Temporal cluster-based organization of sleep spindles underlies motor memory consolidation.

Sleep benefits motor memory consolidation, which is mediated by sleep spindle activity and associated memory reactivations during non-rapid eye movement (NREM) sleep. However, the particular role of NREM2 and NREM3 sleep spindles and the mechanisms triggering this memory consolidation process remain unclear. Here, simultaneous electroencephalographic and functional magnetic resonance imaging (EEG-fMRI) recordings were collected during night-time sleep following the learning of a motor sequence task. Adopting a time-based clustering approach, we provide evidence that spindles iteratively occur within clustered and temporally organized patterns during both NREM2 and NREM3 sleep. However, the clustering of spindles in trains is related to motor memory consolidation during NREM2 sleep only. Altogether, our findings suggest that spindles' clustering and rhythmic occurrence during NREM2 sleep may serve as an intrinsic rhythmic sleep mechanism for the timed reactivation and subsequent consolidation of motor memories, through synchronized oscillatory activity within a subcortical-cortical network involved during learning.

Sleep-related motor skill consolidation and generalizability after physical practice, motor imagery, and action observation.

Sleep benefits the consolidation of motor skills learned by physical practice, mainly through periodic thalamocortical sleep spindle activity. However, motor skills can be learned without overt movement through motor imagery or action observation. Here, we investigated whether sleep spindle activity also supports the consolidation of non-physically learned movements. Forty-five electroencephalographic sleep recordings were collected during a daytime nap after motor sequence learning by physical practice, motor imagery, or action observation. Our findings reveal that a temporal cluster-based organization of sleep spindles underlies motor memory consolidation in all groups, albeit with distinct behavioral outcomes. A daytime nap offers an early sleep window promoting the retention of motor skills learned by physical practice and motor imagery, and its generalizability toward the inter-manual transfer of skill after action observation. Findings may further have practical impacts with the development of non-physical rehabilitation interventions for patients having to remaster skills following peripherical or brain injury.

Conscious awareness of others' actions during observational learning does not benefit motor skill performance.

The conscious awareness of motor success during motor learning has recently been revealed as a learning factor. In these studies, participants had to learn a motor sequence and to detect when they assumed the execution had reached a maximal fluidity. The consciousness groups showed better motor performance during a delayed post-training test than the non-consciousness control groups. Based on the "similar mechanism" hypothesis between observational and physical practice, we tested this beneficial effect of the conscious awareness of action in an observational learning context. In the present study, two groups learned a motor sequence task by observing a videotaped human model performing the task. However, only the consciousness group had to detect the maximal fluidity of the learning human model during observational practice. Unpredictably, no difference was detected between groups during the post-training test. However, the consciousness group outperformed the non-consciousness control group for tests that assessed the motor knowledges.

Conscious awareness of motor fluidity improves performance and decreases cognitive effort in sequence learning.

Motor skill learning is improved when participants are instructed to judge after each trial whether their performed movements have reached maximal fluidity. Consequently, the conscious awareness of this maximal fluidity can be classified as a genuine learning factor for motor sequences. However, it is unknown whether this effect of conscious awareness on motor learning could be mediated by the increased cognitive effort that may accompany such judgment making. The main aim of this study was to test this hypothesis in comparing two groups with, and without, the conscious awareness of the maximal fluidity. To assess the possible involvement of cognitive effort, we have recorded the pupillary dilation to the task, which is well-known to increase in proportion to cognitive effort. Results confirmed that conscious awareness indeed improved motor sequence learning of the trained sequence specifically. Pupil dilation was smaller during trained than during novel sequence performance, indicating that sequence learning decreased the cognitive cost of sequence execution. However, we found that in the group that had to judge on their maximal fluidity, pupil dilation during sequence production was smaller than in the control group, indicating that the motor improvement induced by the fluidity judgment does not involve additional cognitive effort. We discuss these results in the context of motor learning and cognitive effort theories.

A sleep spindle framework for motor memory consolidation.

Sleep spindle activity has repeatedly been found to contribute to brain plasticity and consolidation of both declarative and procedural memories. Here we propose a framework for motor memory consolidation that outlines the essential contribution of the hierarchical and multi-scale periodicity of spindle activity, as well as of the synchronization and interaction of brain oscillations during this sleep-dependent process. We posit that the clustering of sleep spindles in 'trains', together with the temporally organized alternation between spindles and associated refractory periods, is critical for efficient reprocessing and consolidation of motor memories. We further argue that the long-term retention of procedural memories relies on the synchronized (functional connectivity) local reprocessing of new information across segregated, but inter-connected brain regions that are involved in the initial learning process. Finally, we propose that oscillatory synchrony in the spindle frequency band may reflect the cross-structural reactivation, reorganization and consolidation of motor, and potentially declarative, memory traces within broader subcortical-cortical networks during sleep. This article is part of the Theo Murphy meeting issue 'Memory reactivation: replaying events past, present and future'.

Consolidation alters motor sequence-specific distributed representations.

Functional magnetic resonance imaging (fMRI) studies investigating the acquisition of sequential motor skills in humans have revealed learning-related functional reorganizations of the cortico-striatal and cortico-cerebellar motor systems accompanied with an initial hippocampal contribution. Yet, the functional significance of these activity-level changes remains ambiguous as they convey the evolution of both sequence-specific knowledge and unspecific task ability. Moreover, these changes do not specifically assess the occurrence of learning-related plasticity. To address these issues, we investigated local circuits tuning to sequence-specific information using multivariate distances between patterns evoked by consolidated or newly acquired motor sequences production. The results reveal that representations in dorsolateral striatum, prefrontal and secondary motor cortices are greater when executing consolidated sequences than untrained ones. By contrast, sequence representations in the hippocampus and dorsomedial striatum becomes less engaged. Our findings show, for the first time in humans, that complementary sequence-specific motor representations evolve distinctively during critical phases of skill acquisition and consolidation.

Susceptibility of consolidated procedural memory to interference is independent of its active task-based retrieval.

Reconsolidation theory posits that upon retrieval, consolidated memories are destabilized and need to be restabilized in order to persist. It has been suggested that experience with a competitive task immediately after memory retrieval may interrupt these restabilization processes leading to memory loss. Indeed, using a motor sequence learning paradigm, we have recently shown that, in humans, interference training immediately after active task-based retrieval of the consolidated motor sequence knowledge may negatively affect its performance levels. Assessing changes in tapping pattern before and after interference training, we also demonstrated that this performance deficit more likely indicates a genuine memory loss rather than an initial failure of memory retrieval. Here, applying a similar approach, we tested the necessity of the hypothetical retrieval-induced destabilization of motor memory to allow its impairment. The impact of memory retrieval on performance of a new motor sequence knowledge acquired during the interference training was also evaluated. Similar to the immediate post-retrieval interference, interference training alone without the preceding active task-based memory retrieval was also associated with impairment of the pre-established motor sequence memory. Performance levels of the sequence trained during the interference training, on the other hand, were impaired only if this training was given immediately after memory retrieval. Noteworthy, an 8-hour interval between memory retrieval and interference allowed to express intact performance levels for both sequences. The current results suggest that susceptibility of the consolidated motor memory to behavioral interference is independent of its active task-based retrieval. Differential effects of memory retrieval on performance levels of the new motor sequence encoded during the interference training further suggests that memory retrieval may influence the way new information is stored by facilitating its integration within the retrieved memory trace. Thus, impairment of the pre-established motor memory may reflect interference from a competing memory trace rather than involve interruption of reconsolidation.

Thalamo-Cortical White Matter Underlies Motor Memory Consolidation via Modulation of Sleep Spindles in Young and Older Adults.

Ample evidence suggests that consolidation of the memory trace associated with a newly acquired motor sequence is supported by thalamo-cortical spindle activity during subsequent sleep, as well as functional changes in a distributed cortico-striatal network. To date, however, no studies have investigated whether the structural white matter connections between these regions affect motor sequence memory consolidation in relation with sleep spindles. Here, we used diffusion weighted imaging (DWI) tractography to reconstruct the major fascicles of the cortico-striato-pallido-thalamo-cortical loop in both young and older participants who were trained on an explicit finger sequence learning task before and after a daytime nap. Thereby, this allowed us to examine whether post-learning sleep spindles measured using polysomnographic recordings interact with consolidation processes and this specific neural network. Our findings provide evidence corroborating the critical role of NREM2 thalamo-cortical sleep spindles in motor sequence memory consolidation, and show that the post-learning changes in these neurophysiological events relate specifically to white matter characteristics in thalamo-cortical fascicles. Moreover, we demonstrate that microstructure along this fascicle relates indirectly to offline gains in performance through an increase of spindle density over motor-related cortical areas. These results suggest that the integrity of thalamo-cortical projections, via their impact on sleep spindle generation, may represent one of the critical mechanisms modulating the expression of sleep-dependent offline gains following motor sequence learning in healthy adults.

Beyond spindles: interactions between sleep spindles and boundary frequencies during cued reactivation of motor memory representations.

There is now ample evidence that sleep spindles play a critical role in the consolidation of newly acquired motor sequences. Previous studies have also revealed that the interplay between different types of sleep oscillations (e.g. spindles, slow waves, sharp-wave ripples) promotes the consolidation process of declarative memories. Yet the functional contribution of this type of frequency-specific interactions to motor memory consolidation remains unknown. Thus, this study sought to investigate whether spindle oscillations are associated with low- or high-frequency activity at the regional (local) and interregional (connectivity) levels. Using an olfactory-targeted memory reactivation paradigm paired to a motor sequence learning task, we compared the effect of cuing (Cond) to no-cuing (NoCond) on frequency interactions during sleep spindles. Time-frequency decomposition analyses revealed that cuing induced significant differential and localized changes in delta (1-4 Hz) and theta (4-8 Hz) frequencies before, during, and after spindles, as well as changes in high-beta (20-30 Hz) during the spindle oscillation. Finally, coherence analyses yielded significant increases in connectivity during sleep spindles in both theta and sigma (11-17 Hz) bands in the cued group only. These results support the notion that the synchrony between spindle and associated low- or high-frequency rhythmic activity is an integral part of the memory reactivation process. Furthermore, they highlight the importance of not only measuring spindles' characteristics, but to investigate such oscillations in both time and frequency domains when assessing memory consolidation-related changes.

Integrated fMRI Preprocessing Framework Using Extended Kalman Filter for Estimation of Slice-Wise Motion.

Functional MRI acquisition is sensitive to subjects' motion that cannot be fully constrained. Therefore, signal corrections have to be applied a posteriori in order to mitigate the complex interactions between changing tissue localization and magnetic fields, gradients and readouts. To circumvent current preprocessing strategies limitations, we developed an integrated method that correct motion and spatial low-frequency intensity fluctuations at the level of each slice in order to better fit the acquisition processes. The registration of single or multiple simultaneously acquired slices is achieved online by an Iterated Extended Kalman Filter, favoring the robust estimation of continuous motion, while an intensity bias field is non-parametrically fitted. The proposed extraction of gray-matter BOLD activity from the acquisition space to an anatomical group template space, taking into account distortions, better preserves fine-scale patterns of activity. Importantly, the proposed unified framework generalizes to high-resolution multi-slice techniques. When tested on simulated and real data the latter shows a reduction of motion explained variance and signal variability when compared to the conventional preprocessing approach. These improvements provide more stable patterns of activity, facilitating investigation of cerebral information representation in healthy and/or clinical populations where motion is known to impact fine-scale data.

A safety mechanism for observational learning.

This empirical article presents the first evidence of a "safety mechanism" based on an observational-learning paradigm. It is accepted that during observational learning, a person can use different strategies to learn a motor skill, but it is unknown whether the learner is able to circumvent the encoding of an uncompleted observed skill. In this study, participants were tested in a dyadic protocol in which an observer watched a participant practicing two different motor sequences during a learning phase. During this phase, one of the two motor sequences was interrupted by a stop signal that precluded motor learning. The results of the subsequent retention test revealed that both groups learned the two motor sequences, but only the physical practice group showed worse performance for the interrupted sequence. The observers were consequently able to use a safety strategy to learn both sequences equally. Our findings are discussed in light of the implications of the action observation network for sequence learning and the cognitive mechanisms of error-based observation.

Transient synchronization of hippocampo-striato-thalamo-cortical networks during sleep spindle oscillations induces motor memory consolidation.

Sleep benefits motor memory consolidation. This mnemonic process is thought to be mediated by thalamo-cortical spindle activity during NREM-stage2 sleep episodes as well as changes in striatal and hippocampal activity. However, direct experimental evidence supporting the contribution of such sleep-dependent physiological mechanisms to motor memory consolidation in humans is lacking. In the present study, we combined EEG and fMRI sleep recordings following practice of a motor sequence learning (MSL) task to determine whether spindle oscillations support sleep-dependent motor memory consolidation by transiently synchronizing and coordinating specialized cortical and subcortical networks. To that end, we conducted EEG source reconstruction on spindle epochs in both cortical and subcortical regions using novel deep-source localization techniques. Coherence-based metrics were adopted to estimate functional connectivity between cortical and subcortical structures over specific frequency bands. Our findings not only confirm the critical and functional role of NREM-stage2 sleep spindles in motor skill consolidation, but provide first-time evidence that spindle oscillations [11-17 Hz] may be involved in sleep-dependent motor memory consolidation by locally reactivating and functionally binding specific task-relevant cortical and subcortical regions within networks including the hippocampus, putamen, thalamus and motor-related cortical regions.

Re-stepping into the same river: competition problem rather than a reconsolidation failure in an established motor skill.

Animal models suggest that consolidated memories return to their labile state when reactivated and need to be restabilized through reconsolidation processes to persist. Consistent with this notion, post-reactivation pharmacological protein synthesis blockage results in mnemonic failure in hippocampus-dependent memories. It has been proposed that, in humans, post-reactivation experience with a competitive task can also interfere with memory restabilization. However, several studies failed to induce performance deficit implementing this approach. Moreover, even upon effective post-reactivation interference, hindered performance may rapidly recover, raising the possibility of a retrieval rather than a storage deficit. Here, to address these issues in procedural memory domain, we used new learning to interfere with restabilization of motor memory acquired through training on a sequence of finger movements. Only immediate post-reactivation interference was associated with the loss of post-training delayed gains in performance, a hallmark of motor sequence memory consolidation. We also demonstrate that such performance deficit more likely indicates a genuine memory impairment rather than a retrieval failure. However, the reconsolidation view on a reactivation-induced plasticity is not supported. Instead, our results are in line with the integration model according to which new knowledge acquired during the interfering experience, is integrated through its consolidation creating memory competition.

Self-Control of Task Difficulty During Early Practice Promotes Motor Skill Learning.

This study was designed to determine whether the effect of self-control of task difficulty on motor learning is a function of the period of self-control administration. In a complex anticipation-coincidence task that required participants to intercept 3 targets with a virtual racquet, the task difficulty was either self-controlled or imposed to the participants in the two phases of the acquisition session. First, the results confirmed the beneficial effects of self-control over fully prescribed conditions. Second, the authors also demonstrated that a partial self-control of task difficulty better promotes learning than does a complete self-controlled procedure. Overall, the results revealed that these benefits are increased when this choice is allowed during early practice. The findings are discussed in terms of theoretical and applied perspectives.

Mental representations of magnitude and order: a dissociation by sensorimotor learning.

Numbers and spatially directed actions share cognitive representations. This assertion is derived from studies that have demonstrated that the processing of small- and large-magnitude numbers facilitates motor behaviors that are directed to the left and right, respectively. However, little is known about the role of sensorimotor learning for such number-action associations. In this study, we show that sensorimotor learning in a serial reaction-time task can modify the associations between number magnitudes and spatially directed movements. Experiments 1 and 3 revealed that this effect is present only for the learned sequence and does not transfer to a novel unpracticed sequence. Experiments 2 and 4 showed that the modification of stimulus-action associations by sensorimotor learning does not occur for other sets of ordered stimuli such as letters of the alphabet. These results strongly suggest that numbers and actions share a common magnitude representation that differs from the common order representation shared by letters and spatially directed actions. Only the magnitude representation, but not the order representation, can be modified episodically by sensorimotor learning.

Conscious awareness of action potentiates sensorimotor learning.

Many everyday skills are unconsciously learned through repetitions of the same behaviour by binding independent motor acts into unified sets of actions. However, our ability to be consciously aware of producing newly and highly trained motor skills raises the question of the role played by conscious awareness of action upon skill acquisition. In this study we strengthened conscious awareness of self-produced sequential finger movements by way of asking participants to judge their performance in terms of maximal fluency after each trial. Control conditions in which participants did not make any judgment or performance-unrelated judgments were also included. Findings indicate that conscious awareness of action, enhanced via subjective appraisal of motor efficiency, potentiates sensorimotor learning and skilful motor production in optimising the processing and sequencing of action units, as compared to the control groups. The current work lends support to the claim that the learning and skilful expression of sensorimotor behaviours might be grounded upon our ability to be consciously aware of our own motor capability and efficiency.

Modality-specific organization in the representation of sensorimotor sequences.

Sensorimotor representations of movement sequences are hierarchically organized. Here we test the effects of different stimulus modalities on such organizations. In the visual group, participants responded to a repeated sequence of visually presented stimuli by depressing spatially compatible keys on a response pad. In the auditory group, learners were required to respond to auditorily presented stimuli, which had no direct spatial correspondence with the response keys: the lowest pitch corresponded to the leftmost key and the highest pitch to the rightmost key. We demonstrate that hierarchically and auto-organized sensorimotor representations are developed through practice, which are specific both to individuals and stimulus modalities. These findings highlight the dynamic and sensory-specific modulation of chunk processing during sensorimotor learning - sensorimotor chunking - and provide evidence that modality-specific mechanisms underlie the hierarchical organization of sequence representations.

Retrieval practice in motor learning.

In this study we sought to determine whether testing promotes the generalization of motor skills during the process of encoding and/or consolidation. We used a dynamic arm movement task that required participants to reproduce a spatial-temporal pattern of elbow extensions and flexions with their dominant right arm. Generalization of motor learning was tested by the ability to transfer the original pattern (extrinsic transformation) or the mirrored pattern (intrinsic transformation) to the unpractised left arm. To investigate the testing effects during both encoding and consolidation processing, participants were administered an initial testing session during early practice before being evaluated on a post-practice testing session administered either 10min (Testing-Encoding group) or 24hr apart (Testing-Consolidation group), respectively. Control groups were required to perform a post-practice testing session administered after either a 10-min (Control-Encoding group) or 24-hr delay (Control-Consolidation group). The findings revealed that testing produced rapid, within-practice skill improvements, yielding better effector transfer at the 10-min testing for the Testing-Encoding group on both extrinsic and intrinsic transformation tests when compared with the Control-Encoding group. Furthermore, we found better performance for the Testing-Consolidation group at the 24-hr testing for extrinsic and intrinsic transformations of the movement pattern when compared with the Control-Consolidation group. However, our results did not indicate any significant testing advantage on the latent, between-session development of the motor skill representation (i.e., from the 10-min to the 24-hr testing). The testing benefits expressed at the 10-min testing were stabilised but did not extend during the period of consolidation. This indicates that testing contributes to the generalisation of motor skills during encoding but not consolidation.

Testing promotes effector transfer.

The retrieval of information from memory during testing has recently been shown to promote transfer in the verbal domain. Motor-related research, however, has ignored testing as a relevant method to enhance motor transfer. We thus investigated whether testing has the potential to induce generalised motor memories by favouring effector transfer. Participants were required to reproduce a spatial-temporal pattern of elbow extensions and flexions with their dominant right arm. We tested the ability of participants to transfer the original pattern (extrinsic transformation; i.e., goal-based configuration) or the mirrored pattern (intrinsic transformation; i.e., movement-based configuration) to the unpractised non-dominant left arm. To evaluate how testing affects motor transfer at 24-h testing, participants were either administered an initial testing session during early practice (early testing group) or shortly after the end of practice (late testing group; i.e., no alternation between practice and testing sessions). No initial testing session was completed for the control group. We found better effector transfer at 24-h testing for the early testing group for both extrinsic and intrinsic transformations of the movement pattern when compared with the control group, while no testing benefit was observed for the late testing group. This indicates that testing positively affects motor learning, yielding enhanced long-term transfer capabilities. We thus demonstrate the critical role of retrieval practice via testing during the process of motor memory encoding, and provide the conditions under which testing effectively contributes to the generalisation of motor memories.

Observational training in visual half-fields and the coding of movement sequences.

An experiment was conducted to determine if gating information to different hemispheres during observational training facilitates the development of a movement representation. Participants were randomly assigned to one of three observation groups that differed in terms of the type of visual half-field presentation during observation (right visual half-field (RVF), left visual half-field (LVF), or in central position (CE)), and a control group (CG). On Day 1, visual stimuli indicating the pattern of movement to be produced were projected on the respective hemisphere. The task participants observed was a 1300 ms spatial-temporal pattern of elbow flexions and extensions. On Day 2, participants physically performed the task in an inter-manual transfer paradigm with a retention test, and two contralateral transfer tests; a mirror transfer test which required the same pattern of muscle activation and limb joint angles and a non-mirror transfer test which reinstated the visual-spatial pattern of the sequence. The results demonstrated that participants of the CE, RVF and the LVF groups showed superior retention and transfer performance compared to participants of the CG. Participants of the CE- and LVF-groups demonstrated an advantage when the visual-spatial coordinates were reinstated compared to the motor coordinates, while participants of the RVF-group did not promote specific transfer patterns. These results will be discussed in the context of hemisphere specialization.