Abstract
In older adults, motor sequence learning (MSL) is largely intact. However, consolidation of newly learned motor sequences is impaired compared to younger adults, and there is evidence that brain areas supporting enhanced consolidation via sleep degrade with age. It is known that brain activity in hippocampal–cortical–striatal areas is important for sleep-dependent, off-line consolidation of motor-sequences. Yet, the intricacies of how both age and sleep alter communication within this network of brain areas, which facilitate consolidation, are not known. In this study, 37 young (age 20–35) and 49 older individuals (age 55–75) underwent resting state functional magnetic resonance imaging (fMRI) before and after training on a MSL task as well as after either a nap or a period of awake rest. Young participants who napped showed strengthening of functional connectivity (FC) between motor, striatal, and hippocampal areas, compared to older subjects regardless of sleep condition. Follow-up analyses revealed this effect was driven by younger participants who showed an increase in FC between striatum and motor cortices, as well as older participants who showed decreased FC between the hippocampus, striatum, and precuneus. Therefore, different effects of sleep were observed in younger vs. older participants, where young participants primarily showed increased communication in the striatal-motor areas, while older participants showed decreases in key nodes of the default mode network and striatum. Performance gains correlated with FC changes in young adults, and this association was much greater in participants who napped compared to those who stayed awake. Performance gains also correlated with FC changes in older adults, but only in those who napped. This study reveals that, while there is no evidence of time-dependent forgetting/deterioration of performance, older adults exhibit a completely different pattern of FC changes during consolidation compared to younger adults, and lose the benefit that sleep affords to memory consolidation.
Highlights
As we age, the brain activity underlying our sleep changes drastically
We investigated whether sleep-dependent resting state functional connectivity (FC) during offline consolidation of motor sequence learning (MSL) differed between young and older adults
Our results suggest that younger adults exhibit a completely different pattern of FC changes during MSL consolidation over a period of rest, with sleep having further differential effects on these FC
Summary
The brain activity underlying our sleep changes drastically. In youth, sleep-dependent physiological brain processes support important cognitive functions such as skill learning and memory, the ability for sleep to enhance learning and memory begins to deteriorate in middle age and beyond (Mander et al, 2013; Scullin and Bliwise, 2015). Older adults show a specific deficit in the consolidation of newly acquired motor sequences after a period of sleep (Spencer et al, 2007; Wilson et al, 2012) This age-related reduced benefit of sleep for memory consolidation has been associated with a reduction in sleep spindles, as well as reduced change in striatal activity across the retention period (Fogel et al, 2014). It has been proposed that sleep-enhanced memory consolidation proceeds via spindle-induced inter-regional reactivation of the same cortical and subcortical areas that were functionally active during initial learning (Boutin and Doyon, 2020) It is not known whether the process of consolidation is associated with detectable changes in resting state FC, and whether these potential changes are lost with age. We hypothesized that any relationship between FC changes and MSL performance gains would be stronger, or limited to young participants, as the degradation of sleep-dependent consolidation mechanisms should prevent consolidation-supporting FC changes from being observed in older adults
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