Abstract
Memory consolidation during sleep relies on the precisely timed interaction of rhythmic neural events. Here, we investigate differences in slow oscillations (SO; 0.5–1 Hz), sleep spindles (SP), and their coupling across the adult human lifespan and ask whether observed alterations relate to the ability to retain associative memories across sleep. We demonstrate that older adults do not show the fine-tuned coupling of fast SPs (12.5–16 Hz) to the SO peak present in younger adults but, instead, are characterized most by a slow SP power increase (9–12.5 Hz) at the end of the SO up-state. This slow SP power increase, typical for older adults, coincides with worse memory consolidation in young age already, whereas the tight precision of SO–fast SP coupling promotes memory consolidation across younger and older adults. Crucially, brain integrity in source regions of SO and SP generation, including the medial prefrontal cortex, thalamus, hippocampus and entorhinal cortex, reinforces this beneficial SO–SP coupling in old age. Our results reveal that cognitive functioning is not only determined by maintaining structural brain integrity across the adult lifespan, but also by the preservation of precisely timed neural interactions during sleep that enable the consolidation of declarative memories.
Highlights
slow oscillations (SO) and SPs are studied with regard to their independent contribution to consolidation mechanisms
This study investigated whether the coupling of SOs and SPs during sleep changes across the adult lifespan and how these alterations relate to the ability to retain associative memories across sleep
We demonstrate that older adults do not display the central fast SP power increase time-locked to the SO peak that we observed in younger adults
Summary
SOs and SPs are studied with regard to their independent contribution to consolidation mechanisms. In light of the growing interest in the interaction of SOs and SPs, very recent evidence highlights that SO–SP coupling is dispersed in elderly adults, resulting in impaired overnight memory consolidation[43] As this disturbed nesting of SOs and SPs may constitute a possible target for clinical interventions[48], the preconditions and the functional significance of SO–SP coupling across the entire adult lifespan require investigation. Following this rationale, it was our aim to examine age-related changes in the coupling of SOs and both slow and fast SPs. We asked whether observed alterations can be explained by structural brain atrophy in source regions of SO and SP generation and whether the resulting SO–SP dispersion negatively impacts the ability to retain associative memories across sleep. We relate the pattern of SO–SP coupling to the behavioral measure of overnight memory retention and show that the observed ‘aged’ SO–SP coordination explains deficient memory consolidation in old age
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