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

Elucidating 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. H...

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Published inPloS one Vol. 10; no. 5; p. e0127351
Main Authors Elvsåshagen, Torbjørn, Norbom, Linn B, Pedersen, Per Ø, Quraishi, Sophia H, Bjørnerud, Atle, Malt, Ulrik F, Groote, Inge R, Westlye, Lars T
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 28.05.2015
Public Library of Science (PLoS)
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Summary:Elucidating 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. Twenty-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. 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. 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. This 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.
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Competing Interests: Dr. Elvsåshagen has received honoraria for lecturing from GlaxoSmithKline and Pfizer. Dr. Malt has received honoraria for lecturing from AstraZeneca, GlaxoSmithKline, Eli Lilly, Lundbeck, and Schering-Plough, and has received an honorarium from the Norwegian Government's Directorate of Health for participation in writing the national treatment guidelines for depression and bipolar disorders. All other authors have declared that no competing interests exist. This does not alter the authors’ adherence to PLOS ONE policies on sharing data and materials.
Conceived and designed the experiments: TE LBN PØP UFM IRG LTW. Performed the experiments: TE LBN PØP. Analyzed the data: TE SHQ AB LTW. Contributed reagents/materials/analysis tools: LTW. Wrote the paper: TE LBN PØP SHQ AB UFM IRG LTW.
ISSN:1932-6203
1932-6203
DOI:10.1371/journal.pone.0127351