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

Abstract

Learning leads to rapid microstructural changes in grey (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 12h and 24h of intense practice in two different tasks, and after post-training sleep. Compared to baseline wake, 12h of training led to a decline in cortical mean diffusivity. The decrease became even more significant after 24h 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.

Evidence for cortical structural plasticity in humans after a day of waking and sleep deprivation

“…The present findings are consistent with previous studies detecting changes in MRI-derived indices of adult human brain structure within hours to days. 29,30,[40][41][42][43][44][45] Recently, an increase in mean cortical thickness was found after recovery sleep following a night of sleep deprivation. 29 In another recent study, reductions in cortical thickness and grey matter volume from morning to afternoon were detected in healthy volunteers.…”

“…[25][26][27][28] In addition, MRI-based evidence for cortical thickening after recovery sleep following a night of sleep deprivation and changes in grey matter volume and thickness from morning to afternoon was recently reported. 29,30 However, whether hours of wake and sleep are associated with alterations in cortical structure detectable with current MRI techniques remains to be fully clarified.…”

Genetic polymorphisms associated with circadian rhythm dysregulation provide new perspectives on bipolar disorder

“…The authors further suggest that such an association indicates the participation of these polymorphic genes in sleep homeostasis . In fact, the important effect of sleep‐wake cycle homeostasis on brain functioning is undeniable . Furthermore, just like monoaminergic systems, circadian genes are expressed in many brain areas associated with behavioral control, indicating a broad and still undefined influence of neuronal activity at the cellular level .…”

“…Various imaging and functional studies, however, have found an association of disease with defects in the integrity of white matter (WM) tracts in the brain . Sleep promotes the myelination and proliferation of precursor cells of oligodendrocytes and upregulates expression of genes that promote phospholipid synthesis and myelination . In this context, Bollettini et al., analyzing polymorphisms of the CLOCK (rs1801260) and PER3 (rs6313) genes, demonstrated that variations in these genes are associated with variations in the myelination process and consequently WM integrity.…”

Visual imagery and visual perception induce similar changes in occipital slow waves of sleep

“…Wake EEG Recordings. Previous work showed that prolonged practice with particular tasks may lead to a local, regionally-specific increase in low-frequency activity during wakefulness in the theta range (5-9 Hz) (Hung et al, 2013), which may reflect experiencedependent changes in sleep need similar to local SWA during NREM-sleep (Bernardi et al, 2015(Bernardi et al, , 2016Hung et al, 2013;Nir et al, 2017;Pigarev et al, 1997). Thus, we also investigated regional (occipital) changes in theta activity during wakefulness after short-term visual deprivation.…”