Sleep quality and the integrity of ascending reticular activating system - A multimodal MRI study

Abstract

Sleep is crucial for maintaining brain homeostasis and individuals with insufficient sleep are prone to more pronounced brain atrophy as compared to sufficiently sleeping peers. Moreover, sleep quality deteriorates with ageing and ageing is also associated with cerebral structural and functional changes, pointing to their mutual bidirectional interrelationship. This study aimed at determining whether sleep quality and age, separately, affect brain integrity and subsequently, whether sleep significantly modulates the effect of age on brain structural and functional integrity. 113 healthy volunteers underwent a multi-modal MRI imaging to extract information about the microstructure and function of major nodes of the ascending reticular activating system. Sleep quality was assessed by self-administered Pittsburgh's sleep quality index (PSQI) questionnaire. Subject were divided into good (global PSQI score <5) and poor (global PSQI score ≥5) sleep quality group. Whereas only borderline correlations were found between sleep quality and MRI metrics, age exhibited widespread correlations with both functional and microstructural MRI metrics. The latter effect was significantly modulated by sleep quality in ascending reticular activating system, hypothalamus, thalamus and also hippocampus in MRI metrics associated with iron load, cellularity and connectivity, mainly in the subgroup with poor sleep quality. Ergo, our results indicate sleep quality as a substantial contributor to both microstructural and functional brain changes in ageing and call for further research in this emerging topic.

Keywords: Brain ageing; Diffusion weighted imaging; Multimodal MRI; Relaxometry; Sleep quality.

Graphical abstract

Fig. 1

Regions of interest visualised from one representative subject in sagittal, coronal and transverse plane. Slice coordinates provided in left bottom corners. DRN – the dorsal raphe nucleus, PRN – the rostral pontine reticular nucleus, PPN – pedunculopontine tegmental nucleus, MR – the median raphe nucleus, PAG – periaqueductal grey matter, MRF – mesencephalic reticular formation, PRN – the rostral pontine reticular neucleus, ASHyp – anterior superior hypothalamus, AIHyp – anterior inferior hypothalamus, IntHyp – intermediate hypothalamus, PostHyp – posterior hypothalamus.

Fig. 2

Visualisation of regions of interest with significant correlation between age and global PSQI with MRI metrics: ODI (green), fIVCF (blue), wDeCe (pink), T1ρ (yellow) and T2ρ (red) in poor sleep quality group. ODI – orientation dispersion index, fICVF – intracellular volume fraction, wDeCe – weighted degree centrality. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)