Somatosensory targeted memory reactivation enhances motor performance via hippocampal-mediated plasticity.

Increasing evidence suggests that reactivation of newly acquired memory traces during postlearning wakefulness plays an important role in memory consolidation. Here, we sought to boost the reactivation of a motor memory trace during postlearning wakefulness (quiet rest) immediately following learning using somatosensory targeted memory reactivation (TMR). Using functional magnetic resonance imaging, we examined the neural correlates of the reactivation process as well as the effect of the TMR intervention on brain responses elicited by task practice on 24 healthy young adults. Behavioral data of the post-TMR retest session showed a faster learning rate for the motor sequence that was reactivated as compared to the not-reactivated sequence. Brain imaging data revealed that motor, parietal, frontal, and cerebellar brain regions, which were recruited during initial motor learning, were specifically reactivated during the TMR episode and that hippocampo-frontal connectivity was modulated by the reactivation process. Importantly, the TMR-induced behavioral advantage was paralleled by dynamical changes in hippocampal activity and hippocampo-motor connectivity during task practice. Altogether, the present results suggest that somatosensory TMR during postlearning quiet rest can enhance motor performance via the modulation of hippocampo-cortical responses.

Differential effects of acute cardiovascular exercise on explicit and implicit motor memory: The moderating effects of fitness level.

A single bout of cardiovascular exercise (CE) performed after practice can facilitate the consolidation of motor memory. However, the effect is variable and may be modulated by different factors such as the motor task's or participant's characteristics and level of awareness during encoding (implicit vs explicit learning). This study examines the effects of acute CE on the consolidation of motor sequences learned explicitly and implicitly, exploring the potential moderating effect of fitness level and awareness. Fifty-six healthy adults (24.1 ± 3.3 years, 32 female) were recruited. After practicing with either the implicit or explicit variant of the Serial Reaction Time Task (SRTT), participants either performed a bout of 16 min of vigorous CE or rested for the same amount of time. Consolidation was quantified as the change in SRTT performance from the end of practice to a 24 h retention test. Fitness level (V̇O2peak) was determined through a graded exercise test. Awareness (implicit vs explicit learning) was operationalized using a free recall test conducted immediately after retention. Our primary analysis indicated that CE had no statistically significant effects on consolidation, regardless of the SRTT's variant utilized during practice. However, an exploratory analysis, classifying participants based on the level of awareness gained during motor practice, showed that CE negatively influenced consolidation in unfit participants who explicitly acquired the motor sequence. Our findings indicate that fitness level and awareness in sequence acquisition can modulate the interaction between CE and motor memory consolidation. These factors should be taken into account when assessing the effects of CE on motor memory.

Gross motor adaptation benefits from sleep after training.

Sleep has been shown to facilitate the consolidation of newly acquired motor memories. However, the role of sleep in gross motor learning, especially in motor adaptation, is less clear. Thus, we investigated the effects of nocturnal sleep on the performance of a gross motor adaptation task, i.e. riding an inverse steering bicycle. Twenty-six male participants (M = 24.19, SD = 3.70 years) were randomly assigned to a PM-AM-PM (n = 13) or an AM-PM-AM (n = 13) group, i.e. they trained in the evening/morning and were re-tested the next morning/evening and the following evening/morning (PM-AM-PM/AM-PM-AM group) so that every participant spent one sleep as well as one wake interval between the three test sessions. Inverse cycling performance was assessed by speed (riding time) and accuracy (standard deviation of steering angle) measures. Behavioural results showed that in the PM-AM-PM group a night of sleep right after training stabilized performance (accuracy and speed) and was further improved over the subsequent wake interval. In the AM-PM-AM group, a significant performance deterioration after the initial wake interval was followed by the restoration of subjects' performance levels from right after training when a full night of sleep was granted. Regarding sleep, right hemispheric fast N2 sleep spindle activity was related to better stabilization of inverse cycling skills, thus possibly reflecting the ongoing process of updating the participants' mental model from "how to ride a bicycle" to "how to ride an inverse steering bicycle". Our results demonstrate that sleep facilitates the consolidation of gross motor adaptation, thus adding further insights to the role of sleep for tasks with real-life relevance.

Age-related changes in brain deactivation but not in activation after motor learning.

It is poorly understood how healthy aging affects neural mechanisms underlying motor learning. We used blood-oxygen-level dependent (BOLD) contrasts to examine age-related changes in brain activation after acquisition and consolidation (24 h) of a visuomotor tracking skill. Additionally, structural magnetic resonance imaging and diffusion tensor imaging were used to examine age-related structural changes in the brain. Older adults had reduced gray matter volume (628 ±â€¯57 ml) and mean white matter anisotropy (0.18 ±â€¯0.03) compared with young adults (741 ±â€¯59 ml and 0.22 ±â€¯0.02, respectively). Although motor performance was 53% lower in older (n = 15, mean age 63.1 years) compared with young adults (n = 15, mean age 25.5 years), motor practice improved motor performance similarly in both age groups. While executing the task, older adults showed in general greater brain activation compared with young adults. BOLD activation decreased in parietal and occipital areas after skill acquisition but activation increased in these areas after consolidation in both age groups, indicating more efficient visuospatial processing immediately after skill acquisition. Changes in deactivation in specific areas were age-dependent after consolidating the motor skill into motor memory. Young adults showed greater deactivations from post-test to retention in parietal, occipital and temporal cortices, whereas older adults showed smaller deactivation in the frontal cortex. Since learning rate was similar between age groups, age-related changes in activation patterns may be interpreted as a compensatory mechanism for age-related structural decline.

The impact of sleep on complex gross-motor adaptation in adolescents.

Sleep has been shown to facilitate the consolidation of newly acquired motor memories in adults. However, the role of sleep in motor memory consolidation is less clear in children and adolescents, especially concerning real-life gross-motor skills. Therefore, we investigated the effects of sleep and wakefulness on a complex gross-motor adaptation task by using a bicycle with an inverse steering device. A total of 29 healthy adolescents aged between 11 and 14 years (five female) were either trained to ride an inverse steering bicycle (learning condition) or a stationary bicycle (control condition). Training took place in the morning (wake, n = 14) or in the evening (sleep, n = 15) followed by a 9-hr retention interval and a subsequent re-test session. Slalom cycling performance was assessed by speed (riding time) and accuracy (standard deviation of steering angle) measures. Behavioural results showed no evidence for sleep-dependent memory consolidation. However, overnight gains in accuracy were associated with an increase in left hemispheric N2 slow sleep spindle activity from control to learning night. Furthermore, decreases in REM and tonic REM duration were related to higher overnight improvements in accuracy. Regarding speed, an increase in REM and tonic REM duration was favourable for higher overnight gains in riding time. Thus, although not yet detectable on a behavioural level, sleep seemed to play a role in the acquisition of gross-motor skills. A promising direction for future research is to focus on the possibility of delayed performance gains in adolescent populations.

Changing Sleep Architecture through Motor Learning: Influences of a Trampoline Session on REM Sleep Parameters.

Previous research has shown that learning procedural tasks enhances REM sleep the following night. Here, we investigate whether complex motor learning affects sleep architecture. An experiment in which twenty-two subjects either learned a motor task (trampolining) or engaged in a control task (ergometer) was carried out in a balanced within-group design. After an initial laboratory adaptation night, two experimental nights were consecutive. The results indicate that learning a motor task had an effect on REM sleep parameters and, therefore, support the hypothesis that learning a procedural skill is related to an increase in REM sleep parameters. However, the statistical effect on REM sleep is smaller than found in previous studies. One might speculate that the motor learning was not intense enough compared to other studies. For sports practice, the results suggest that REM sleep, which is particularly rich in the morning, plays an important role in motor memory consolidation. Thus, this phase should not be interrupted after complex motor skill learning sessions. In future studies, other motor tasks should be applied.

Motor learning is independent of effects of subthalamic deep brain stimulation on motor execution.

Motor learning is defined as an improvement in performance through practice. The ability to learn new motor skills may be particularly challenged in patients with Parkinson's disease, in whom motor execution is impaired by the disease-defining motor symptoms such as bradykinesia. Subthalamic deep brain stimulation is an effective treatment in advanced Parkinson's disease, and its beneficial effects on Parkinsonian motor symptoms and motor execution have been widely demonstrated. Much less is known about whether deep brain stimulation directly interacts with motor learning independent of modulation of motor execution. We investigated motor sequence learning in 19 patients with Parkinson's disease treated with subthalamic deep brain stimulation and 19 age-matched controls. In a cross-over design, patients performed an initial motor sequence training session with active and inactive stimulation, respectively (experiments separated by ≥14 days). Performance was retested after 5 min and after a 6 h consolidation interval with active stimulation. Healthy controls performed a similar experiment once. We further investigated neural correlates underlying stimulation-related effects on motor learning by exploring the association of normative subthalamic deep brain stimulation functional connectivity profiles with stimulation-related differences in performance gains during training. Pausing deep brain stimulation during initial training resulted in the inhibition of performance gains that could have been indicative of learning at the behavioural level. Task performance improved significantly during training with active deep brain stimulation, but did not reach the level of learning dynamics of healthy controls. Importantly, task performance after the 6 h consolidation interval was similar across patients with Parkinson's disease independent of whether the initial training session had been performed with active or inactive deep brain stimulation. This indicates that early learning and subsequent consolidation were relatively intact despite severe impairments of motor execution during training with inactive deep brain stimulation. Normative connectivity analyses revealed plausible and significant connectivity of volumes of tissue activated by deep brain stimulation with several cortical areas. However, no specific connectivity profiles were associated with stimulation-dependent differences in learning during initial training. Our results show that motor learning in Parkinson's disease is independent of modulation of motor execution by subthalamic deep brain stimulation. This indicates an important role of the subthalamic nucleus in regulating general motor execution, whereas its role in motor learning appears negligible. Because longer-term outcomes were independent of performance gains during initial training, patients with Parkinson's disease may not need to wait for an optimal motor state to practice new motor skills.

Connectivity in Large-Scale Resting-State Brain Networks Is Related to Motor Learning: A High-Density EEG Study.

Previous research has shown that resting-state functional connectivity (rsFC) between different brain regions (seeds) is related to motor learning and motor memory consolidation. Using high-density electroencephalography (hdEEG), we addressed this question from a brain network perspective. Specifically, we examined frequency-dependent functional connectivity in resting-state networks from twenty-nine young healthy participants before and after they were trained on a motor sequence learning task. Consolidation was assessed with an overnight retest on the motor task. Our results showed training-related decreases in gamma-band connectivity within the motor network, and between the motor and functionally distinct resting-state networks including the attentional network. Brain-behavior correlation analyses revealed that baseline beta, delta, and theta rsFC were related to subsequent motor learning and memory consolidation such that lower connectivity within the motor network and between the motor and several distinct resting-state networks was correlated with better learning and overnight consolidation. Lastly, training-related increases in beta-band connectivity between the motor and the visual networks were related to greater consolidation. Altogether, our results indicate that connectivity in large-scale resting-state brain networks is related to-and modulated by-motor learning and memory consolidation processes. These finding corroborate previous seed-based connectivity research and provide evidence that frequency-dependent functional connectivity in resting-state networks is critically linked to motor learning and memory consolidation.

Transcranial Alternating Current Stimulation of the Primary Motor Cortex after Skill Acquisition Improves Motor Memory Retention in Humans: A Double-Blinded Sham-Controlled Study.

Consolidation leading to retention of motor memory following motor practice involves activity-dependent plastic processes in the corticospinal system. To investigate whether beta-band transcranial alternating current stimulation (tACS) applied immediately following skill acquisition can enhance ongoing consolidation processes and thereby motor skill retention 20 adults participated in a randomized, double-blinded, sham-controlled study. Participants received tACS at peak beta-band corticomuscular coherence (CMC) frequency or sham tACS for 10 min following practice of a visuomotor ankle dorsiflexion task. Performance was measured as the average percentage time on target. Electroencephalograhy (EMG) was measured at Cz and EMG from the right tibialis anterior muscle. CMC and intramuscular coherence (IMC) were estimated during 2-min tonic dorsiflexion. Motor skill retention was tested 1 and 7 days after motor practice. From the end of motor practice to the retention tests, motor performance improved more in the tACS group compared with the sham tACS group after 1 (P = 0.05) and 7 days (P < 0.001). At both retention tests, beta-band IMC increased in the tACS group compared with post-tACS. Beta-band CMC increased in the tACS group at retention day 1 compared with post-tACS. Changes in CMC but not IMC were correlated with performance 1 and 7 days following practice. This study shows that tACS applied at beta-band CMC frequency improves consolidation following visuomotor practice and increases beta-band CMC and IMC. We propose that oscillatory beta activity in the corticospinal system may facilitate consolidation of the motor skill.

Sleep-dependent motor memory consolidation in healthy adults: A meta-analysis.

It is widely accepted that sleep better facilitates the consolidation of motor memories than does a corresponding wake interval (King et al., 2017). However, no in-depth analysis of the various motor tasks and their relative sleep gain has been conducted so far. Therefore, the present meta-analysis considered 48 studies with a total of 53 sleep (n = 829) and 53 wake (n = 825) groups. An overall comparison between all sleep and wake groups resulted in a small effect for the relative sleep gain in motor memory consolidation (g = 0.43). While no subgroup differences were identified for differing designs, a small effect for the finger tapping task (g = 0.47) and a medium effect for the mirror tracing task (g = 0.62) were found. In summary, the meta-analysis substantiates that sleep generally benefits the consolidation of motor memories. However, to further our understanding of the mechanisms underlying this effect, examining certain task dimensions and their relative sleep gain would be a promising direction for future research.

Enhancing Children's Motor Memory Retention Through Acute Intense Exercise: Effects of Different Exercise Durations.

Physical exercise has been proposed as a viable means to stimulate motor learning. Exercise characteristics, including intensity and duration, may play a role in modulating the exercise effect on motor learning. While some evidence exists regarding the benefits of intense and relatively long exercise, little is known about the effect of short exercise bouts on motor learning, especially in children. This study aimed to assess the effect of long versus short intense exercise bouts on the adaptation and consolidation of a rotational visuomotor adaptation task. The participants were 71 healthy children from two sites divided into three groups: long exercise bout (LONG), short exercise bout (SHORT), and no exercise (CON). Children performed a rotated (clockwise 60° rotation) motor task on four different occasions: an adaptation set and 1 h, 24 h, and 7 days delayed retention sets. Exercise bouts were performed prior to the adaptation set. Results showed a group effect during motor adaptation [F(2,68) = 3.160; p = 0.049; η p 2 = 0.087], but no statistical differences were found between groups. Regarding retention tests, both exercise groups (LONG and SHORT) showed superior retention compared to CON group [F(2,68) = 7.102; p = 0.002; η p 2 = 0.175]. No differences were found between exercise groups, indicating similar benefits for the two exercise interventions. Overall, whether the exercise duration was long or short, exercise improved motor memory retention as an estimate of memory consolidation process. The use of short exercise bouts may be suitable to improve children's motor memory consolidation in environments where time constraints exist.

Contextual Interference Effect Is Independent of Retroactive Inhibition but Variable Practice Is Not Always Beneficial.

Positive effects of variable practice conditions on subsequent motor memory consolidation and generalization are widely accepted and described as the contextual interference effect (CIE). However, the general benefits of CIE are low and these benefits might even depend on decreased retest performances in the blocked-practicing control group, caused by retroactive inhibition. The aim of this study was to investigate if CIE represents a true learning phenomenon or possibly reflects confounding effects of retroactive inhibition. We tested 48 healthy human participants adapting their reaching movements to three different force field magnitudes. Subjects practiced the force fields in either a Blocked (B), Random (R), or Constant (C) schedule. In addition, subjects of the Blocked group performed either a retest schedule that did (Blocked-Matched; BM) or did not (Blocked-Unmatched; BU) control for retroactive inhibition. Results showed that retroactive inhibition did not affect the results of the BU group much and that the Random group showed a better consolidation performance compared to both Blocked groups. However, compared to the Constant group, the Random group showed only slight benefits in its memory consolidation of the mean performance across all force field magnitudes and no benefits in absolute performance values. This indicates that CIE reflects a true motor learning phenomenon, which is independent of retroactive inhibition. However, random practice is not always beneficial over constant practice.

The effects of aging on cortico-spinal excitability and motor memory consolidation.

We investigated whether cortico-spinal excitability (CSE), a marker of synaptic plasticity, is associated with age-related differences in the consolidation of motor memory. Young and older participants practiced a visuomotor tracking task. Skill retention was assessed 8 and 24 hours after motor practice. Transcranial magnetic stimulation applied over the primary motor cortex at rest and during an isometric muscle contraction was used to assess absolute and normalized to baseline CSE at different points after practice. When skill performance was normalized to baseline level, both groups showed similar gains in acquisition, but the young group showed better retention 24 hours after practice. The young group also showed greater absolute CSE assessed during the isometric muscle contraction. Although young participants with greater absolute CSE showed better skill retention, it was the capacity to increase CSE after motor practice, and not absolute CSE, what was associated with skill retention in older participants. Older adults who have the capacity to increase CSE during motor memory consolidation show a better capacity to retain motor skills.

Induced sensorimotor cortex plasticity remediates chronic treatment-resistant visual neglect.

Right brain injury causes visual neglect - lost awareness of left space. During prism adaptation therapy, patients adapt to a rightward optical shift by recalibrating right arm movements leftward. This can improve left neglect, but the benefit of a single session is transient (~1 day). Here we show that tonic disinhibition of left motor cortex during prism adaptation enhances consolidation, stabilizing both sensorimotor and cognitive prism after-effects. In three longitudinal patient case series, just 20 min of combined stimulation/adaptation caused persistent cognitive after-effects (neglect improvement) that lasted throughout follow-up (18-46 days). Moreover, adaptation without stimulation was ineffective. Thus stimulation reversed treatment resistance in chronic visual neglect. These findings challenge consensus that because the left hemisphere in neglect is pathologically over-excited it ought to be suppressed. Excitation of left sensorimotor circuits, during an adaptive cognitive state, can unmask latent plastic potential that durably improves resistant visual attention deficits after brain injury.

Motor Skill Acquisition and Retention after Somatosensory Electrical Stimulation in Healthy Humans.

Somatosensory electrical stimulation (SES) can increase motor performance, presumably through a modulation of neuronal excitability. Because the effects of SES can outlast the period of stimulation, we examined the possibility that SES can also enhance the retention of motor performance, motor memory consolidation, after 24 h (Day 2) and 7 days (Day 7), that such effects would be scaled by SES duration, and that such effects were mediated by changes in aspects of corticospinal excitability, short-interval intracortical inhibition (SICI), and intracortical facilitation (ICF). Healthy young adults (n = 40) received either 20 (SES-20), 40 (SES-40), or 60 min (SES-60) of real SES, or sham SES (SES-0). The results showed SES-20 increased visuomotor performance on Day 2 (15%) and Day 7 (17%) and SES-60 increased visuomotor performance on Day 7 (11%; all p < 0.05) compared with SES-0. Specific responses to transcranial magnetic stimulation (TMS) increased immediately after SES (p < 0.05) but not on Days 2 and 7. In addition, changes in behavioral and neurophysiological parameters did not correlate, suggesting that paths and structures other than the ones TMS can assay must be (also) involved in the increases in visuomotor performance after SES. As examined in the present study, low-intensity peripheral electrical nerve stimulation did not have acute effects on healthy adults' visuomotor performance but SES had delayed effects in the form of enhanced motor memory consolidation that were not scaled by the duration of SES.

Better than sleep: theta neurofeedback training accelerates memory consolidation.

Consistent empirical results showed that both night and day sleep enhanced memory consolidation. In this study we explore processes of consolidation of memory during awake hours. Since theta oscillations have been shown to play a central role in exchange of information, we hypothesized that elevated theta during awake hours will enhance memory consolidation. We used a neurofeedback protocol, to enhance the relative power of theta or beta oscillations. Participants trained on a tapping task, were divided into three groups: neurofeedback theta; neurofeedback beta; control. We found a significant improvement in performance in the theta group, relative to the beta and control groups, immediately after neurofeedback. Performance was further improved after night sleep in all groups, with a significant advantage favoring the theta group. Theta power during training was correlated with the level of improvement, indicating a clear relationship between memory consolidation, and theta neurofeedback.