Age-related changes in fast spindle clustering during non-rapid eye movement sleep and their relevance for memory consolidation

Abstract

Sleep plays a crucial role in memory consolidation. Recent data in rodents and young adults revealed that fast spindle band power fluctuates at a 0.02-Hz infraslow scale during non-rapid eye movement (NREM) sleep. These fluctuations result from a periodic temporal clustering of spindles and may modulate sleep maintenance and memory consolidation. With age, sleep undergoes substantial changes but age-related changes in spindle clustering have never been investigated. Polysomnography data were collected in 147 older (mean age ± SD: 69.3 ± 4.1 years) and 32 young-middle aged (34.5 ± 10.9 years) adults. Sleep-dependent memory consolidation was assessed in a subsample of 57 older adults using a visuospatial memory task. We analyzed power fluctuations in fast spindle frequency band, detected fast spindles and quantified their clustering during the night separating encoding and retrieval. Fast spindle band power fluctuated at a 0.02-Hz infraslow scale in young-middle aged and older adults. However, the proportion of clustered fast spindles decreased non-linearly with age (p < 0.001). This effect was not mediated by NREM sleep fragmentation. The clustering level of fast spindles modulated their characteristics (p < 0.001). Finally, the mean size of spindle clusters was positively associated with memory consolidation (p = 0.036) and negatively with NREM sleep micro-arousals density (p = 0.033). These results suggest that clusters of fast spindles may constitute stable sleep periods promoting off-line processes such as memory consolidation. We emphasize the relevance of considering spindle dynamics, obviously impaired during ageing, to understand the impact of age-related sleep changes on memory.

Sleep spindle density and temporal clustering are associated with sleep-dependent memory consolidation in Parkinson’s disease

“…Our results are broadly consistent with findings in healthy younger and older adults showing that higher spindle density is associated with better overnight preservation of memory 13,15–18,40 . We additionally found that greater clustering of spindles into trains was associated with better consolidation in Parkinson’s patients, which is also consistent with recent work in young and older adults 25,27,28,41 . One proposed mechanism for the relationship between spindles and memory consolidation is that spindles could facilitate the reactivation of a memory engram and the integration of a memory trace into relevant brain networks during sleep 14,20,42–45 .…”

“…Much less is known about aging effects on the temporal clustering of spindles. One study found that the proportion of clustered spindles and the length of train of clustered spindles decreased with age, and that shorter trains were associated with worse declarative memory consolidation 28 . Our study is the first to report on sleep spindle trains in Parkinson’s disease, therefore it remains unknown if the effect of Parkinson’s disease on spindle trains is similar to that of the disease on spindle density, i.e.…”

Individualized temporal patterns dominate cortical upstate and sleep depth in driving human sleep spindle timing

“…We also find a significant reduction in the duration of the excitatory period along with a lower peak height (though not statistically significant) with aging. This suggests that spindle patterns become less periodic and more variable with age, which provides additional evidence of age-related impairment of sleep spindle dynamics 25,38 .…”

“…Recent studies, however, have started to assess temporal patterns of spindles. Antony et al reported the refractoriness of spindles by visualizing the distribution of inter-spindle lags and highlighted the importance of spindle timing in optimal memory reactivation 40 ; Boutin and Doyon proposed the idea of temporal clusters of spindles by defining the “train of spindles” as a group of at least 2 consecutive spindles interspaced by less than 6 seconds 39 , and based on this criterion, Champetier et al further studied how spindle temporal clustering changes over age and their relevance for memory consolidation 38 . Those attempts to understand spindle temporal patterns highlight the importance of spindle dynamics in various functional roles.…”

“…Numerous studies have demonstrated that spindle activity dynamically and continuously evolves over time and is mediated by a variety of intrinsic and extrinsic factors including sleep stage 5,28 , slow oscillation activity (0.5 -1.5 Hz) 25,[29][30][31][32][33][34] , hippocampal ripples 29,33,35,36 , and infra-slow oscillations (< 0.1 Hz) 5,[37][38][39][40] . The timing and rate of occurrence of spindles is also influenced by homeostatic and circadian factors, chronotype, biological sex, and IQ, as well as the biophysical properties of thalamic reticular nucleus and thalamocortical neurons, their synaptic connectivity and their modulation by ascending arousal systems 5 .…”