Cortical Thinning Explains Changes in Sleep Slow Waves during Adulthood

Abstract

Sleep slow waves (SWs) change considerably throughout normal aging. In humans, SWs are generated and propagate on a structural backbone of highly interconnected cortical regions that form most of the default mode network, such as the insula, cingulate cortices, temporal lobe, parietal lobe, and medial frontal lobe. Regions in this network undergo cortical thinning and breakdown in structural and functional connectivity over the course of normal aging. In this study, we investigated how changes in cortical thickness (CT), a measure of gray matter integrity, are involved in modifications of sleep SWs during adulthood in humans. Thirty young (mean age ϭ 23.49 years; SD ϭ 2.79) and 33 older (mean age ϭ 60.35 years; SD ϭ 5.71) healthy subjects underwent a nocturnal polysomnography and T1 MRI. We show that, when controlling for age, higher SW density (nb/min of nonrapid eye movement sleep) was associated with higher CT in cortical regions involved in SW generation surrounding the lateral fissure (insula, superior temporal, parietal, middle frontal), whereas higher SW amplitude was associated with higher CT in middle frontal, medial prefrontal, and medial posterior regions. Mediation analyses demonstrated that thinning in a network of cortical regions involved in SW generation and propagation, but also in cognitive functions, explained the age-related decrease in SW density and amplitude. Altogether, our results suggest that microstructural degradation of specific cortical regions compromise SW generation and propagation in older subjects, critically contributing to age-related changes in SW oscillations.

Differences in electroencephalographic non-rapid-eye movement sleep slow-wave characteristics between young and old mice

“…However, older mice showed higher absolute SWA values across the whole recording period, with significant differences compared to the young animals, particularly in the light period and at the end of the dark period. These observations contrast human studies, where absolute SWA values, as well as absolute amplitude, frequency and density of slow waves are found to be decreased in aging123563738.Moreover, the decay rate in SWA in the first three hours after SD was slower in the older mice compared to the young controls. The latter suggests that sleep in older mice is less efficient in dissipating sleep pressure.…”

“…Since aged mice show increased sleep fragmentation and increased sleep propensity in their habitual waking period during the night as well as less pronounced circadian rhythms of sleep and wakefulness711, they have been considered a good model to investigate age-dependent changes in sleep physiology. In humans, changes in NREM sleep SWA and slow-wave characteristics were studied thoroughly and were found to be consistent with the decrease in the amount of sleep seen in aging123456. However, in mice the effects of age on slow-wave parameters, that could provide insight into cortical network properties, have not been studied, and it remains unknown whether EEG changes occur in parallel with global sleep-wake alterations.…”

Do Older Adults Need Sleep? A Review of Neuroimaging, Sleep, and Aging Studies

“…Walker and colleagues [69] reported that greater slow wave activity was associated with greater medial PFC gray matter volume (see also [70]). Likewise, Carrier and colleagues [71] found that slow wave density was associated with greater cortical thickness in widespread frontal, temporal, and parietal regions. They concluded that age-related cortical atrophy explains age-related changes in slow wave activity.…”

“…The sleep and neuroimaging correlations reviewed herein disfavor the reduced-sleep-need view, regardless of whether sleep loss causes neural changes [60, 61] or whether neural changes cause sleep loss [47, 71]. Rather than concluding that older adults do not need sleep, if cortical thinning or amyloidal deposition are the cause of older adults’ poor sleep then a more fitting interpretation is that they have lost the ability to sleep in a restorative manner.…”

Novel word learning in older adults: A role for sleep?

“…Globally, spectral EEG power is reduced during sleep in older adults (Landolt & Borbély, 2001), possibly due to age-related changes in brain morphology (Dubé et al, 2015; Mander et al, 2013). This reduction is especially profound during sleep stages nREM2 and SWS: Older adults have reduced EEG sigma power (a surrogate of spindles) during nREM2 (Mander et al, 2013) and reduced SWA during SWS (Dubé et al, 2015). Given that SWA is influenced by both the number of underlying firing neurons and the synchronicity between these neurons (see review: Greene & Frank, 2010), a reduction in SWA represents the breakdown of these processes.…”