Sleep and sleep deprivation differentially alter white matter microstructure: a mixed model design utilising advanced diffusion modelling

Abstract

Sleep deprivation influences several critical functions, yet how it affects human brain white matter (WM) is not well understood. The aim of the present work was to investigate the effect of 32 hours of sleep deprivation on WM microstructure compared to changes observed in a normal sleep-wake cycle (SWC). To this end, we utilised diffusion weighted imaging (DWI) including the diffusion tensor model, diffusion kurtosis imaging and the spherical mean technique, a novel biophysical diffusion model. 46 healthy adults (23 sleep deprived vs 23 with normal SWC) underwent DWI across 4 time points (morning, evening, next day morning and next day afternoon, after a total of 32 hours). Linear mixed models revealed significant group × time interaction effects, indicating that sleep deprivation and normal SWC differentially affect WM microstructure. Voxel-wise comparisons showed that these effects spanned large, bilateral WM regions. These findings provide important insight into how sleep deprivation affects the human brain.

Nighttime Sleep Characteristics and White Matter Integrity in Young Adults

“…In contrast to other studies, 21 , 65 , 68 we did not identify differences in white matter indices between the Short and Reference sleep groups. With regard to this result, it is relevant to note that other reports did not find a significant relation between sleep and white matter integrity.…”

“…79,80 In this study, the Long sleep group had higher sleep fragmentation in the nocturnal period than the Reference group, which could suggest the fact that sleep quality is a key factor in the maintenance of brain microstructure. In contrast to other studies, 21,65,68 we did not identify differences in white matter indices between the Short and Reference sleep groups. With regard to this result, it is relevant to note that other reports did not find a significant relation between sleep and white matter integrity.…”

“… 61 , 62 Abnormalities in white matter integrity of this tract have been identified in patients with primary insomnia 63 , 64 and associated with disrupted sleep patterns. 58 , 65 Alterations in the white matter of the anterior thalamic radiation, which connects the thalamus and the frontal lobe, 66 have been linked to poor sleep quality, 67 sleep deprivation, 68 and sleep spindles activity. 69 …”

“…61,62 Abnormalities in white matter integrity of this tract have been identified in patients with primary insomnia 63,64 and associated with disrupted sleep patterns. 58,65 Alterations in the white matter of the anterior thalamic radiation, which connects the thalamus and the frontal lobe, 66 have been linked to poor sleep quality, 67 sleep deprivation, 68 and sleep spindles activity. 69 Because sleep fragmentation in the Long sleep group occurred mainly in the second half of the night, we suggest that REM sleep 70,71 is involved in the reduced integrity of white matter microstructure.…”