Associations between self-reported sleep quality and white matter in community-dwelling older adults: A prospective cohort study - PubMed (original) (raw)
. 2017 Nov;38(11):5465-5473.
doi: 10.1002/hbm.23739. Epub 2017 Jul 26.
Enikő Zsoldos 2, Nicola Filippini 2, Ludovica Griffanti 1, Anderson Winkler 1, Abda Mahmood 2, Charlotte L Allan 2, Anya Topiwala 2, Simon D Kyle 3, Kai Spiegelhalder 4, Archana Singh-Manoux 5, Mika Kivimaki 6, Clare E Mackay 2, Heidi Johansen-Berg 1, Klaus P Ebmeier 2
Affiliations
- PMID: 28745016
- PMCID: PMC5655937
- DOI: 10.1002/hbm.23739
Associations between self-reported sleep quality and white matter in community-dwelling older adults: A prospective cohort study
Claire E Sexton et al. Hum Brain Mapp. 2017 Nov.
Abstract
Both sleep disturbances and decline in white matter microstructure are commonly observed in ageing populations, as well as in age-related psychiatric and neurological illnesses. A relationship between sleep and white matter microstructure may underlie such relationships, but few imaging studies have directly examined this hypothesis. In a study of 448 community-dwelling members of the Whitehall II Imaging Sub-Study aged between 60 and 82 years (90 female, mean age 69.2 ± 5.1 years), we used the magnetic resonance imaging technique diffusion tensor imaging to examine the relationship between self-reported sleep quality and white matter microstructure. Poor sleep quality at the time of the diffusion tensor imaging scan was associated with reduced global fractional anisotropy and increased global axial diffusivity and radial diffusivity values, with small effect sizes. Voxel-wise analysis showed that widespread frontal-subcortical tracts, encompassing regions previously reported as altered in insomnia, were affected. Radial diffusivity findings remained significant after additional correction for demographics, general cognition, health, and lifestyle measures. No significant differences in general cognitive function, executive function, memory, or processing speed were detected between good and poor sleep quality groups. The number of times participants reported poor sleep quality over five time-points spanning a 16-year period was not associated with white matter measures. In conclusion, these data demonstrate that current sleep quality is linked to white matter microstructure. Small effect sizes may limit the extent to which poor sleep is a promising modifiable factor that may maintain, or even improve, white matter microstructure in ageing. Hum Brain Mapp 38:5465-5473, 2017. © 2017 Wiley Periodicals, Inc.
Keywords: brain; cognition; diffusion tensor imaging; executive function; insomnia; magnetic resonance imaging; memory; processing speed.
© 2017 The Authors Human Brain Mapping Published by Wiley Periodicals, Inc.
Figures
Figure 1
Localization of group differences in DTI measures between current good and poor sleep quality groups. Voxels displaying a significant reduction in FA (red), increase in AD (yellow) or increase in RD (blue) in the poor sleep quality group, dilated for illustrative purposes using tbss_fill, are overlaid on a green skeleton. Age, sex and education were included as covariates, with significance threshold set at P < 0.05, corrected for multiple comparisons across voxels. [Color figure can be viewed at
]
Similar articles
- The prospective association of objectively measured sleep and cerebral white matter microstructure in middle-aged and older persons.
Kocevska D, Tiemeier H, Lysen TS, de Groot M, Muetzel RL, Van Someren EJW, Ikram MA, Vernooij MW, Luik AI. Kocevska D, et al. Sleep. 2019 Oct 9;42(10):zsz140. doi: 10.1093/sleep/zsz140. Sleep. 2019. PMID: 31270542 - Neural correlates of sleep quality in children: Sex-specific associations shown by brain diffusion tractography.
Raja R, Na X, Badger TM, Ou X. Raja R, et al. J Neuroimaging. 2022 May;32(3):530-543. doi: 10.1111/jon.12964. Epub 2022 Jan 18. J Neuroimaging. 2022. PMID: 35041231 Free PMC article. - Relationship between sleep, physical fitness, brain microstructure, and cognition in healthy older adults: A pilot study.
Mueller C, Nenert R, Catiul C, Pilkington J, Szaflarski JP, Amara AW. Mueller C, et al. Brain Res. 2024 Sep 15;1839:149016. doi: 10.1016/j.brainres.2024.149016. Epub 2024 May 18. Brain Res. 2024. PMID: 38768934 - Associations between modifiable risk factors and white matter of the aging brain: insights from diffusion tensor imaging studies.
Wassenaar TM, Yaffe K, van der Werf YD, Sexton CE. Wassenaar TM, et al. Neurobiol Aging. 2019 Aug;80:56-70. doi: 10.1016/j.neurobiolaging.2019.04.006. Epub 2019 Apr 11. Neurobiol Aging. 2019. PMID: 31103633 Free PMC article. Review. - Aging and white matter microstructure and macrostructure: a longitudinal multi-site diffusion MRI study of 1218 participants.
Schilling KG, Archer D, Yeh FC, Rheault F, Cai LY, Hansen C, Yang Q, Ramdass K, Shafer AT, Resnick SM, Pechman KR, Gifford KA, Hohman TJ, Jefferson A, Anderson AW, Kang H, Landman BA. Schilling KG, et al. Brain Struct Funct. 2022 Jul;227(6):2111-2125. doi: 10.1007/s00429-022-02503-z. Epub 2022 May 23. Brain Struct Funct. 2022. PMID: 35604444 Free PMC article. Review.
Cited by
- Risk factors associated with the Motoric Cognitive Risk syndrome: A meta-analysis of data from a cross-national study.
Jayakody O, Blumen HM, Breslin M, Wang C, Verghese J. Jayakody O, et al. J Am Geriatr Soc. 2024 Sep;72(9):2656-2666. doi: 10.1111/jgs.19032. Epub 2024 Jun 14. J Am Geriatr Soc. 2024. PMID: 38872608 - Abnormal microstructure of corpus callosum in children with primary nocturnal enuresis: a DTI study.
Li J, Zhang Y, Chen J, Du X, Di Y, Liu Q, Wang C, Zhang Q. Li J, et al. Eur Child Adolesc Psychiatry. 2024 Mar 21. doi: 10.1007/s00787-024-02416-8. Online ahead of print. Eur Child Adolesc Psychiatry. 2024. PMID: 38514474 - Association between the Pittsburgh sleep quality index and white matter integrity in healthy adults: a whole-brain magnetic resonance imaging study.
Hidese S, Ota M, Matsuo J, Ishida I, Yokota Y, Hattori K, Yomogida Y, Kunugi H. Hidese S, et al. Sleep Biol Rhythms. 2023 Jan 2;21(2):249-256. doi: 10.1007/s41105-022-00442-0. eCollection 2023 Apr. Sleep Biol Rhythms. 2023. PMID: 38469289 Free PMC article. - Comprehensive assessment of sleep duration, insomnia, and brain structure within the UK Biobank cohort.
Stolicyn A, Lyall LM, Lyall DM, Høier NK, Adams MJ, Shen X, Cole JH, McIntosh AM, Whalley HC, Smith DJ. Stolicyn A, et al. Sleep. 2024 Feb 8;47(2):zsad274. doi: 10.1093/sleep/zsad274. Sleep. 2024. PMID: 37889226 Free PMC article. - Causal associations between sleep traits and brain structure: a bidirectional Mendelian randomization study.
Wang Q, Hu S, Qi L, Wang X, Jin G, Wu D, Wang Y, Ren L. Wang Q, et al. Behav Brain Funct. 2023 Oct 2;19(1):17. doi: 10.1186/s12993-023-00220-z. Behav Brain Funct. 2023. PMID: 37784181 Free PMC article.
References
- Allan CL, Sexton CE, Filippini N, Topiwala A, Mahmood A, Zsoldos E, Singh‐Manoux A, Shipley MJ, Kivimaki M, Mackay CE, Ebmeier KP (2016): Sub‐threshold depressive symptoms and brain structure: A magnetic resonance imaging study within the Whitehall II cohort. J Affect Disord 204:219–225. - PMC - PubMed
- Andersson JLR, Graham MS, Zsoldos E, Sotiropoulos SN (2016): Incorporating outlier detection and replacement into a non‐parametric framework for movement and distortion correction of diffusion MR images. Neuroimage 41:556–572. - PubMed
- Andersson JLR, Skare S, Ashburner J (2003): How to correct susceptibility distortions in spin‐echo echo‐planar images: application to diffusion tensor imaging. Neuroimage 20:870–888. - PubMed
- Baillet M, Dilharreguy B, Peres K, Dartigues JF, Mayo W, Catheline G (2017): Activity/rest cycle and disturbances of structural backbone of cerebral networks in aging. Neuroimage 146:814–820. - PubMed
Publication types
MeSH terms
Grants and funding
- MR/L023784/1/MRC_/Medical Research Council/United Kingdom
- K013351/MRC_/Medical Research Council/United Kingdom
- MR/M024962/1/MRC_/Medical Research Council/United Kingdom
- Wellcome Trust/United Kingdom
- G1001354/MRC_/Medical Research Council/United Kingdom
- MC_EX_MR/N50192X/1/MRC_/Medical Research Council/United Kingdom
LinkOut - more resources
Full Text Sources
Other Literature Sources
Medical