Habitual sleep durations and subjective sleep quality predict white matter differences in the human brain

Sakh Khalsa,Joanne R Hale,Aimee Goldstone,Rebecca S Wilson,Stephen D Mayhew,Manny Bagary,Andrew P Bagshaw

doi:10.1016/j.nbscr.2017.03.001

Abstract

Self-imposed short sleep durations are increasingly commonplace in society, and have considerable health and performance implications for individuals. Reduced sleep duration over multiple nights has similar behavioural effects to those observed following acute total sleep deprivation, suggesting that lack of sleep affects brain function cumulatively. A link between habitual sleep patterns and functional connectivity has previously been observed, and the effect of sleep duration on the brain's intrinsic functional architecture may provide a link between sleep status and cognition. However, it is currently not known whether differences in habitual sleep patterns across individuals are related to changes in the brain's white matter, which underlies structural connectivity. In the present study we use diffusion–weighted imaging and a group comparison application of tract based spatial statistics (TBSS) to investigate changes to fractional anisotropy (FA) and mean diffusivity (MD) in relation to sleep duration and quality, hypothesising that white matter metrics would be positively associated with sleep duration and quality. Diffusion weighted imaging data was acquired from a final cohort of 33 (23–29 years, 10 female, mean 25.4 years) participants. Sleep patterns were assessed for a 14day period using wrist actigraphs and sleep diaries, and subjective sleep quality with the Pittsburgh Sleep Quality Index (PSQI). Median splits based on total sleep time and PSQI were used to create groups of shorter/longer and poorer/better sleepers, whose imaging data was compared using TBSS followed by post-hoc correlation analysis in regions identified as significantly different between the groups. There were significant positive correlations between sleep duration and FA in the left orbito-frontal region and the right superior corona radiata, and significant negative correlations between sleep duration and MD in right orbito-frontal white matter and the right inferior longitudinal fasciculus. Improved sleep quality was positively correlated with FA in left caudate nucleus, white matter tracts to the left orbito-frontal region, the left anterior cingulum bundle and the white matter tracts associated with the right operculum and insula, and negatively correlated with MD in left orbito-frontal white matter and the left anterior cingulum bundle. Our findings suggest that reduced cumulative total sleep time (cTST) and poorer subjective sleep quality are associated with subtle white matter micro-architectural changes. The regions we identified as being related to habitual sleep patterns were restricted to the frontal and temporal lobes, and the functions they support are consistent with those which have previously been demonstrated as being affected by short sleep durations (e.g., attention, cognitive control, memory). Examining how inter-individual differences in brain structure are related to habitual sleep patterns could help to shed light on the mechanisms by which sleep habits are associated with brain function, behaviour and cognition, as well as potentially the networks and systems responsible for variations in sleep patterns themselves.

Highlights

Sleep patterns have been investigated in relation to behaviour and functional connectivity (FC, De Havas et al, 2012; Gujar et al, 2010; Khalsa et al, 2016), but to date there have limited investigations in relation to brain structure
Our findings suggest that reduced cumulative total sleep time and poorer subjective sleep quality are associated with subtle white matter microarchitectural changes
The regions we identified as being related to habitual sleep patterns were restricted to the frontal and temporal lobes, and the functions they support are consistent with those which have previously been demonstrated as being affected by short sleep durations

Summary

Introduction

Sleep patterns have been investigated in relation to behaviour and functional connectivity (FC, De Havas et al, 2012; Gujar et al, 2010; Khalsa et al, 2016), but to date there have limited investigations in relation to brain structure. Acute sleep deprivation has been shown to reduce thalamic volume (Liu et al, 2014), in general the relative impact of acute and long term sleep patterns, as well as the mechanisms underlying them, remain to be understood These studies suggest that there is a link between sleep duration and brain structure. SC refers to the anatomical links between brain regions, rather than the statistical dependencies between activity time series that are the basis of functional connectivity It can be characterised non-invasively in humans using diffusion tensor imaging (DTI), with fractional anisotropy (FA) and mean diffusivity (MD), two commonly used metrics to quantify white matter tracts (Beaulieu et al, 2002; Le Bihan, 2003). These measures have been used extensively as markers of white matter microstructural changes in a variety of situations (Alexander et al, 2007), and may be altered by a variety of changes to the underlying white matter, such as increases or decreases in myelination, the extent of coherent alignment of fibres, the presence and orientation of crossing fibres from other bundles etc (Jones et al, 2013), as well as short term plasticity (Engvig et al, 2012) or disease state (e.g., Korgaonkar et al, 2011; Shukla et al, 2011)

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