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Poor Sleep Quality Associates With Decreased Functional and Structural Brain Connectivity in Normative Aging: A MRI Multimodal Approach

  • Liliana Amorim
  • , Ricardo Magalhães
  • , Ana Coelho
  • , Pedro Silva Moreira
  • , Carlos Portugal-Nunes
  • , Teresa Costa Castanho
  • , Paulo Marques
  • , Nuno Sousa
  • , Nadine Correia Santos
  • University of Minho
  • Clinical Academic Center – Braga

Research output: Contribution to journalArticlepeer-review

37 Citations (Scopus)

Abstract

Sleep is a ubiquitous phenomenon, essential to the organism homeostasis. Notwithstanding, there has been an increasing concern with its disruption, not only within the context of pathological conditions, such as neurologic and psychiatric diseases, but also in health. In fact, sleep complaints are becoming particularly common, especially in middle-aged and older adults, which may suggest an underlying susceptibility to sleep quality loss and/or its consequences. Thus, a whole-brain modeling approach to study the shifts in the system can cast broader light on sleep quality mechanisms and its associated morbidities. Following this line, we sought to determine the association between the standard self-reported measure of sleep quality, the Pittsburgh Sleep Quality Index (PSQI) and brain correlates in a normative aging cohort. To this purpose, 86 participants (age range 52–87 years) provided information regarding sociodemographic parameters, subjective sleep quality and associated psychological variables. A multimodal magnetic resonance imaging (MRI) approach was used, with whole-brain functional and structural connectomes being derived from resting-state functional connectivity (FC) and probabilistic white matter tractography (structural connectivity, SC). Brain regional volumes and white matter properties associations were also explored. Results show that poor sleep quality was associated with a decrease in FC and SC of distinct networks, overlapping in right superior temporal pole, left middle temporal and left inferior occipital regions. Age displayed important associations with volumetric changes in the cerebellum cortex and white matter, thalamus, hippocampus, right putamen, left supramarginal and left lingual regions. Overall, results suggest that not only the PSQI global score may act as a proxy of changes in FC/SC in middle-aged and older individuals, but also that the age-related regional volumetric changes may be associated to an adjustment of brain connectivity. These findings may also represent a step further in the comprehension of the role of sleep disturbance in disease, since the networks found share regions that have been shown to be affected in pathologies, such as depression and Alzheimer's disease.

Original languageEnglish
Article number375
JournalFrontiers in Aging Neuroscience
Volume10
DOIs
Publication statusPublished - 20 Nov 2018
Externally publishedYes

Bibliographical note

Publisher Copyright:
© Copyright © 2018 Amorim, Magalhães, Coelho, Moreira, Portugal-Nunes, Castanho, Marques, Sousa and Santos.

Funding

We would also like to thank Miguel Pais-Vieira for the attentive reading and useful insight on the manuscript. Funding. Financial support was provided by FEDER funds through the Operational Programme Competitiveness Factors-COMPETE and National Funds through FCT-Foundation for Science and Technology under the project POCI-01-0145-FEDER-007038, by the project NORTE-01-0145-FEDER-000013 [supported by the Northern Portugal Regional Operational Programme (NORTE 2020), under the Portugal 2020 (P2020) Partnership Agreement, through the European Regional Development Fund (FEDER)], by POCI-01-0145-FEDER-016428 [supported by the Operational Programme Competitiveness and Internationalization (COMPETE 2020) and the Regional Operational Program of Lisbon and National Funding through Portuguese Foundation for Science and Technology (FCT, Portugal)], and by the Portuguese North Regional Operational Programme [ON.2 – O Novo Norte, under the National Strategic Reference Framework (QREN), through FEDER]. The work was also developed under the scope of the projects SwitchBox (European Commission, FP7; contract HEALTH-F2-2010-259772) and TEMPO-Better mental health during aging based on temporal prediction of individual brain aging trajectories (Fundação Calouste Gulbenkian; Contract grant number P-139977). LA, TC, RM, PSM, and CP-N were supported by FCT PhD scholarships [SFRH/BD/101398/2014 to LA; SFRH/BD/90078/2012 to TC; PDE/BDE/113604/2015 from the PhD-iHES Programme to RM; PDE/BDE/113601/2015 to PSM; PD/BD/106050/2015 from the Inter-University Doctoral Programme in Aging and Chronic Disease (PhDOC) to CP-N] and AC by a scholarship from the project NORTE-08-5639-FSE-000041 (NORTE 2020; UMINHO/BD/51/2017). NCS was a recipient of a Research Assistantship by the through the FCT Investigator Programme 200∞ Ciência.

FundersFunder number
Portuguese North Regional Operational Programme
European Commission
National Strategic Reference Framework
Operational Programme Competitiveness and Internationalization
Programa Operacional Temático Factores de Competitividade
Operational Programme Competitiveness Factors-COMPETE
QREN
Northern Portugal Regional Operational ProgrammeP2020
Fundação para a Ciência e a TecnologiaPOCI-01-0145-FEDER-007038, PD/BD/106050/2015, NORTE-01-0145-FEDER-000013
European Regional Development FundPOCI-01-0145-FEDER-016428
Seventh Framework ProgrammeP-139977, PD/BD/106050/2015, PDE/BDE/113604/2015, NORTE-08-5639-FSE-000041, PDE/BDE/113601/2015, UMINHO/BD/51/2017, SFRH/BD/101398/2014, 259772, SFRH/BD/90078/2012, HEALTH-F2-2010-259772

Keywords

  • MRI
  • PSQI
  • Pittsburgh Sleep Quality Index
  • brain connectivity
  • resting-state
  • whole-brain modeling

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