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.

Sleep spindles and slow waves are physiological markers for age-related changes in gray matter in brain regions supporting problem-solving skills.

As we age, the added benefit of sleep for memory consolidation is lost. One of the hallmark age-related changes in sleep is the reduction of sleep spindles and slow waves. Gray matter neurodegeneration is related to both age-related changes in sleep and age-related changes in memory, including memory for problem-solving skills. Here, we investigated whether spindles and slow waves might serve as biological markers for neurodegeneration of gray matter and for the related memory consolidation deficits in older adults. Forty healthy young adults (20-35 yr) and 30 healthy older adults (60-85 yr) were assigned to either nap or wake conditions. Participants were trained on the Tower of Hanoi in the morning, followed by either a 90-min nap opportunity or period of wakefulness, and were retested afterward. We found that age-related changes in sleep spindles and slow waves were differentially related to gray matter intensity in young and older adults in brain regions that support sleep-dependent memory consolidation for problem-solving skills. Specifically, we found that spindles were related to gray matter in neocortical areas (e.g., somatosensory and parietal cortex), and slow waves were related to gray matter in the anterior cingulate, hippocampus, and caudate, all areas known to support problem-solving skills. These results suggest that both sleep spindles and slow waves may serve as biological markers of age-related neurodegeneration of gray matter and the associated reduced benefit of sleep for memory consolidation in older adults.

Age-related differences in problem-solving skills: Reduced benefit of sleep for memory trace consolidation.

We investigated the behavioural and neuronal functional consequences of age-related differences in sleep for gaining insight into novel cognitive strategies. Forty healthy young adults (20-35 years), and twenty-nine healthy older adults (60-85 years) were assigned to either nap or wake conditions. Participants were trained on the Tower of Hanoi in the AM, followed by either a 90-minute nap opportunity or period of wakefulness, and were retested afterward. Functional magnetic resonance imaging scans examined differences in brain activation from training to retest in young versus older adults as a function of sleep. Sleep enhanced performance and transformed the memory trace in young adults via hippocampal-neocortical transfer, but not older adults. This is consistent with the notion that as the consolidation of a newly formed memory trace progresses, the hippocampus becomes less involved; especially so when sleep occurs during that time. These results demonstrate a critical role for sleep in supporting problem-solving skills and suggest that the benefit of sleep for consolidation of these skills is reduced with age.

Sustained vigilance is negatively affected by mild and acute sleep loss reflected by reduced capacity for decision making, motor preparation, and execution.

Study Objectives: The behavioral and cognitive consequences of severe sleep deprivation are well understood. Surprisingly, relatively little is known about the neural correlates of mild and acute sleep restriction on tasks that require sustained vigilance for prolonged periods of time during the day. Methods and Results: Event-related potential (ERP) paradigms can reveal insight into the neural correlates underlying visual processing and behavioral responding that is impaired with reduced alertness, as a consequence of sleep loss. Here, we investigated the impact of reduced vigilance following at-home mild sleep restriction to better understand the associated behavioral consequences and changes in information processing revealed by ERPs. As expected, vigilance was reduced (e.g. increased lapses and response slowing) that increased over the course of the experiment in the "sleep restricted" (5 hr sleep) compared with the "sleep-extension" (9 hr sleep) condition. Corresponding to these lapses, we found decreased positivity of visually evoked potentials in the Sleep Restriction vs. Sleep Extension condition emerging from 316 to 449 ms, maximal over parietal/occipital cortex. We also investigated electrophysiological signs of motor-related processing by comparing lateralized readiness potentials (LRPs) and found reduced positivity of LRPs in the Sleep Restriction vs. Sleep Extension condition at 70-40 ms before, and 115-158 ms after a response was made. Conclusions: These results suggest that even a single night of mild sleep restriction can negatively affect vigilance, reflected by reduced processing capacity for decision making, and dulls motor preparation and execution.