Effect of emotional and neutral declarative memory consolidation on sleep architecture.

The relationship between emotional or neutral declarative memory consolidation and sleep architecture was investigated. Thirty university students (21 females) viewed negative, neutral, or positive pictures and rated their valence and arousal in the evening. Participants performed a recognition test 1 h later and then underwent overnight polysomnography. Their post-encoding sleep architecture was compared to a baseline night. Participants returned 6 days following encoding for a second recognition test. Results showed no group (Negative, Neutral, Positive) differences in recognition 1 h or 6 days following encoding. Stage 2 sleep spindle density decreased across all groups following encoding, and recognition after 6 days was positively correlated with Stage 2 sleep spindle density on both nights. There was no change in REM density in any of the groups. This is the first investigation into phasic sleep microarchitecture changes following emotional and neutral declarative learning. Future investigations may benefit from more salient emotional stimuli.

Validating an automated sleep spindle detection algorithm using an individualized approach.

The goal of the current investigation was to develop a systematic method to validate the accuracy of an automated method of sleep spindle detection that takes into consideration individual differences in spindle amplitude. The benchmarking approach used here could be employed more generally to validate automated spindle scoring from other detection algorithms. In a sample of Stage 2 sleep from 10 healthy young subjects, spindles were identified both manually and automatically. The minimum amplitude threshold used by the Prana (PhiTools, Strasbourg, France) software spindle detection algorithm to identify a spindle was subject-specific and determined based upon each subject's mean peak spindle amplitude. Overall sensitivity and specificity values were 98.96 and 88.49%, respectively, when compared to manual scoring. Selecting individual amplitude thresholds for spindle detection based on systematic benchmarking data may validate automated spindle detection methods and improve reproducibility of experimental results. Given that interindividual differences are accounted for, we feel that automatic spindle detection provides an accurate and efficient alternative approach for detecting sleep spindles.

Dissociable learning-dependent changes in REM and non-REM sleep in declarative and procedural memory systems.

Sleep spindles and rapid eye movements have been found to increase following an intense period of learning on a combination of procedural memory tasks. It is not clear whether these changes are task specific, or the result of learning in general. The current study investigated changes in spindles, rapid eye movements, K-complexes and EEG spectral power following learning in good sleepers randomly assigned to one of four learning conditions: Pursuit Rotor (n=9), Mirror Tracing (n=9), Paired Associates (n=9), and non-learning controls (n=9). Following Pursuit Rotor learning, there was an increase in the duration of Stage 2 sleep, spindle density (number of spindles/min), average spindle duration, and an increase in low frequency sigma power (12-14Hz) at occipital regions during SWS and at frontal regions during Stage 2 sleep in the second half of the night. These findings are consistent with previous findings that Pursuit Rotor learning is consolidated during Stage 2 sleep, and provide additional data to suggest that spindles across all non-REM stages may be a mechanism for brain plasticity. Following Paired Associates learning, theta power increased significantly at central regions during REM sleep. This study provides the first evidence that REM sleep theta activity is involved in declarative memory consolidation. Together, these findings support the hypothesis that brain plasticity during sleep does not involve a unitary process; that is, different types of learning have unique sleep-related memory consolidation mechanisms that act in dissociable brain regions at different times throughout the night.

Post-training intra-striatal scopolamine or flupenthixol impairs radial maze learning in rats.

Systemic treatments with acetylcholine (ACh) or dopamine (DA) receptor antagonists during hours 0-4 but not during hours 5-8 following training on a radial arm maze (RAM) or lesions of the dorsal striata impair learning. This suggested that intra-striatal infusions of ACh or DA receptor antagonists during hours 0-4 following training may impair learning. Rats were randomly assigned to groups (ns=5-11) receiving dorsal striatal infusions of the ACh receptor antagonist scopolamine (0-18 microg/microL at 0 and 2h or at 4 and 6h after training), the DA receptor antagonist cis-flupenthixol (0-25 microg/microL at 0, 4 or 12h after training) or the inactive isomer trans-flupenthixol (6 microg/microL at 0 h after training). Scopolamine and cis-flupenthixol impaired the habit-learning version of the task. Given after hours 0-4 following training, the effects of scopolamine were diminished but those of cis-flupenthixol were not. Trans-flupenthixol produced less impairment than cis-flupenthixol. Results suggest that ACh and DA receptors in the dorsal striatum during hours 0-4 following training play a role in habit learning.

Sleep Changes in Adolescents Following Procedural Task Training.

Recent research has suggested that some of the inter-individual variation in sleep spindle activity is due to innate learning ability. Sleep spindles have also been observed to vary following learning in both young and older adults. We examined the effect of procedural task acquisition on sleep stages and on sleep spindles in an adolescent sample. Participants were 32 adolescents (17 females) between the ages of 12 and 19 years. Spindle activity was examined in three different frequency ranges: 11.00-13.50 Hz (slow), 13.51-16.00 Hz (fast), and 16.01-18.50 Hz (superfast). No changes in spindle density were observed after successful learning of the pursuit rotor task. This result was in contrast to a number of studies reporting spindle density increases following successful learning. In the present study, participants who successfully learned the task showed no changes in their sleep stage proportions, but participants who were not successful showed a decrease in the proportion of stage 2 and increases in both SWS and REM sleep. We suggest that these changes in the sleep stages are consistent with the two stage model of sleep and memory proposed by Smith et al. (2004a).

Ventromedial prefrontal theta activity during rapid eye movement sleep is associated with improved decision-making on the Iowa Gambling Task.

Recent research is beginning to reveal an intricate relationship between sleep and decision-making. The Iowa Gambling Task (IGT) is a unique decision-making task that relies on the ventromedial prefrontal cortex (vmPFC), an area that integrates and weighs previous experiences with reward and loss to select choices with the highest overall value. Recently, it has been demonstrated that a period of sleep can enhance decision-making on this task. Our study investigated the sleep mechanisms (sleep stages and cortical activity) that underlie this improvement. We recorded electrophysiology for 3 consecutive nights: a habituation, baseline, and acquisition night. On acquisition night participants were administered either a 200-trial IGT (IGT group; n = 13) or a 200-trial control (IGT-control group; n = 8) version of the task prior to sleep. Compared with baseline, the IGT group had a significant increase in theta frequency (4 Hz-8 Hz) on cites located above vmPFC and left prefrontal cortex during REM sleep. This increase correlated with subsequent performance improvement from deck B, a high reward deck with negative long-term outcomes. Furthermore, presleep emotional arousal (measured via skin conductance response) toward deck B correlated to increased theta activity above the right vmPFC during REM sleep. Overall, these results suggests that insight into deck B may be enhanced via vmPFC theta activity during REM sleep and REM sleep may have distinct mechanisms for processing decision-making information. (PsycINFO Database Record

Correlations between adolescent processing speed and specific spindle frequencies.

Sleep spindles are waxing and waning thalamocortical oscillations with accepted frequencies of between 11 and 16 Hz and a minimum duration of 0.5 s. Our research has suggested that there is spindle activity in all of the sleep stages, and thus for the present analysis we examined the link between spindle activity (Stage 2, rapid eye movement (REM) and slow wave sleep (SWS)) and waking cognitive abilities in 32 healthy adolescents. After software was used to filter frequencies outside the desired range, slow spindles (11.00-13.50 Hz), fast spindles (13.51-16.00 Hz) and spindle-like activity (16.01-18.50 Hz) were observed in Stage 2, SWS and REM sleep. Our analysis suggests that these specific EEG frequencies were significantly related to processing speed, which is one of the subscales of the intelligence score, in adolescents. The relationship was prominent in SWS and REM sleep. Further, the spindle-like activity (16.01-18.50 Hz) that occurred during SWS was strongly related to processing speed. Results suggest that the ability of adolescents to respond to tasks in an accurate, efficient and timely manner is related to their sleep quality. These findings support earlier research reporting relationships between learning, learning potential and sleep spindle activity in adults and adolescents.

Scopolamine during the paradoxical sleep window impairs radial arm maze learning in rats.

It has been proposed that there are paradoxical sleep windows (PSW) during which REM sleep is required for effective learning. Thus, rats deprived of REM sleep during 0-4 (but not 5-8) h after training show impaired learning of a radial maze task. As cholinergic (ACh) systems are active during REM sleep and may be involved in learning, this experiment investigated the effects on learning of pharmacological manipulation of the cholinergic system during the period identified as the PSW. Sprague-Dawley rats were randomly assigned to groups that were physically deprived of REM for 4 h either immediately after training or beginning 4 h after training or treated with the ACh receptor antagonist scopolamine (0-0.4 mg/kg at 0 and 2 h after training or 0.006 mg/kg at 4 and 6 h after training) on each of 9 days of radial maze training. Post-training REM deprivation (0-4 h but not 5-8 h after training) and scopolamine dose-dependently impaired learning. Results suggest that REM sleep and intact ACh neurotransmission are required during the PSW for rats to learn the radial maze task.

Post learning sleep improves cognitive-emotional decision-making: evidence for a 'deck B sleep effect' in the Iowa Gambling Task.

The Iowa Gambling Task (IGT) is widely used to assess real life decision-making impairment in a wide variety of clinical populations. Our study evaluated how IGT learning occurs across two sessions, and whether a period of intervening sleep between sessions can enhance learning. Furthermore, we investigate whether pre-sleep learning is necessary for this improvement. A 200-trial version of the IGT was administered at two sessions separated by wake, sleep or sleep and wake (time-of-day control). Participants were categorized as learners and non-learners based on initial performance in session one. In session one, participants initially preferred the high-frequency reward decks B and D, however, a subset of learners decreased choice from negative expected value 'bad' deck B and increased choices towards with a positive expected value 'good' decks (decks C and D). The learners who had a period of sleep (sleep and sleep/wake control conditions) between sessions showed significantly larger reduction in choices from deck B and increase in choices from good decks compared to learners that had intervening wake. Our results are the first to show that post-learning sleep can improve performance on a complex decision-making task such as the IGT. These results provide new insights into IGT learning and have important implications for understanding the neural mechanisms of "sleeping on" a decision.

Age differences in the variability and distribution of sleep spindle and rapid eye movement densities.

The present study had two main objectives. The first objective was to compare the sleep architecture of young and older adults, with an emphasis on sleep spindle density and REM density. The second objective was to examine two aspects of age differences that have not been considered in previous studies: age differences in the variability of sleep measures as well as the magnitude of age differences in phasic events across the distribution of values (i.e., at each decile rather than a single measure of location such as the mean or median. A total of 24 young (mean age=20.75 ± 1.78 years) and 24 older (mean age=71.17 ± 6.15 years) adults underwent in-home polysomnography. Whole-night spindle density was significantly higher in young adults than older adults. The two age groups did not differ significantly in whole-night REM density, although significant increases in REM density across the night were observed in both age groups. These results suggest that spindle density is more affected by age than REM density. Although age differences were observed in the degree of absolute variability (older adults had significantly larger variances than young adults for sleep efficiency and time spent awake after sleep onset), a similar pattern was also observed within the two age groups: the four sleep measures with the lowest degrees of relative variability were the same and included time spent in REM and Stage 2 sleep, total sleep time, and sleep efficiency. The distributional analysis of age differences in sleep spindle density revealed that the largest age differences were initially observed in the middle of the distributions, but as the night progressed, they were seen at the upper end of the distributions. The results reported here have potential implications for the causes and functional implications of age-related changes in sleep architecture.

The function of the sleep spindle: a physiological index of intelligence and a mechanism for sleep-dependent memory consolidation.

Until recently, the electrophysiological mechanisms involved in strengthening new memories into a more permanent form during sleep have been largely unknown. The sleep spindle is an event in the electroencephalogram (EEG) characterizing Stage 2 sleep. Sleep spindles may reflect, at the electrophysiological level, an ideal mechanism for inducing long-term synaptic changes in the neocortex. Recent evidence suggests the spindle is highly correlated with tests of intellectual ability (e.g.; IQ tests) and may serve as a physiological index of intelligence. Further, spindles increase in number and duration in sleep following new learning and are correlated with performance improvements. Spindle density and sigma (14-16Hz) spectral power have been found to be positively correlated with performance following a daytime nap, and animal studies suggest the spindle is involved in a hippocampal-neocortical dialogue necessary for memory consolidation. The findings reviewed here collectively provide a compelling body of evidence that the function of the sleep spindle is related to intellectual ability and memory consolidation.

Different types of avoidance behavior in rats produce dissociable post-training changes in sleep.

Avoidance learning affects post-training sleep, and post-training sleep deprivation impairs performance. However, not all rats learn to make avoidance responses, and some rats fail to escape; a definitive behavior of learned helplessness, a model of depression. This study investigated the changes in sleep associated with different behaviors adopted following avoidance training. Rats (n=53) were trained for 100 trials over 2 days (50 trials/day), followed by 23-24 h of post-training polysomnography, then re-tested (25 trials). At re-test, rats were categorized into: 1) Active Avoiders (AA; n=22), 2), Non-learning (NL; n=21), or 3) Escape Failures (EF; n=10). AA rats increased avoidances over days, whereas the NL and EF groups did not. EF rats increased escape failures over days, whereas the NL and AA rats did not. EF rats had increased rapid eye movement (REM) sleep in the first 4h on training day 1. They also had increased non-REM sleep in the first 4h and last 4h on both training days. AA rats had increased REM sleep 13-20 h post-training. The type of behavioral strategy adopted throughout training is associated with a unique pattern of changes in post-training sleep. Training-dependent changes in post-acquisition sleep may reflect distinct processes involved in the consolidation of these different memory traces.

Evidence for 2-stage models of sleep and memory: learning-dependent changes in spindles and theta in rats.

What processes are involved in the formation of enduring memory traces? Sleep has been proposed to play a role in memory consolidation and the present study provides evidence to support 2-stage models of sleep and memory including both non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. Previous research has shown REM sleep increases following avoidance learning and memory is impaired if REM deprivation occurs during these post-training periods indicating that REM sleep may have a role in memory consolidation processes. These discrete post-training periods have been termed REM sleep windows (RSWs). It is not known whether the electroencephalogram has unique characteristics during the RSW. Further investigation of the RSW was one of the primary goals of this study. We investigated the epidural-recorded electrophysiological learning-related changes following avoidance training in rats. Theta power increased in the learning group during the RSW, suggesting that theta is involved in memory consolidation during this period. Sleep spindles subsequently increased in slow wave sleep (SWS). The results suggest that both NREM and REM sleep are involved in sleep-dependent memory consolidation, and provide support for existing 2-stage models. Perhaps first theta increases to organize and consolidate material via hippocampal-neocortical dialogue, followed by subsequent refinement in the cortex by spindles during SWS.

Changes in sleep architecture following motor learning depend on initial skill level.

Previous research has linked both rapid eye movement (REM) sleep and Stage 2 sleep to procedural memory consolidation. The present study sought to clarify the relationship between sleep stages and procedural memory consolidation by examining the effect of initial skill level in this relationship in young adults. In-home sleep recordings were performed on participants before and after learning the pursuit rotor task. We divided the participants into low- and high-skill groups based on their initial performance of the pursuit rotor task. In high-skill participants, there was a significant increase in Stage 2 spindle density after learning, and there was a significant correlation between the spindle density that occurred after learning and pursuit rotor performance at retest 1 week later. In contrast, there was a significant correlation between changes in REM density and performance on the pursuit rotor task during retest 1 week later in low-skill participants, although the actual increase in REM density failed to reach significance in this group. The results of the present study suggest the presence of a double dissociation in the sleep-related processes that are involved in procedural memory consolidation in low- and high-skill individuals. These results indicate that the changes in sleep microarchitecture that take place after learning depend on the initial skill level of the individual and therefore provide validation for the model proposed by Smith et al. [Smith, C. T., Aubrey, J. B., & Peters, K. R. Different roles for REM and Stage 2 sleep in motor learning. Psychologica Belgica, 44, 79-102, 2004]. Accordingly, skill level is an important variable that needs to be considered in future research on sleep and memory consolidation.

Learning-dependent changes in sleep spindles and Stage 2 sleep.

It has become increasingly clear that sleep is necessary for efficient memory consolidation. Recently, it has been found that Stage 2 sleep disruption impairs procedural memory performance, and that memory performance is correlated with the duration of Stage 2 sleep; but the mechanisms involved in synaptic plasticity for procedural memory during sleep have not been identified. The present study examined the learning-dependent changes in sleep, including Stage 2 sleep spindles. Following an intense period of simple motor procedural learning, the duration of Stage 2 sleep and spindle density increased. There were no changes observed in the duration of any other stage of sleep or in the density of rapid eye movements. These findings support the hypothesis that sleep spindles are involved in the off-line reprocessing of simple motor procedural memory during Stage 2 sleep.

Posttraining increases in REM sleep intensity implicate REM sleep in memory processing and provide a biological marker of learning potential.

Posttraining rapid eye movement (REM) sleep has been reported to be important for efficient memory consolidation. The present results demonstrate increases in the intensity of REM sleep during the night of sleep following cognitive procedural/implicit task acquisition. These REM increases manifest as increases in total number of rapid eye movements (REMs) and REM densities, whereas the actual time spent in REM sleep did not change. Further, the participants with the higher intelligence (IQ) scores showed superior task acquisition scores as well as larger posttraining increases in number of REMs and REM density. No other sleep state changes were observed. None of the pretraining baseline measures of REM sleep were correlated with either measured IQ or task performance. Posttraining increases in REM sleep intensity implicate REM sleep mechanisms in further off-line memory processing, and provide a biological marker of learning potential.