Poor Sleep Quality Associates With Decreased Functional and Structural Brain Connectivity in Normative Aging: A MRI Multimodal Approach

Abstract

Sleep is a ubiquitous phenomenon, essential to the organism homeostasis. Notwithstanding, there has been an increasing concern with its disruption, not only within the context of pathological conditions, such as neurologic and psychiatric diseases, but also in health. In fact, sleep complaints are becoming particularly common, especially in middle-aged and older adults, which may suggest an underlying susceptibility to sleep quality loss and/or its consequences. Thus, a whole-brain modeling approach to study the shifts in the system can cast broader light on sleep quality mechanisms and its associated morbidities. Following this line, we sought to determine the association between the standard self-reported measure of sleep quality, the Pittsburgh Sleep Quality Index (PSQI) and brain correlates in a normative aging cohort. To this purpose, 86 participants (age range 52–87 years) provided information regarding sociodemographic parameters, subjective sleep quality and associated psychological variables. A multimodal magnetic resonance imaging (MRI) approach was used, with whole-brain functional and structural connectomes being derived from resting-state functional connectivity (FC) and probabilistic white matter tractography (structural connectivity, SC). Brain regional volumes and white matter properties associations were also explored. Results show that poor sleep quality was associated with a decrease in FC and SC of distinct networks, overlapping in right superior temporal pole, left middle temporal and left inferior occipital regions. Age displayed important associations with volumetric changes in the cerebellum cortex and white matter, thalamus, hippocampus, right putamen, left supramarginal and left lingual regions. Overall, results suggest that not only the PSQI global score may act as a proxy of changes in FC/SC in middle-aged and older individuals, but also that the age-related regional volumetric changes may be associated to an adjustment of brain connectivity. These findings may also represent a step further in the comprehension of the role of sleep disturbance in disease, since the networks found share regions that have been shown to be affected in pathologies, such as depression and Alzheimer's disease.

White Matter Microstructure Underlies the Effects of Sleep Quality and Life Stress on Depression Symptomatology in Older Adults

“…In contrast to our findings, several DTI studies (Khalsa et al, 2017;Sexton et al, 2017;Amorim et al, 2018;Takeuchi et al, 2018) reported that worsened sleep quality was associated with disrupted WM tracts of frontal, temporal, occipital, and subcortical regions. It should be noted that the above studies are varying with demographics of the participants (e.g., gender and ages), sample size, MRI sequences, and the statistical methods FIGURE 1 | Significant voxel-wise correlations between diffusion metrics of brain white matter (WM) tracts and BDI scores using TBSS (5000 permutations, FWER at p < 0.05).…”

“…Poor sleep quality has been associated with changes of brain structure and function by using advanced magnetic resonance imaging (MRI) techniques (Sexton et al, 2014;Spira et al, 2016;Amorim et al, 2018). Of these MRI modalities, diffusion tensor imaging (DTI) (Le Bihan et al, 2001), which quantifies three-dimensional displacements of water molecules along axons, reflects white matter (WM) microstructure connecting distributed brain regions.…”

Brain health consequences of digital technology use

“…31 Poor sleep quality is associated with brain changes, such as reduced functional connectivity and decreased gray-matter volume, as well as an increased risk for age-associated cognitive impairment and Alzheimer disease. 32,33 It is unclear whether the act of looking at screens or media content disrupts sleep; however, it is well-known that the wavelength of light exposure affects the circadian rhythms that govern sleep. Computer and phone light-emitting diode (LED) screens emit slow wave, blue light that interferes with circadian rhythms.…”

The role of sleep and wakefulness in myelin plasticity

“…More recently, using a whole‐brain multimodal MRI approach 86 participants were investigated to explore the association between subjective sleep quality (PSQI global score) and functional and structural connectivity. Both measures decreased in association with poor sleep (Amorim et al, ). In related work, a structural MRI study carried out in 448 community‐dwelling older adults showed that poor sleep quality was associated with reduced global FA and increased global axial and radial diffusivity values of frontal white matter tracts (Sexton et al, ), thus suggesting that sleep quality is linked to white matter microstructure.…”