Spindle-slow wave coupling and problem-solving skills: impact of age.

We examined how aging affects the role of sleep in the consolidation of newly learned cognitive strategies. Forty healthy young adults (20-35 years) and 30 healthy older adults (60-85 years) were included. Participants were trained on the Tower of Hanoi (ToH) task, then, half of each age group were assigned to either the 90-minute nap condition, or stayed awake, before retesting. The temporal co-occurrence between slow waves (SW) and sleep spindles (SP) during non-rapid eye movement sleep was examined as a function of age in relation to memory consolidation of problem-solving skills. We found that despite intact learning, older adults derived a reduced benefit of sleep for problem-solving skills relative to younger adults. As expected, the percentage of coupled spindles was lower in older compared to younger individuals from control to testing sessions. Furthermore, coupled spindles in young adults were more strongly coupled to the SW upstate compared to older individuals. Coupled spindles in older individuals were lower in amplitude (mean area under the curve; µV) compared to the young group. Lastly, there was a significant relationship between offline gains in accuracy on the ToH and percent change of spindles coupled to the upstate of the slow wave in older, but not younger adults. Multiple regression revealed that age accounted for differences in offline gains in accuracy, as did spindle coupling during the upstate. These results suggest that with aging, spindle-slow wave coupling decreases. However, the degree of the preservation of coupling with age correlates with the extent of problem-solving skill consolidation during sleep.

Eye movements during phasic versus tonic rapid eye movement sleep are biomarkers of dissociable electroencephalogram processes for the consolidation of novel problem-solving skills.

The hallmark eye movement (EM) bursts that occur during rapid eye movement (REM) sleep are markers of consolidation for procedural memory involving novel cognitive strategies and problem-solving skills. Examination of the brain activity associated with EMs during REM sleep might elucidate the processes involved in memory consolidation, and may uncover the functional significance of REM sleep and EMs themselves. Participants performed a REM-dependent, novel procedural problem-solving task (i.e. the Tower of Hanoi; ToH) before and after intervals of either overnight sleep (n = 20) or a daytime 8-hour wake period (n = 20). In addition, event-related spectral perturbation of the electroencephalogram (EEG) time-locked to EMs occurring either in bursts (i.e. phasic REM), or in isolation (i.e. tonic REM), were compared to sleep on a non-learning control night. ToH improvement was greater following sleep compared to wakefulness. During sleep, prefrontal theta (~2-8 Hz) and central-parietal-occipital sensorimotor rhythm (SMR) activity (~8-16 Hz) time-locked to EMs, were greater on the ToH night versus control night, and during phasic REM sleep, were both positively correlated with overnight memory improvements. Furthermore, SMR power during tonic REM increased significantly from the control night to ToH night, but was relatively stable from night to night during phasic REM. These results suggest that EMs are markers of learning-related increases in theta and SMR during phasic and tonic REM sleep. Phasic and tonic REM sleep may be functionally distinct in terms of their contribution to procedural memory consolidation.

Sleep strengthens resting-state functional communication between brain areas involved in the consolidation of problem-solving skills.

Sleep consolidates procedural memory for motor skills, and this process is associated with strengthened functional connectivity in hippocampal-striatal-cortical areas. It is unknown whether similar processes occur for procedural memory that requires cognitive strategies needed for problem-solving. It is also unclear whether a full night of sleep is indeed necessary for consolidation to occur, compared with a daytime nap. We examined how resting-state functional connectivity within the hippocampal-striatal-cortical network differs after offline consolidation intervals of sleep, nap, or wake. Resting-state fMRI data were acquired immediately before and after training on a procedural problem-solving task that requires the acquisition of a novel cognitive strategy and immediately prior to the retest period (i.e., following the consolidation interval). ROI to ROI and seed to whole-brain functional connectivity analyses both specifically and consistently demonstrated strengthened hippocampal-prefrontal functional connectivity following a period of sleep versus wake. These results were associated with task-related gains in behavioral performance. Changes in functional communication were also observed between groups using the striatum as a seed. Here, we demonstrate that at the behavioral level, procedural strategies benefit from both a nap and a night of sleep. However, a full night of sleep is associated with enhanced functional communication between regions that support problem-solving skills.