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Effects of Aging on Sleep-Dependent Consolidation of Declarative Memory

Sleep plays a critical role in memory consolidation. However, aging is associated with changes in sleep architecture and memory impairments. The goal of the present study was to identify age-related changes in the memory function of sleep by investigating sleep-dependent changes in neural activation patterns during memory retrieval in young and older adults. Healthy young (21-29 years) and older (62-74 years) adults were trained on a declarative word-pair learning task. Recall was tested 5 hr later while undergoing functional magnetic resonance imaging (fMRI). Participants completed this testing procedure twice, separated by 1 week; once following a mid-day nap and once following continuous wakefulness in a counter-balanced order. Sleep was recorded by polysomnography for the naps and subsequent nocturnal intervals. It was found that napping, as compared to wakefulness, was associated with decreased hippocampal activation and decreased hippocampo-frontal co-activation in young adults. Specifically, slow wave sleep (SWS) in the young adult naps was associated with better memory retention (r = .61, p = .035) and decreased hippocampal activation (r = -.71, p = .01) lending support to the two-stage model of memory consolidation (McClelland, McNaughton & O’Reilly, 1995). On the other hand, sleep-dependent neural reorganization patterns were different in the older adult group. Following a nap, retrieval still required hippocampal activation and hippocampo-frontal co-activation (adjusted R2 = .701, F(1,10) = 22.08, p = .002). Furthermore, in contrast to a SWS-dependent decrease in anterior cingulate cortex (ACC) activation in young adults for successful retrieval (r = -.61, p = .037), ACC activation in older adults was increased when retrieval was tested following a nap compared to wakefulness, and was not significantly associated with measures of SWS. This suggests that successful retrieval following a nap required allocation of error monitoring processes in older adults. In summary, the present study shows that the efficiency with which systems level consolidation takes place in the first sleep opportunity following learning of a declarative memory task changes in healthy aging. Slow wave sleep-dependent reactivation processes may be disrupted, leaving memory traces at a more labile state of storage that requires additional allocation of cognitive control processes.
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