Widespread changes in white matter microstructure after a day of waking and sleep deprivation.

Torbjørn Elvsåshagen,Lars T. Westlye,Atle Bjørnerud,Linn B. Norbom,Sophia H. Quraishi,Ulrik F. Malt,Per Ø. Pedersen,Inge R. Groote,Joseph Najbauer

doi:10.1371/journal.pone.0127351

Torbjørn Elvsåshagen, Lars T. Westlye + Show 7 more

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https://doi.org/10.1371/journal.pone.0127351

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Abstract

BackgroundElucidating the neurobiological effects of sleep and waking remains an important goal of the neurosciences. Recently, animal studies indicated that sleep is important for cell membrane and myelin maintenance in the brain and that these structures are particularly susceptible to insufficient sleep. Here, we tested the hypothesis that a day of waking and sleep deprivation would be associated with changes in diffusion tensor imaging (DTI) indices of white matter microstructure sensitive to axonal membrane and myelin alterations.MethodsTwenty-one healthy adult males underwent DTI in the morning [7:30AM; time point (TP)1], after 14 hours of waking (TP2), and then after another 9 hours of waking (TP3). Whole brain voxel-wise analysis was performed with tract based spatial statistics.ResultsA day of waking was associated with widespread increases in white matter fractional anisotropy, which were mainly driven by radial diffusivity reductions, and sleep deprivation was associated with widespread fractional anisotropy decreases, which were mainly explained by reductions in axial diffusivity. In addition, larger decreases in axial diffusivity after sleep deprivation were associated with greater sleepiness. All DTI changes remained significant after adjusting for hydration measures.ConclusionsThis is the first DTI study of sleep deprivation in humans. Although previous studies have observed localized changes in DTI indices of cerebral microstructure over the course of a few hours, further studies are needed to confirm widespread DTI changes within hours of waking and to clarify whether such changes in white matter microstructure serve as neurobiological substrates of sleepiness.

Highlights

Sleep is an enigmatic, evolutionarily conserved process required for human health and functioning [1,2,3]
A day of waking was associated with widespread increases in white matter fractional anisotropy, which were mainly driven by radial diffusivity reductions, and sleep deprivation was associated with widespread fractional anisotropy decreases, which were mainly explained by reductions in axial diffusivity
Larger decreases in axial diffusivity after sleep deprivation were associated with greater sleepiness

Summary

Introduction

Evolutionarily conserved process required for human health and functioning [1,2,3]. A longstanding and widely held belief is that sleep is restorative [10, 11] In support of this hypothesis, increased brain expression of genes regulating macromolecule biosynthesis has consistently been found in flies, rodents, and birds during sleep [12,13,14,15]. Consistent with a role for sleep in membrane lipid homeostasis, sleep deprivation caused a marked increase in breakdown of membrane phospholipids of neurons in vitro and in vivo [18]. Together, these findings indicate that sleep is important for cell membrane and myelin maintenance in the brain and that these structures might be susceptible to insufficient sleep [17, 18]. We tested the hypothesis that a day of waking and sleep deprivation would be associated with changes in diffusion tensor imaging (DTI) indices of white matter microstructure sensitive to axonal membrane and myelin alterations

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Results

Conclusion