Abstract
BACKGROUNDTight relationships between sleep quality, cognition, and amyloid-β (Aβ) accumulation, a hallmark of Alzheimer’s disease (AD) neuropathology, have been shown. Sleep arousals become more prevalent with aging and are considered to reflect poorer sleep quality. However, heterogeneity in arousals has been suggested while their associations with Aβ and cognition are not established.METHODSWe recorded undisturbed night-time sleep with EEG in 101 healthy individuals aged 50–70 years, devoid of cognitive and sleep disorders. We classified spontaneous arousals according to their association with muscular tone increase (M+/M–) and sleep stage transition (T+/T–). We assessed cortical Aβ burden over earliest affected regions via PET imaging and assessed cognition via neuropsychological testing.RESULTSArousal types differed in their oscillatory composition in θ (4–8 Hz) and β (16–30 Hz) EEG bands. Furthermore, T+M– arousals, interrupting sleep continuity, were positively linked to Aβ burden (P = 0.0053, R²β* = 0.08). By contrast, more prevalent T–M+ arousals, upholding sleep continuity, were associated with lower Aβ burden (P = 0.0003, R²β* = 0.13), and better cognition, particularly over the attentional domain (P < 0.05, R²β* ≥ 0.04).CONCLUSIONContrasting with what is commonly accepted, we provide empirical evidence that arousals are diverse and differently associated with early AD-related neuropathology and cognition. This suggests that sleep arousals, and their coalescence with other brain oscillations during sleep, may actively contribute to the beneficial functions of sleep and constitute markers of favorable brain and cognitive health trajectories.TRIAL REGISTRATIONEudraCT 2016-001436-35.FUNDINGFRS-FNRS Belgium (FRSM 3.4516.11), Actions de Recherche Concertées Fédération Wallonie-Bruxelles (SLEEPDEM 17/27-09), ULiège, and European Regional Development Fund (Radiomed Project).
Highlights
Sleep is central to health and cognition, and it deteriorates with aging [1]
We first chose to focus on whether arousals did trigger a sleep stage transition (T+) or not (T–), as arousals may or may not lead to a lighter sleep stage [12] and they have already been investigated in that regard [17]
We assessed whether characterizing sleep arousals by their association with sleep stage transition (T+ or T–), and the cooccurrence of an EMG tone increase (M+) or not (M–) resulted in differences in their oscillatory properties
Summary
Sleep is central to health and cognition, and it deteriorates with aging [1]. In addition, sleep disruption is associated with Alzheimer’s disease (AD), as assessed by hyperphosphorylated tau and amyloid-β (Aβ) brain accumulation, most likely in a bidirectional manner [2, 3]. Sleep arousals, defined as transient accelerations in sleep electroencephalogram (EEG) rhythms, are usually considered as brain reactions to internal (e.g., apnea) or external (e.g., auditory stimulus) perturbations [11]. Several conceptual definitions classified them almost exclusively in the context of sleep disorders (e.g., sleep disordered breathing [SDB] and, to a smaller extent, periodic limb movements syndrome [PLMS]) or, in experimental protocols, inducing arousals through external — mainly auditory — stimulation [13, 14]. These types of studies yielded mixed results. Heterogeneity in arousals has been suggested while their associations with Aβ and cognition are not established
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