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Sleep Duration is Associated with Cognitive Performance and White Matter Microstructure in Healthy, Young Adults
Harald Kugel1, Pascal Grumbach2, Nils Opel2, Susanne Meinert2, Elisabeth J Leehr2, Ronny Redlich2, Verena Enneking2, Janik Goltermann2, Bernhard T Baune2,3, Udo Dannlowski2, and Jonathan Repple2
1Institute of Clinical Radiology, University of Muenster, Muenster, Germany, 2Department of Psychiatry, University of Muenster, Muenster, Germany, 3Department of Psychiatry, University of Melbourne, Melbourne, Australia

Synopsis

This cross-sectional study showed that real-world differences in sleep duration but not subjective sleep quality are related to cognitive performance measures and - as indicated by fractional anisotropy measures in the SLF - white matter integrity in healthy, young adults, suggesting a detrimental effect of shorter sleep duration on brain structure and function.

Introduction

Reduced sleep duration and sleep deprivation have been associated with cognitive impairment1,2 as well as decreased white matter integrity3-5 in experimental studies. However, it is largely unknown whether real-world differences in sleep duration and sleep quality might affect microstructural white matter and cognition. Therefore, the present study aims to examine the cross-sectional relationship between sleep duration, sleep quality and cognitive performance by focusing on the underlying alterations of white matter integrity in a large sample of healthy, young adults.

Methods

1065 participants (28.8 ± 3.7 years, 54% f) were taken from the open-access WU-Minn HCP 1200 Subjects Data Release,6 who underwent diffusion tensor imaging on a customized Siemens 3T “Connectome Skyra” at Washington University (Spin-echo EPI, TR/TE/FA 5520 ms/89,5 ms/78 deg, refocusing angle 160 deg, 111 slices, cubic voxels 1.25 mm edge length, b-values 1000, 2000, 3000 s/mm2). With Standard TBSS preprocessing7 Fractional Anisotropy (FA) images were registered to the FMROB58 FA template. Cognitive performance measures (NIH Cognition Toolbox),8 sleep duration, and sleep quality (Pittsburgh Sleep Quality Index)9 were assessed. Statistical analysis was done within SPSS (IBM Version 25). Associations were investigated while correcting for age and sex, for (1) correlation between sleep duration and sleep quality vs. global cognitive performance, for (2) association between sleep measures and FA (for whole brain and for the superior longitudinal fascicles (SLF)), and for (3) correlation between FA values, which correlated significantly in step (2), and global cognition. In addition, (4) a mediation analysis was performed with sleep measure as predictor variable (X), extracted mean FA from sleep analysis as mediator (M) and global cognitive performance as outcome variable (Y) with age and sex as covariates, applying a bootstrapping approach as implemented in the SPSS macro PROCESS.10

Results

The results revealed (1) a small but significant positive association between sleep duration and overall cognitive performance, especially in cognitive domains such as vocabulary knowledge and reading decoding. Furthermore (2), we found a trend towards a positive association of sleep duration with whole-brain FA, a marker of white matter integrity. Regions of interest (ROI) analysis showed that shorter sleep duration highly significantly correlated with FA reductions in the left SLF (Fig. 1). In turn, (3) FA in this tract is substantially related to measures of cognitive performance. (4) FA was shown to significantly mediate the association of sleep duration and cognition. Investigations into subjective sleep quality showed no such associations.

Discussion

The present study showed that real-world differences in sleep duration - but not subjective sleep quality - are related to cognitive performance measures and white matter integrity in the SLF in healthy, young adults, suggesting a detrimental effect of shorter sleep duration on brain structure and function. The study is cross-sectional in nature, thus the correlation should not be directly interpreted as proof of a causal relation. In addition, it must be noted that in this study the correlations are found for young adults, and the relations may be different in older persons.11,12

Acknowledgements

Funded by the German Research Foundation (DFG, grant FOR2107 DA1151/5-1 and DA1151/5-2 to UD; SFB-TRR58, Projects C09 and Z02 to UD) and the Interdisciplinary Center for Clinical Research (IZKF) of the medical faculty of Münster (grant Dan3/012/17 to UD). Data were provided [in part] by the Human Connectome Project, WU-Minn Consortium (Principal Investigators: David Van Essen and Kamil Ugurbil; 1U54MH091657) funded by the 16 NIH Institutes and Centers that support the NIH Blueprint for Neuroscience Research; and by the McDonnell Center for Systems Neuroscience at Washington University.

References

(1) Deak MC, Stickgold RK. Sleep and cognition. Wiley Interdiscip Rev Cogn Sci. 2010; 1(4):491-500. (2) Lim J, Dinges DF. A Meta-Analysis of the Impact of Short-Term Sleep Deprivation on Cognitive Variables. Psychol Bull. 2010; 136(3):375-389. (3) Elvsåshagen T, Norbom LB, Pedersen P, et al. Widespread changes in white matter microstructure after a day of waking and sleep deprivation. PLoS One. 2015; 10(5):e0127351. (4) Yaffe K, Nasrallah I, Hoang TD, et al. Sleep Duration and White Matter Quality in Middle-Aged Adults. Sleep. 2016; 39(9):1743-1747. (5) Li S, Tian J, Bauer A, et al. Reduced Integrity of Right Lateralized White Matter in Patients with Primary Insomnia: A Diffusion-Tensor Imaging Study. Radiology. 2016; 280(2):520-528. (6) Van Essen DC, Smith SM, Barch DM, et al. The WU-Minn Human Connectome Project: An overview. Neuroimage. 2013; 80:62-79. (7) Smith SM, Jenkinson M, Johansen-Berg H, et al. Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage. 2006; 31(4):1487-1505. (8) Weintraub S, Dikmen SS, Heaton RK, et al. Cognition assessment using the NIH Toolbox. Neurology. 2013; 80(11 Suppl 3):S49-S53. (9) Buysse DJ, Reynolds CF, Monk TH, et al. The Pittsburgh Sleep Quality Index: A New Instrument for Psychiatric Practice and Research. Psychiatry Res. 1989; 28(2):193-213. (10) Opel N, Martin S, Meinert S, et al. White matter microstructure mediates the association between physical fitness and cognition in healthy, young adults. Sci Rep. 2019; 9(1):12885. (11) Saint Martin M, Sforza E, Barthélémy JC, et al. Does subjective sleep affect cognitive function in healthy elderly subjects? The Proof cohort. Sleep Med. 2012; 13(9):1146-1152. (12) Blackwell T, Yaffe K, Ancoli-Israel S, et al. Association of Sleep Characteristics and Cognition in Older Community-Dwelling Men: the MrOS Sleep Study. Sleep. 2011; 34(10):1347-1356.

Figures

Figure 1: A: Sagittal slice with x= -38 (MNI) of a mean FA map. Red-yellow areas represent voxels (using FSL’s „fill“ command for better visualization), where a significant positive association between sleep duration and Fractional Anisotropy was detected (left superior longitudinal fascicle, pFWE< .05); B: Coronal slice (y= -10) C: Axial slice (z= 29); D: Scatterplot showing the association sleep duration and extracted mean FA values from all significant voxels of the corresponding TBSS analysis.

Proc. Intl. Soc. Mag. Reson. Med. 28 (2020)
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