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Neuroimage. 2016 Apr 1;129:367-377. doi: 10.1016/j.neuroimage.2016.01.020. Epub 2016 Jan 23.

Sleep reverts changes in human gray and white matter caused by wake-dependent training.

Author information

1
Dept. of Psychiatry, University of Wisconsin, Madison, WI 53719, USA; Laboratory of Clinical Biochemistry and Molecular Biology, University of Pisa, Pisa 56126, Italy; Clinical Psychology Branch, University of Pisa, AOUP Santa Chiara, Pisa 56126, Italy.
2
Laboratory of Clinical Biochemistry and Molecular Biology, University of Pisa, Pisa 56126, Italy; Clinical Psychology Branch, University of Pisa, AOUP Santa Chiara, Pisa 56126, Italy.
3
Dept. of Psychiatry, University of Wisconsin, Madison, WI 53719, USA.
4
Waisman Laboratory for Brain Imaging and Behavior, University of Wisconsin, Madison, WI 53705, USA.
5
Dept. of Psychiatry, University of Wisconsin, Madison, WI 53719, USA; Waisman Laboratory for Brain Imaging and Behavior, University of Wisconsin, Madison, WI 53705, USA; Dept. of Medical Physics, University of Wisconsin, Madison, WI 53705, USA.
6
Dept. of Physiology and Pharmacology, City University of New York Medical School, New York, NY 10031, USA.
7
Laboratory of Clinical Biochemistry and Molecular Biology, University of Pisa, Pisa 56126, Italy; Clinical Psychology Branch, University of Pisa, AOUP Santa Chiara, Pisa 56126, Italy; IMT School for Advanced Studies Lucca, Lucca 55100, Italy. Electronic address: pietro.pietrini@imtlucca.it.
8
Dept. of Psychiatry, University of Wisconsin, Madison, WI 53719, USA. Electronic address: ccirelli@wisc.edu.
9
Dept. of Psychiatry, University of Wisconsin, Madison, WI 53719, USA. Electronic address: gtononi@wisc.edu.

Abstract

Learning leads to rapid microstructural changes in gray (GM) and white (WM) matter. Do these changes continue to accumulate if task training continues, and can they be reverted by sleep? We addressed these questions by combining structural and diffusion weighted MRI and high-density EEG in 16 subjects studied during the physiological sleep/wake cycle, after 12 h and 24 h of intense practice in two different tasks, and after post-training sleep. Compared to baseline wake, 12 h of training led to a decline in cortical mean diffusivity. The decrease became even more significant after 24 h of task practice combined with sleep deprivation. Prolonged practice also resulted in decreased ventricular volume and increased GM and WM subcortical volumes. All changes reverted after recovery sleep. Moreover, these structural alterations predicted cognitive performance at the individual level, suggesting that sleep's ability to counteract performance deficits is linked to its effects on the brain microstructure. The cellular mechanisms that account for the structural effects of sleep are unknown, but they may be linked to its role in promoting the production of cerebrospinal fluid and the decrease in synapse size and strength, as well as to its recently discovered ability to enhance the extracellular space and the clearance of brain metabolites.

KEYWORDS:

DWI; Extracellular space; MRI; Mean diffusivity; Sleep deprivation

PMID:
26812659
PMCID:
PMC4803519
DOI:
10.1016/j.neuroimage.2016.01.020
[Indexed for MEDLINE]
Free PMC Article

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