Practice Makes Imperfect: Restorative Effects of Sleep on Motor Learning

Emerging evidence suggests that sleep plays a key role in procedural learning, particularly in the continued development of motor skill learning following initial acquisition. We argue that a detailed examination of the time course of performance across sleep on the finger-tapping task, established as the paradigm for studying the effect of sleep on motor learning, will help distinguish a restorative role of sleep in motor skill learning from a proactive one. Healthy subjects rehearsed for 12 trials and, following a night of sleep, were tested. Early training rapidly improved speed as well as accuracy on pre-sleep training. Additional rehearsal caused a marked slow-down in further improvement or partial reversal in performance to observed levels below theoretical upper limits derived on the basis of early pre-sleep rehearsal. This decrement in learning efficacy does not occur always, but if and only if it does, overnight sleep has an effect in fully or partly restoring the efficacy and actual performance to the optimal theoretically achieveable level. Our findings re-interpret the sleep-dependent memory enhancement in motor learning reported in the literature as a restoration of fatigued circuitry specialized for the skill. In providing restitution to the fatigued brain, sleep eliminates the rehearsal-induced synaptic fatigue of the circuitry specialized for the task and restores the benefit of early pre-sleep rehearsal. The present findings lend support to the notion that latent sleep-dependent enhancement of performance is a behavioral expression of the brain's restitution in sleep

Sleep-effects on implicit and explicit memory in repeated visual search

In repeated visual search tasks, facilitation of reaction times (RTs) due to repetition of the spatial arrangement of items occurs independently of RT facilitation due to improvements in general task performance. Whereas the latter represents typical procedural learning, the former is a kind of implicit memory that depends on the medial temporal lobe (MTL) memory system and is impaired in patients with amnesia. A third type of memory that develops during visual search is the observers’ explicit knowledge of repeated displays. Here, we used a visual search task to investigate whether procedural memory, implicit contextual cueing, and explicit knowledge of repeated configurations, which all arise independently from the same set of stimuli, are influenced by sleep. Observers participated in two experimental sessions, separated by either a nap or a controlled rest period. In each of the two sessions, they performed a visual search task in combination with an explicit recognition task. We found that (1) across sessions, MTL-independent procedural learning was more pronounced for the nap than rest group. This confirms earlier findings, albeit from different motor and perceptual tasks, showing that procedural memory can benefit from sleep. (2) Likewise, the sleep group compared with the rest group showed enhanced context-dependent configural learning in the second session. This is a novel finding, indicating that the MTL-dependent, implicit memory underlying contextual cueing is also sleep-dependent. (3) By contrast, sleep and wake groups displayed equivalent improvements in explicit recognition memory in the second session. Overall, the current study shows that sleep affects MTL-dependent as well as MTL-independent memory, but it affects different, albeit simultaneously acquired, forms of MTL-dependent memory differentially

Complementary roles of slow-wave sleep and rapid eye movement sleep in emotional memory consolidation

Although rapid eye movement sleep (REM) is regularly implicated in emotional memory consolidation, the role of slow-wave sleep (SWS) in this process is largely uncharacterized. In the present study, we investigated the relative impacts of nocturnal SWS and REM upon the consolidation of emotional memories using functional magnetic resonance imaging (fMRI) and polysomnography (PSG). Participants encoded emotionally positive, negative, and neutral images (remote memories) before a night of PSG-monitored sleep. Twenty-four hours later, they encoded a second set of images (recent memories) immediately before a recognition test in an MRI scanner. SWS predicted superior memory for remote negative images and a reduction in right hippocampal responses during the recollection of these items. REM, however, predicted an overnight increase in hippocampal–neocortical connectivity associated with negative remote memory. These findings provide physiological support for sequential views of sleep-dependent memory processing, demonstrating that SWS and REM serve distinct but complementary functions in consolidation. Furthermore, these findings extend those ideas to emotional memory by showing that, once selectively reorganized away from the hippocampus during SWS, emotionally aversive representations undergo a comparably targeted process during subsequent REM

Pre-sleep experiences shape neural activity and dream content in the sleeping brain

Dreams incorporate recent experiences, and memory-related brain activity is reactivated during sleep, suggesting that dreaming, memory consolidation, and reactivation are tightly linked. We devised a paradigm to investigate whether memory reprocessing during sleep contributes to dreaming. Participants listened to different audiobooks before falling asleep, introducing dissimilar experiences to be processed at night. We show that audiobook content was reprocessed at the neural level using multivariate pattern analyses. Brain activity during rapid eye movement sleep, particularly in the beta range, carried information about the audiobook. While the amount of neural reinstatement did not correlate with memory retention, global beta power during REM sleep was associated with better memory performance. Moreover, blind raters could determine which audiobook participants had studied based on dream reports. Participants who dreamt of the audiobook also showed stronger neural reinstatement. Reprocessing of pre-sleep experiences during sleep may thus shape our brain activity, our dreams, and our memories

Structure-Based Rationale for Selectivity in the Asymmetric Allylic Alkylation of Cycloalkenyl Esters Employing the Trost ‘Standard Ligand’ (TSL): Isolation, Analysis and Alkylation of the Monomeric form of the Cationic η3-Cyclohexenyl Complex [(η3-c-C6H9)Pd(TSL)]+

The solution-phase structures of the monomeric forms of the cationic Pd-η3-allyl and Pd-η3-cyclohexenyl complexes [Pd(R,R)-1(η3-C3H5)]+ (7+) and [Pd(R,R)-1(η3-C6H9)]+ (8+) bearing the trans-cyclohexylenediamine-based Trost ‘Standard Ligand’ (R,R)-1 have been elucidated by NMR, isotopic labeling and computation. In both complexes, (R,R)-1 is found to adopt a C1-symmetric conformation, leading to a concave shape in the 13-membered chelate in which one amide group in the chiral scaffold projects its NH unit out of the concave surface in close vicinity to one allyl terminus. The adjacent amide has a reversed orientation and projects its carbonyl group out of the concave face in the vicinity of the opposite allyl terminus. Stoichiometric and catalytic asymmetric alkylations of [8+][X−] by MCHE2 (E = ester, M = ‘escort’ counterion, X = Pd allyl counterion) show the same selectivities and trends as have been reported for in situ-generated catalysts, and a new model for the enantioselectivity has been explored computationally. Three factors are found to govern the regioselectivity (pro-S vs pro-R) of attack of nucleophiles on the η3-C6H9 ring in 8+ and thus the ee of the alkylation product: (i) a pro-R torquoselective bias is induced by steric interaction of the η3-C6H9 moiety with one phenyl ring of the ligand; (ii) pro-S delivery of the nucleophile can be facilitated by hydrogen-bonding with the concave orientated amide N−H; and (iii) pro-R delivery of the nucleophile can be facilitated by escort ion (M) binding to the concave orientated amide carbonyl. The latter two opposing interactions lead to the selectivity of the alkylation being sensitive to the identities of X− and M+. The generation of 8+ from cyclohexenyl ester substrate has also been explored computationally. The concave orientated amide N−H is able to activate the leaving group of the allylic ester by hydrogen bonding to its carbonyl group. However, this interaction is only feasible for the (S)-enantiomer of substrate, leading to the prediction of a powerful kinetic resolution (kS kR), as is found experimentally. This new model involving two regiochemically distinct (NH) and (CO) locations for nucleofuge or nucleophile binding, may prove of broad utility for the interpretation of the selectivity in asymmetric allylic alkylation reactions catalyzed by Pd complexes of (R,R)-1 and related ligands.<br/

Night sleep in patients with vegetative state

Polysomnographic recording of night sleep was carried out in 15 patients with the diagnosis vegetative state (syn. unresponsive wakefulness syndrome). Sleep scoring was performed by three raters, and confirmed by means of a spectral power analysis of the electroencephalogram, electrooculogram and electromyogram. All patients but one exhibited at least some signs of sleep. In particular, sleep stage N1 was found in 13 patients, N2 in 14 patients, N3 in nine patients, and rapid eye movement sleep in 10 patients. Three patients exhibited all phenomena characteristic for normal sleep, including spindles and rapid eye movements. However, in all but one patient, sleep patterns were severely disturbed as compared with normative data. All patients had frequent and long periods of wakefulness during the night. In some apparent rapid eye movement sleep episodes, no eye movements were recorded. Sleep spindles were detected in five patients only, and their density was very low. We conclude that the majority of vegetative state patients retain some important circadian changes. Further studies are necessary to disentangle multiple factors potentially affecting sleep pattern of vegetative state patients. © 2017 European Sleep Research SocietyThis study was supported by the Deutsche Forschungsgemeinschaft

To Sleep, to Strive, or Both: How Best to Optimize Memory

While numerous studies have shown that a night of sleep profits memory relative to wake, we still have little understanding about what factors mediate this effect of sleep. A clear understanding of the dynamics of this effect of sleep beyond the initial night of sleep is also lacking. Here, we examined the effect of extrinsic rewards on sleep-dependent declarative memory processing across 12 and 24 hr training-retest intervals. Subjects were either paid based on their performance at retest ($1 for each correct answer), or received a flat fee for participation. After a 12 hr interval we observed pronounced benefits of both sleep and reward on memory. Over an extended 24 hr interval we found 1) that an initial night of sleep partially protects memories from subsequent deterioration during wake, and 2) that sleep blocks further deterioration, and may even have a restorative effect on memory, when it follows a full day of wake. Interestingly, the benefit imparted to rewarded (relative to unrewarded) stimuli was equal for sleep and wake subjects, suggesting that the sleeping brain may not differentially process rewarded information, relative to wake. However, looking at the overall impact of sleep relative to reward in this protocol, it was apparent that sleep both imparted a stronger mnemonic boost than reward, and provided a benefit to memory regardless of whether it occurred in the first or the second 12 hrs following task training

Decoding material-specific memory reprocessing during sleep in humans

Neuronal learning activity is reactivated during sleep but the dynamics of this reactivation in humans are still poorly understood. Here we use multivariate pattern classification to decode electrical brain activity during sleep and determine what type of images participants had viewed in a preceding learning session. We find significant patterns of learning-related processing during rapid eye movement (REM) and non-REM (NREM) sleep, which are generalizable across subjects. This processing occurs in a cyclic fashion during time windows congruous to critical periods of synaptic plasticity. Its spatial distribution over the scalp and relevant frequencies differ between NREM and REM sleep. Moreover, only the strength of reprocessing in slow-wave sleep influenced later memory performance, speaking for at least two distinct underlying mechanisms between these states. We thus show that memory reprocessing occurs in both NREM and REM sleep in humans and that it pertains to different aspects of the consolidation process

Memory for Semantically Related and Unrelated Declarative Information: The Benefit of Sleep, the Cost of Wake

Numerous studies have examined sleep's influence on a range of hippocampus-dependent declarative memory tasks, from text learning to spatial navigation. In this study, we examined the impact of sleep, wake, and time-of-day influences on the processing of declarative information with strong semantic links (semantically related word pairs) and information requiring the formation of novel associations (unrelated word pairs). Participants encoded a set of related or unrelated word pairs at either 9am or 9pm, and were then tested after an interval of 30 min, 12 hr, or 24 hr. The time of day at which subjects were trained had no effect on training performance or initial memory of either word pair type. At 12 hr retest, memory overall was superior following a night of sleep compared to a day of wakefulness. However, this performance difference was a result of a pronounced deterioration in memory for unrelated word pairs across wake; there was no sleep-wake difference for related word pairs. At 24 hr retest, with all subjects having received both a full night of sleep and a full day of wakefulness, we found that memory was superior when sleep occurred shortly after learning rather than following a full day of wakefulness. Lastly, we present evidence that the rate of deterioration across wakefulness was significantly diminished when a night of sleep preceded the wake period compared to when no sleep preceded wake, suggesting that sleep served to stabilize the memories against the deleterious effects of subsequent wakefulness. Overall, our results demonstrate that 1) the impact of 12 hr of waking interference on memory retention is strongly determined by word-pair type, 2) sleep is most beneficial to memory 24 hr later if it occurs shortly after learning, and 3) sleep does in fact stabilize declarative memories, diminishing the negative impact of subsequent wakefulness

The consolidation of implicit sequence memory in obstructive sleep apnea

Obstructive Sleep Apnea (OSA) Syndrome is a relatively frequent sleep disorder characterized by disrupted sleep patterns. It is a well-established fact that sleep has beneficial effect on memory consolidation by enhancing neural plasticity. Implicit sequence learning is a prominent component of skill learning. However, the formation and consolidation of this fundamental learning mechanism remains poorly understood in OSA. In the present study we examined the consolidation of different aspects of implicit sequence learning in patients with OSA. We used the Alternating Serial Reaction Time task to measure general skill learning and sequence-specific learning. There were two sessions: a learning phase and a testing phase, separated by a 10-hour offline period with sleep. Our data showed differences in offline changes of general skill learning between the OSA and control group. The control group demonstrated offline improvement from evening to morning, while the OSA group did not. In contrast, we did not observe differences between the groups in offline changes in sequence-specific learning. Our findings suggest that disrupted sleep in OSA differently affects neural circuits involved in the consolidation of sequence learning