Awareness modifies the skill-learning benefits of sleep

Behind every skilled movement lies months of practice. However, practice alone is not responsible for the acquisition of all skill; performance can improve between, not just within, practice sessions. An important principle shaping these offline improvements may be an individual's awareness of learning a new skill. New skills, such as a sequence of finger movements, can be learned unintentionally (with little awareness for the sequence, implicit learning) or intentionally (explicit learning). We measured skill in an implicit and explicit sequence-learning task before and after a 12 hr interval. This interval either did (8 p.m. to 8 a.m.) or did not (8 a.m. to 8 p.m.) include a period of sleep. Following explicit sequence learning, offline skill improvements were only observed when the 12 hr interval included sleep. This overnight improvement was correlated with the amount of NREM sleep. The same improvement could also be observed in the evening (with an interval from 8 p.m. to 8 p.m.), so it was not coupled to retesting at a particular time of day and cannot therefore be attributed to circadian factors. In contrast, in the implicit learning task, offline learning was observed regardless of whether the 12 hr interval did or did not contain a period of sleep. However, these improvements were not observed with only a 15 min interval between sessions. Therefore, the practice available within each session cannot account for these skill improvements. Instead, sufficient time is necessary for offline learning to occur. These results show a behavioral dissociation, based upon an individual's awareness for having learned a sequence of finger movements. Offline learning is sleep dependent for explicit skills but time dependent for implicit skills.     

Here Today,Gone Tomorrow – Adaptation to Change in Memory-Guided Visual Search

Visual search for a target object can be facilitated by the repeated presentation of an invariant configuration of nontargets (‘contextual cueing’). Here, we tested adaptation of learned contextual associations after a sudden, but permanent, relocation of the target. After an initial learning phase targets were relocated within their invariant contexts and repeatedly presented at new locations, before they returned to the initial locations. Contextual cueing for relocated targets was neither observed after numerous presentations nor after insertion of an overnight break. Further experiments investigated whether learning of additional, previously unseen context-target configurations is comparable to adaptation of existing contextual associations to change. In contrast to the lack of adaptation to changed target locations, contextual cueing developed for additional invariant configurations under identical training conditions. Moreover, across all experiments, presenting relocated targets or additional contexts did not interfere with contextual cueing of initially learned invariant configurations. Overall, the adaptation of contextual memory to changed target locations was severely constrained and unsuccessful in comparison to learning of an additional set of contexts, which suggests that contextual cueing facilitates search for only one repeated target location.     

Effect of daytime nap on consolidation of declarative memory in humans

We studied effects of a daytime nap (1 hour) with including only NREM sleep on performance of declarative memory task (60 semantically unrelated word pairs) and general functional state. During training, procedure of learning of 30 word pairs was presented once, and that of the other 30 pairs was repeated twice. Strength of the task acquisition was tested. Subjects participated in two experiments: basic and control one. After learning participants either took a nap (basic experiment) or kept awake looking movies (control experiment). In 4.5 hours after the training session all the subjects were retested. As compared to the subjects who stayed awake during the training-retesting interval, subjects who had a NREM nap demonstrated enhanced performance. Concerning the strength of task acquisition, sleep-dependent performance was observed only for the word pairs learned once. Naps did not affect the functional state assessed by the reaction time dynamics and psychological testing.     

No childhood advantage in the acquisition of skill in using an artificial language rule

A leading notion is that language skill acquisition declines between childhood and adulthood. While several lines of evidence indicate that declarative ("what", explicit) memory undergoes maturation, it is commonly assumed that procedural ("how-to", implicit) memory, in children, is well established. The language superiority of children has been ascribed to the childhood reliance on implicit learning. Here we show that when 8-year-olds, 12-year-olds and young adults were provided with an equivalent multi-session training experience in producing and judging an artificial morphological rule (AMR), adults were superior to children of both age groups and the 8-year-olds were the poorest learners in all task parameters including in those that were clearly implicit. The AMR consisted of phonological transformations of verbs expressing a semantic distinction: whether the preceding noun was animate or inanimate. No explicit instruction of the AMR was provided. The 8-year-olds, unlike most adults and 12-year-olds, failed to explicitly uncover the semantic aspect of the AMR and subsequently to generalize it accurately to novel items. However, all participants learned to apply the AMR to repeated items and to generalize its phonological patterns to novel items, attaining accurate and fluent production, and exhibiting key characteristics of procedural memory. Nevertheless, adults showed a clear advantage in learning implicit task aspects, and in their long-term retention. Thus, our findings support the notion of age-dependent maturation in the establishment of declarative but also of procedural memory in a complex language task. In line with recent reports of no childhood advantage in non-linguistic skill learning, we propose that under some learning conditions adults can effectively express their language skill acquisition potential. Altogether, the maturational effects in the acquisition of an implicit AMR do not support a simple notion of a language skill learning advantage in children.     

Sleep-dependent consolidation of contextual learning

Memory consolidation is facilitated by sleep. Specifying the functional domain of sleep-dependent consolidation (SDC) is important for identifying the neural mechanisms underlying this phenomenon. Previous work indicates that SDC may be limited to conditions in which learning is explicit. In the present study, we tested the hypothesis that SDC may also occur with implicit learning when learning benefits from the formation of contextual associations, a function associated with the hippocampus. Three versions of the serial-reaction-time task (SRTT) were examined, and SDC was assessed by comparing performance after 12 hr breaks that included or did not include sleep. SDC was observed in the Explicit condition. Two implicit conditions were compared. In the Implicit Noncontextual condition, participants performed a concurrent tone-counting task with the pitch of each tone selected at random, precluding cross-dimensional associations. In the Implicit Contextual condition, participants responded to the color of the cues while the spatial location of the cues followed a correlated sequence. Whereas learning was observed in both implicit conditions, SDC was restricted to the contextual condition. Given that the formation of contextual associations is dependent on the hippocampus, we suggest that SDC is a hippocampus-mediated process.     

Implicit Versus Explicit Local Contextual Processing

We investigated the effects of implicit local contextual processing using behavioral and electrophysiological measures. EEG recording blocks consisted of targets preceded by either randomized sequences of standards or by sequences including a predictive sequence signaling the occurrence of a target event. Subjects performed two sessions: in the first the regularity of the predictive sequence was implicit, while in the second this regularity was made explicit. Subjects pressed a button in response to targets. Both the implicit and explicit sessions showed shorter reaction times and peak P3b latencies for predicted versus random targets, although to a greater extent in the explicit session. In both sessions the middle and last most-informative stimuli of the three-standard predictive sequence induced a significant larger P3b compared with randomized standards. The findings show that local contextual information is processed implicitly, but that this modulation was significantly greater when subjects were explicitly instructed to attend to target-predictive contextual information. The findings suggest that top-down attentional networks have a role in modulating the extent to which contextual information is utilized.     

Relational memory: a daytime nap facilitates the abstraction of general concepts

It is increasingly evident that sleep strengthens memory. However, it is not clear whether sleep promotes relational memory, resultant of the integration of disparate memory traces into memory networks linked by commonalities. The present study investigates the effect of a daytime nap, immediately after learning or after a delay, on a relational memory task that requires abstraction of general concept from separately learned items. Specifically, participants learned English meanings of Chinese characters with overlapping semantic components called radicals. They were later tested on new characters sharing the same radicals and on explicitly stating the general concepts represented by the radicals. Regardless of whether the nap occurred immediately after learning or after a delay, the nap participants performed better on both tasks. The results suggest that sleep--even as brief as a nap--facilitates the reorganization of discrete memory traces into flexible relational memory networks.     

Learning to Attend to Threat Accelerates and Enhances Memory Consolidation

Practice on a procedural task involves within-session learning and between-session consolidation of learning, with the latter requiring a minimum of about four hours to evolve due to involvement of slower cellular processes. Learning to attend to threats is vital for survival and thus may involve faster memory consolidation than simple procedural learning. Here, we tested whether attention to threat modulates the time-course and magnitude of learning and memory consolidation effects associated with skill practice. All participants (N = 90) practiced in two sessions on a dot-probe task featuring pairs of neutral and angry faces followed by target probes which were to be discriminated as rapidly as possible. In the attend-threat training condition, targets always appeared at the angry face location, forming an association between threat and target location; target location was unrelated to valence in a control training condition. Within each attention training condition, duration of the between-session rest interval was varied to establish the time-course for emergence of consolidation effects. During the first practice session, we observed robust improvement in task performance (online, within-session gains), followed by saturation of learning. Both training conditions exhibited similar overall learning capacities, but performance in the attend-threat condition was characterized by a faster learning rate relative to control. Consistent with the memory consolidation hypothesis, between-session performance gains (delayed gains) were observed only following a rest interval. However, rest intervals of 1 and 24 hours yielded similar delayed gains, suggesting accelerated consolidation processes. Moreover, attend-threat training resulted in greater delayed gains compared to the control condition. Auxiliary analyses revealed that enhanced performance was retained over several months, and that training to attend to neutral faces resulted in effects similar to control. These results provide a novel demonstration of how attention to threat can accelerate and enhance memory consolidation effects associated with skill acquisition.     

Rapid-Eye-Movement-Sleep (REM) Associated Enhancement of Working Memory Performance after a Daytime Nap

The main objective was to study the impact of a daytime sleep opportunity on working memory and the mechanism behind such impact. This study adopted an experimental design in a sleep research laboratory. Eighty healthy college students (Age:17-23, 36 males) were randomized to either have a polysomnography-monitored daytime sleep opportunity (Nap-group, n=40) or stay awake (Wake-group, n=40) between the two assessment sessions. All participants completed a sleep diary and wore an actigraph-watch for 5 days before and one day after the assessment sessions. They completed the state-measurement of sleepiness and affect, in addition to a psychomotor vigilance test and a working memory task before and after the nap/wake sessions. The two groups did not differ in their sleep characteristics prior to and after the lab visit. The Nap-group had higher accuracy on the working memory task, fewer lapses on the psychomotor vigilance test and lower state-sleepiness than the Wake-group. Within the Nap-group, working memory accuracy was positively correlated with duration of rapid eye movement sleep (REM) and total sleep time during the nap. Our findings suggested that “sleep gain” during a daytime sleep opportunity had significant positive impact on working memory performance, without affecting subsequent nighttime sleep in young adult, and such impact was associated with the duration of REM. While REM abnormality has long been noted in pathological conditions (e.g. depression), which are also presented with cognitive dysfunctions (e.g. working memory deficits), this was the first evidence showing working memory enhancement associated with REM in daytime napping in college students, who likely had habitual short sleep duration but were otherwise generally healthy.     

Daytime Sleep Enhances Consolidation of the Spatial but Not Motoric Representation of Motor Sequence Memory

Motor sequence learning is known to rely on more than a single process. As the skill develops with practice, two different representations of the sequence are formed: a goal representation built under spatial allocentric coordinates and a movement representation mediated through egocentric motor coordinates. This study aimed to explore the influence of daytime sleep (nap) on consolidation of these two representations. Through the manipulation of an explicit finger sequence learning task and a transfer protocol, we show that both allocentric (spatial) and egocentric (motor) representations of the sequence can be isolated after initial training. Our results also demonstrate that nap favors the emergence of offline gains in performance for the allocentric, but not the egocentric representation, even after accounting for fatigue effects. Furthermore, sleep-dependent gains in performance observed for the allocentric representation are correlated with spindle density during non-rapid eye movement (NREM) sleep of the post-training nap. In contrast, performance on the egocentric representation is only maintained, but not improved, regardless of the sleep/wake condition. These results suggest that motor sequence memory acquisition and consolidation involve distinct mechanisms that rely on sleep (and specifically, spindle) or simple passage of time, depending respectively on whether the sequence is performed under allocentric or egocentric coordinates.     

Linking implicit and explicit memory: common encoding factors and shared representations

Dissociations between implicit and explicit memory have featured prominently in theories of human memory. However, similarities between the two forms of memory have been less studied. One open question concerns whether implicit and explicit memory share encoding resources. To explore this question, we employed a subsequent memory design in which several novel scenes were repeated once during an fMRI session and explicit memory for the scenes was unexpectedly tested afterward. Subsequently remembered scenes produced more behavioral priming and neural attenuation-two conventional measures of implicit memory-than did subsequently forgotten scenes. Moreover, brain-behavior correlations between these two implicit measures were mediated by subsequent memory. Finally, tonic activity, possibly reflecting the natural time course of attention, was predictive of subsequent memory. These results suggest that implicit and explicit memory are subject to the same encoding factors and can rely on similar perceptual processes and representations.     

Reexposure to a sensorimotor perturbation produces opposite effects on explicit and implicit learning processes

The motor system demonstrates an exquisite ability to adapt to changes in the environment and to quickly reset when these changes prove transient. If similar environmental changes are encountered in the future, learning may be faster, a phenomenon known as savings. In studies of sensorimotor learning, a central component of savings is attributed to the explicit recall of the task structure and appropriate compensatory strategies. Whether implicit adaptation also contributes to savings remains subject to debate. We tackled this question by measuring, in parallel, explicit and implicit adaptive responses in a visuomotor rotation task, employing a protocol that typically elicits savings. While the initial rate of learning was faster in the second exposure to the perturbation, an analysis decomposing the 2 processes showed the benefit to be solely associated with explicit re-aiming. Surprisingly, we found a significant decrease after relearning in aftereffect magnitudes during no-feedback trials, a direct measure of implicit adaptation. In a second experiment, we isolated implicit adaptation using clamped visual feedback, a method known to eliminate the contribution of explicit learning processes. Consistent with the results of the first experiment, participants exhibited a marked reduction in the adaptation function, as well as an attenuated aftereffect when relearning from the clamped feedback. Motivated by these results, we reanalyzed data from prior studies and observed a consistent, yet unappreciated pattern of attenuation of implicit adaptation during relearning. These results indicate that explicit and implicit sensorimotor processes exhibit opposite effects upon relearning: Explicit learning shows savings, while implicit adaptation becomes attenuated

Humans learning a new motor task typically improve with repeated practice due to the faster expression of more effective explicit strategies; this study reveals that when motor learning occurs without awareness, performance deteriorates upon relearning.     

Sleep-dependent facilitation of episodic memory details

While a role for sleep in declarative memory processing is established, the qualitative nature of this consolidation benefit, and the physiological mechanisms mediating it, remain debated. Here, we investigate the impact of sleep physiology on characteristics of episodic memory using an item- (memory elements) and context- (contextual details associated with those elements) learning paradigm; the latter being especially dependent on the hippocampus. Following back-to-back encoding of two word lists, each associated with a different context, participants were assigned to either a Nap-group, who obtained a 120-min nap, or a No Nap-group. Six hours post-encoding, participants performed a recognition test involving item-memory and context-memory judgments. In contrast to item-memory, which demonstrated no between-group differences, a significant benefit in context-memory developed in the Nap-group, the extent of which correlated both with the amount of stage-2 NREM sleep and frontal fast sleep-spindles. Furthermore, a difference was observed on the basis of word-list order, with the sleep benefit and associated physiological correlations being selective for the second word-list, learned last (most proximal to sleep). These findings suggest that sleep may preferentially benefit contextual (hippocampal-dependent) aspects of memory, supported by sleep-spindle oscillations, and that the temporal order of initial learning differentially determines subsequent offline consolidation.     

After Being Challenged by a Video Game Problem,Sleep Increases the Chance to Solve It

In the past years many studies have demonstrated the role of sleep on memory consolidation. It is known that sleeping after learning a declarative or non-declarative task, is better than remaining awake. Furthermore, there are reports of a possible role for dreams in consolidation of declarative memories. Other studies have reported the effect of naps on memory consolidation. With similar protocols, another set of studies indicated that sleep has a role in creativity and problem-solving. Here we hypothesised that sleep can increase the likelihood of solving problems. After struggling to solve a video game problem, subjects who took a nap (n = 14) were almost twice as likely to solve it when compared to the wake control group (n = 15). It is interesting to note that, in the nap group 9 out 14 subjects engaged in slow-wave sleep (SWS) and all solved the problem. Surprisingly, we did not find a significant involvement of Rapid Eye Movement (REM) sleep in this task. Slow-wave sleep is believed to be crucial for the transfer of memory-related information to the neocortex and implement intentions. Sleep can benefit problem-solving through the generalisation of newly encoded information and abstraction of the gist. In conclusion, our results indicate that sleep, even a nap, can potentiate the solution of problems that involve logical reasoning. Thus, sleep''s function seems to go beyond memory consolidation to include managing of everyday-life events.     

Assessing implicit odor localization in humans using a cross-modal spatial cueing paradigm

Background

Navigation based on chemosensory information is one of the most important skills in the animal kingdom. Studies on odor localization suggest that humans have lost this ability. However, the experimental approaches used so far were limited to explicit judgements, which might ignore a residual ability for directional smelling on an implicit level without conscious appraisal.

Methods

A novel cueing paradigm was developed in order to determine whether an implicit ability for directional smelling exists. Participants performed a visual two-alternative forced choice task in which the target was preceded either by a side-congruent or a side-incongruent olfactory spatial cue. An explicit odor localization task was implemented in a second experiment.

Results

No effect of cue congruency on mean reaction times could be found. However, a time by condition interaction emerged, with significantly slower responses to congruently compared to incongruently cued targets at the beginning of the experiment. This cueing effect gradually disappeared throughout the course of the experiment. In addition, participants performed at chance level in the explicit odor localization task, thus confirming the results of previous research.

Conclusion

The implicit cueing task suggests the existence of spatial information processing in the olfactory system. Response slowing after a side-congruent olfactory cue is interpreted as a cross-modal attentional interference effect. In addition, habituation might have led to a gradual disappearance of the cueing effect. It is concluded that under immobile conditions with passive monorhinal stimulation, humans are unable to explicitly determine the location of a pure odorant. Implicitly, however, odor localization seems to exert an influence on human behaviour. To our knowledge, these data are the first to show implicit effects of odor localization on overt human behaviour and thus support the hypothesis of residual directional smelling in humans.     

Implicit and Explicit Contributions to Object Recognition: Evidence from Rapid Perceptual Learning

The present study investigated implicit and explicit recognition processes of rapidly perceptually learned objects by means of steady-state visual evoked potentials (SSVEP). Participants were initially exposed to object pictures within an incidental learning task (living/non-living categorization). Subsequently, degraded versions of some of these learned pictures were presented together with degraded versions of unlearned pictures and participants had to judge, whether they recognized an object or not. During this test phase, stimuli were presented at 15 Hz eliciting an SSVEP at the same frequency. Source localizations of SSVEP effects revealed for implicit and explicit processes overlapping activations in orbito-frontal and temporal regions. Correlates of explicit object recognition were additionally found in the superior parietal lobe. These findings are discussed to reflect facilitation of object-specific processing areas within the temporal lobe by an orbito-frontal top-down signal as proposed by bi-directional accounts of object recognition.     

Visual Search Elicits the Electrophysiological Marker of Visual Working Memory

Background

Although limited in capacity, visual working memory (VWM) plays an important role in many aspects of visually-guided behavior. Recent experiments have demonstrated an electrophysiological marker of VWM encoding and maintenance, the contralateral delay activity (CDA), which has been shown in multiple tasks that have both explicit and implicit memory demands. Here, we investigate whether the CDA is evident during visual search, a thoroughly-researched task that is a hallmark of visual attention but has no explicit memory requirements.

Methodology/Principal Findings

The results demonstrate that the CDA is present during a lateralized search task, and that it is similar in amplitude to the CDA observed in a change-detection task, but peaks slightly later. The changes in CDA amplitude during search were strongly correlated with VWM capacity, as well as with search efficiency. These results were paralleled by behavioral findings showing a strong correlation between VWM capacity and search efficiency.

Conclusions/Significance

We conclude that the activity observed during visual search was generated by the same neural resources that subserve VWM, and that this activity reflects the maintenance of previously searched distractors.     

The Effects of a Nap Opportunity in Quiet and Noisy Environments on Driving Performance

While napping has previously been shown to alleviate the effects of sleep loss, before advocating the use of naps in transport accident campaigns it is necessary to consider whether a nap opportunity in a noisy uncomfortable environment can produce the same benefits as a nap opportunity in conditions that are conducive to sleep. To examine this, eight participants drove a driving simulator for 50 min at 11:00 h on three different test days. The simulator used has previously been found to be sensitive to the effects of sleep loss, alcohol consumption, and time of day. All three sessions were conducted after one night of sleep loss. Prior to driving during each session the participants either had a 60 min nap opportunity in a quiet or noisy environment, or no nap opportunity. Driving performance and reaction time while driving were measured, as were subjective sleepiness and ratings of sleep quality. No significant benefits of nap opportunities on driving performance were found. Levels of subjective sleepiness were not affected by the nap opportunity condition; however, sleep was rated as more refreshing and restful after a nap in a quiet environment compared to noisy environment. The measures of effect size reported suggest further research is required to unequivocally test the effects of nap opportunities on driving ability.     

The effects of a nap opportunity in quiet and noisy environments on driving performance

While napping has previously been shown to alleviate the effects of sleep loss, before advocating the use of naps in transport accident campaigns it is necessary to consider whether a nap opportunity in a noisy uncomfortable environment can produce the same benefits as a nap opportunity in conditions that are conducive to sleep. To examine this, eight participants drove a driving simulator for 50 min at 11:00 h on three different test days. The simulator used has previously been found to be sensitive to the effects of sleep loss, alcohol consumption, and time of day. All three sessions were conducted after one night of sleep loss. Prior to driving during each session the participants either had a 60 min nap opportunity in a quiet or noisy environment, or no nap opportunity. Driving performance and reaction time while driving were measured, as were subjective sleepiness and ratings of sleep quality. No significant benefits of nap opportunities on driving performance were found. Levels of subjective sleepiness were not affected by the nap opportunity condition; however, sleep was rated as more refreshing and restful after a nap in a quiet environment compared to noisy environment. The measures of effect size reported suggest further research is required to unequivocally test the effects of nap opportunities on driving ability.