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.     

Sleep-Dependent Reactivation of Ensembles in Motor Cortex Promotes Skill Consolidation

Despite many prior studies demonstrating offline behavioral gains in motor skills after sleep, the underlying neural mechanisms remain poorly understood. To investigate the neurophysiological basis for offline gains, we performed single-unit recordings in motor cortex as rats learned a skilled upper-limb task. We found that sleep improved movement speed with preservation of accuracy. These offline improvements were linked to both replay of task-related ensembles during non-rapid eye movement (NREM) sleep and temporal shifts that more tightly bound motor cortical ensembles to movements; such offline gains and temporal shifts were not evident with sleep restriction. Interestingly, replay was linked to the coincidence of slow-wave events and bursts of spindle activity. Neurons that experienced the most consistent replay also underwent the most significant temporal shift and binding to the motor task. Significantly, replay and the associated performance gains after sleep only occurred when animals first learned the skill; continued practice during later stages of learning (i.e., after motor kinematics had stabilized) did not show evidence of replay. Our results highlight how replay of synchronous neural activity during sleep mediates large-scale neural plasticity and stabilizes kinematics during early motor learning.     

Sleep Is Associated with Offline Improvement of Motor Sequence Skill in Children

In adults, sleep is necessary for the offline improvement of certain skills, such as sequential finger tapping, but whether children show a similar effect is still debatable. Here, we tested whether sleep is associated with offline performance improvement in children. Nine- and 11-year-old children trained on an explicit sequential finger tapping task. On the night following training, their parents observed and recorded the duration of each child’s sleep. The following day, all children performed a surprise retest session on the previously trained sequence. In both 9- and 11-year-old children, skill performance was significantly improved during the first retest session relative to the end of training on the previous day, confirming the offline improvement in performance. There was a significant correlation between the degree of improvement and sleep duration the night after training, suggesting that in children, as in adults, sleep is associated with offline skill enhancement.     

Social Rewards Enhance Offline Improvements in Motor Skill

Motor skill memory is first encoded online in a fragile form during practice and then converted into a stable form by offline consolidation, which is the behavioral stage critical for successful learning. Praise, a social reward, is thought to boost motor skill learning by increasing motivation, which leads to increased practice. However, the effect of praise on consolidation is unknown. Here, we tested the hypothesis that praise following motor training directly facilitates skill consolidation. Forty-eight healthy participants were trained on a sequential finger-tapping task. Immediately after training, participants were divided into three groups according to whether they received praise for their own training performance, praise for another participant''s performance, or no praise. Participants who received praise for their own performance showed a significantly higher rate of offline improvement relative to other participants when performing a surprise recall test of the learned sequence. On the other hand, the average performance of the novel sequence and randomly-ordered tapping did not differ between the three experimental groups. These results are the first to indicate that praise-related improvements in motor skill memory are not due to a feedback-incentive mechanism, but instead involve direct effects on the offline consolidation process.     

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.     

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.     

Reward improves long-term retention of a motor memory through induction of offline memory gains

In humans, training in which good performance is rewarded or bad performance punished results in transient behavioral improvements. The relative effects of reward and punishment on consolidation and long-term retention, critical behavioral stages for successful learning, are not known. Here, we investigated the effects of reward and punishment on these different stages of human motor skill learning. We studied healthy subjects who trained on a motor task under rewarded, punished, or neutral control conditions. Performance was tested before and immediately, 6 hr, 24 hr, and 30 days after training in the absence of reward or punishment. Performance improvements immediately after training were comparable in the three groups. At 6 hr, the rewarded group maintained performance gains, whereas the other two groups experienced significant forgetting. At 24 hr, the reward group showed significant offline (posttraining) improvements, whereas the other two groups did not. At 30 days, the rewarded group retained the gains identified at 24 hr, whereas the other two groups experienced significant forgetting. We conclude that training under rewarded conditions is more effective than training under punished or neutral conditions in eliciting lasting motor learning, an advantage driven by offline memory gains that persist over time.     

An FMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning

fMRI was used to investigate the neural substrates supporting implicit and explicit sequence learning, focusing especially upon the role of the medial temporal lobe. Participants performed a serial reaction time task (SRTT). For implicit learning, they were naive about a repeating pattern, whereas for explicit learning, participants memorized another repeating sequence. fMRI analyses comparing repeating versus random sequence blocks demonstrated activation of frontal, parietal, cingulate, and striatal regions implicated in previous SRTT studies. Importantly, mediotemporal lobe regions were active in both explicit and implicit SRTT learning. Moreover, the results provide evidence of a role for the hippocampus and related cortices in the formation of higher order associations under both implicit and explicit learning conditions, regardless of conscious awareness of sequence knowledge.     

Ego Depletion Impairs Implicit Learning

Implicit skill learning occurs incidentally and without conscious awareness of what is learned. However, the rate and effectiveness of learning may still be affected by decreased availability of central processing resources. Dual-task experiments have generally found impairments in implicit learning, however, these studies have also shown that certain characteristics of the secondary task (e.g., timing) can complicate the interpretation of these results. To avoid this problem, the current experiments used a novel method to impose resource constraints prior to engaging in skill learning. Ego depletion theory states that humans possess a limited store of cognitive resources that, when depleted, results in deficits in self-regulation and cognitive control. In a first experiment, we used a standard ego depletion manipulation prior to performance of the Serial Interception Sequence Learning (SISL) task. Depleted participants exhibited poorer test performance than did non-depleted controls, indicating that reducing available executive resources may adversely affect implicit sequence learning, expression of sequence knowledge, or both. In a second experiment, depletion was administered either prior to or after training. Participants who reported higher levels of depletion before or after training again showed less sequence-specific knowledge on the post-training assessment. However, the results did not allow for clear separation of ego depletion effects on learning versus subsequent sequence-specific performance. These results indicate that performance on an implicitly learned sequence can be impaired by a reduction in executive resources, in spite of learning taking place outside of awareness and without conscious intent.     

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.     

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.     

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.     

Watch and learn: seeing is better than doing when acquiring consecutive motor tasks

During motor adaptation learning, consecutive physical practice of two different tasks compromises the retention of the first. However, there is evidence that observational practice, while still effectively aiding acquisition, will not lead to interference and hence prove to be a better practice method. Observers and Actors practised in a clockwise (Task A) followed by a counterclockwise (Task B) visually rotated environment, and retention was immediately assessed. An Observe-all and Act-all group were compared to two groups who both physically practised Task A, but then only observed (ObsB) or did not see or practice Task B (NoB). The two observer groups and the NoB control group better retained Task A than Actors, although importantly only the observer groups learnt Task B. RT data and explicit awareness of the rotation suggested that the observers had acquired their respective tasks in a more strategic manner than Actor and Control groups. We conclude that observational practice benefits learning of multiple tasks more than physical practice due to the lack of updating of implicit, internal models for aiming in the former.     

Visuospatial Sequence Learning without Seeing

Background

The ability to detect and integrate associations between unrelated items that are close in space and time is a key feature of human learning and memory. Learning sequential associations between non-adjacent visual stimuli (higher-order visuospatial dependencies) can occur either with or without awareness (explicit vs. implicit learning) of the products of learning. Existing behavioural and neurocognitive studies of explicit and implicit sequence learning, however, are based on conscious access to the sequence of target locations and, typically, on conditions where the locations for orienting, or motor, responses coincide with the locations of the target sequence.

Methodology/Principal Findings

Dichoptic stimuli were presented on a novel sequence learning task using a mirror stereoscope to mask the eye-of-origin of visual input from conscious awareness. We demonstrate that conscious access to the sequence of target locations and responses that coincide with structure of the target sequence are dispensable features when learning higher-order visuospatial associations. Sequence knowledge was expressed in the ability of participants to identify the trained higher-order visuospatial sequence on a recognition test, even though the trained and untrained recognition sequences were identical when viewed at a conscious binocular level, and differed only at the level of the masked sequential associations.

Conclusions/Significance

These results demonstrate that unconscious processing can support perceptual learning of higher-order sequential associations through interocular integration of retinotopic-based codes stemming from monocular eye-of-origin information. Furthermore, unlike other forms of perceptual associative learning, visuospatial attention did not need to be directed to the locations of the target sequence. More generally, the results pose a challenge to neural models of learning to account for a previously unknown capacity of the human visual system to support the detection, learning and recognition of higher-order sequential associations under conditions where observers are unable to see the target sequence or perform responses that coincide with structure of the target sequence.     

Multidisciplinary Views on Applying Explicit and Implicit Motor Learning in Practice: An International Survey

Background

A variety of options and techniques for causing implicit and explicit motor learning have been described in the literature. The aim of the current paper was to provide clearer guidance for practitioners on how to apply motor learning in practice by exploring experts’ opinions and experiences, using the distinction between implicit and explicit motor learning as a conceptual departure point.

Methods

A survey was designed to collect and aggregate informed opinions and experiences from 40 international respondents who had demonstrable expertise related to motor learning in practice and/or research. The survey was administered through an online survey tool and addressed potential options and learning strategies for applying implicit and explicit motor learning. Responses were analysed in terms of consensus (≥ 70%) and trends (≥ 50%). A summary figure was developed to illustrate a taxonomy of the different learning strategies and options indicated by the experts in the survey.

Results

Answers of experts were widely distributed. No consensus was found regarding the application of implicit and explicit motor learning. Some trends were identified: Explicit motor learning can be promoted by using instructions and various types of feedback, but when promoting implicit motor learning, instructions and feedback should be restricted. Further, for implicit motor learning, an external focus of attention should be considered, as well as practicing the entire skill. Experts agreed on three factors that influence motor learning choices: the learner’s abilities, the type of task, and the stage of motor learning (94.5%; n = 34/36). Most experts agreed with the summary figure (64.7%; n = 22/34).

Conclusion

The results provide an overview of possible ways to cause implicit or explicit motor learning, signposting examples from practice and factors that influence day-to-day motor learning decisions.     

Sequence Skill Acquisition and Off-Line Learning in Normal Aging

It is well known that certain cognitive abilities decline with age. The ability to form certain new declarative memories, particularly memories for facts and events, has been widely shown to decline with advancing age. In contrast, the effects of aging on the ability to form new procedural memories such as skills are less well known, though it appears that older adults are able to acquire some new procedural skills over practice. The current study examines the effects of normal aging on procedural memory more closely by comparing the effects of aging on the encoding or acquisition stage of procedural learning versus its effects on the consolidation, or between-session stage of procedural learning. Twelve older and 14 young participants completed a sequence-learning task (the Serial Reaction Time Task) over a practice session and at a re-test session 24 hours later. Older participants actually demonstrated more sequence skill during acquisition than the young. However, older participants failed to show skill improvement at re-test as the young participants did. Age thus appears to have a differential effect upon procedural learning stages such that older adults'' skill acquisition remains relatively intact, in some cases even superior, compared to that of young adults, while their skill consolidation may be poorer than that of young adults. Although the effect of normal aging on procedural consolidation remains unclear, aging may actually enhance skill acquisition on some procedural tasks.     

The role of medial temporal lobe structures in implicit learning: an event-related FMRI study

The medial temporal lobe (MTL) has been associated with declarative learning of flexible relational rules and the basal ganglia with implicit learning of stimulus-response mappings. It remains an open question of whether MTL or basal ganglia are involved when learning flexible relational contingencies without awareness. We studied learning of an explicit stimulus-response association with fMRI. Embedded in this explicit task was a hidden structure that was learnt implicitly. Implicit learning of the sequential regularities of the "hidden rule" activated the ventral perirhinal cortex, within the MTL, whereas learning the fixed stimulus-response associations activated the basal ganglia, indicating that the function of the MTL and the basal ganglia depends on the learned material and not necessarily on the participants' awareness.     

Both the hippocampus and striatum are involved in consolidation of motor sequence memory

Functional magnetic resonance imaging (fMRI) was used to investigate the cerebral correlates of motor sequence memory consolidation. Participants were scanned while training on an implicit oculomotor sequence learning task and during a single testing session taking place 30 min, 5 hr, or 24 hr later. During training, responses observed in hippocampus and striatum were linearly related to the gain in performance observed overnight, but not over the day. Responses in both structures were significantly larger at 24 hr than at 30 min or 5 hr. Additionally, the competitive interaction observed between these structures during training became cooperative overnight. These results stress the importance of both hippocampus and striatum in procedural memory consolidation. Responses in these areas during training seem to condition the overnight memory processing that is associated with a change in their functional interactions. These results show that both structures interact during motor sequence consolidation to optimize subsequent behavior.     

The Effect of an Acute Bout of Moderate-Intensity Aerobic Exercise on Motor Learning of a Continuous Tracking Task

Introduction

There is evidence for beneficial effects of acute and long-term exercise interventions on several forms of memory, including procedural motor learning. In the present study we examined how performing a single bout of continuous moderate intensity aerobic exercise would impact motor skill acquisition and retention in young healthy adults, compared to a period of rest. We hypothesized that exercise would improve motor skill acquisition and retention, compared to motor practice alone.

Materials and Methods

Sixteen healthy adults completed sessions of aerobic exercise or seated rest that were immediately followed by practice of a novel motor task (practice). Exercise consisted of 30 minutes of continuous cycling at 60% peak O₂ uptake. Twenty-four hours after practice, we assessed motor learning with a no-exercise retention test (retention). We also quantified changes in offline motor memory consolidation, which occurred between practice and retention (offline). Tracking error was separated into indices of temporal precision and spatial accuracy.

Results

There were no differences between conditions in the timing of movements during practice (p = 0.066), at retention (p = 0.761), or offline (p = 0.966). However, the exercise condition enabled participants to maintain spatial accuracy during practice (p = 0.477); whereas, following rest performance diminished (p = 0.050). There were no significant differences between conditions at retention (p = 0.532) or offline (p = 0.246).

Discussion

An acute bout of moderate-intensity aerobic exercise facilitated the maintenance of motor performance during skill acquisition, but did not influence motor learning. Given past work showing that pairing high intensity exercise with skilled motor practice benefits learning, it seems plausible that intensity is a key modulator of the effects of acute aerobic exercise on changes in complex motor behavior. Further work is necessary to establish a dose-response relationship between aerobic exercise and motor learning.     

When Money Is Not Enough: Awareness,Success, and Variability in Motor Learning

When performing a skill such as throwing a dart, many different combinations of joint motions suffice to hit the target. The motor system adapts rapidly to reduce bias in the desired outcome (i.e., the first-order moment of the error); however, the essence of skill is to produce movements with less variability (i.e., to reduce the second-order moment). It is easy to see how feedback about success or failure could sculpt performance to achieve this aim. However, it is unclear whether the dimensions responsible for success or failure need to be known explicitly by the subjects, or whether learning can proceed without explicit awareness of the movement parameters that need to change. Here, we designed a redundant, two-dimensional reaching task in which we could selectively manipulate task success and the variability of action outcomes, whilst also manipulating awareness of the dimension along which performance could be improved. Variability was manipulated either by amplifying natural errors, leaving the correlation between the executed movement and the visual feedback intact, or by adding extrinsic noise, decorrelating movement and feedback. We found that explicit, binary, feedback about success or failure was only sufficient for learning when participants were aware of the dimension along which motor behavior had to change. Without such awareness, learning was only present when extrinsic noise was added to the feedback, but not when task success or variability was manipulated in isolation; learning was also much slower. Our results highlight the importance of conscious awareness of the relevant dimension during motor learning, and suggest that higher-order moments of outcome signals are likely to play a significant role in skill learning in complex tasks.