera O, Operto G, Falcón C, Sánchez-Benavides G, Cacciaglia R, Brugulat-Serrat A, Gramunt N, Salvadó G, Suárez-Calvet M, Minguillon C, Iranzo Á, Gispert JD, Molinuevo JL; ALFA Study. Association between insomnia and cognitive performance, gray matter volume, and white matter microstructure in cognitively unimpaired adults. Alzheimers Res Ther. 2020; 12(1):4. DOI: 10.1186/s13195-019-0547-3
  • dc.identifier.doi http://dx.doi.org/10.1186/s13195-019-0547-3
  • dc.identifier.issn 1758-9193
  • dc.identifier.uri http://hdl.handle.net/10230/44217
  • dc.language.iso eng
  • dc.publisher BioMed Central
  • dc.relation.ispartof Alzheimers Res Ther. 2020; 12(1):4
  • dc.relation.projectID info:eu-repo/grantAgreement/EC/H2020/752310
  • dc.rights © The Author(s). 2020 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
  • dc.rights.accessRights info:eu-repo/semantics/openAccess
  • dc.rights.uri http://creativecommons.org/licenses/by/4.0/
  • dc.subject.keyword Alzheimer disease
  • dc.subject.keyword Diffusion-weighted imaging
  • dc.subject.keyword Inflammation
  • dc.subject.keyword Insomnia
  • dc.subject.keyword Magnetic resonance imaging
  • dc.subject.keyword Neurocognitive disorders
  • dc.subject.keyword Neuropsychology
  • dc.subject.keyword Sleep
  • dc.subject.keyword Voxel-based morphometry
  • dc.title Association between insomnia and cognitive performance, gray matter volume, and white matter microstructure in cognitively unimpaired adults
  • dc.type info:eu-repo/semantics/article
  • dc.type.version info:eu-repo/semantics/publishedVersion