Memory consolidation of sequence learning and dynamic adaptation during wakefulness.

Motor learning involves acquiring new movement sequences and adapting motor commands to novel conditions. Labile motor memories, acquired through sequence learning and dynamic adaptation, undergo a consolidation process during wakefulness after initial training. This process stabilizes the new memories, leading to long-term memory formation. However, it remains unclear if the consolidation processes underlying sequence learning and dynamic adaptation are independent and if distinct neural regions underpin memory consolidation associated with sequence learning and dynamic adaptation. Here, we first demonstrated that the initially labile memories formed during sequence learning and dynamic adaptation were stabilized against interference through time-dependent consolidation processes occurring during wakefulness. Furthermore, we found that sequence learning memory was not disrupted when immediately followed by dynamic adaptation and vice versa, indicating distinct mechanisms for sequence learning and dynamic adaptation consolidation. Finally, by applying patterned transcranial magnetic stimulation to selectively disrupt the activity in the primary motor (M1) or sensory (S1) cortices immediately after sequence learning or dynamic adaptation, we found that sequence learning consolidation depended on M1 but not S1, while dynamic adaptation consolidation relied on S1 but not M1. For the first time in a single experimental framework, this study revealed distinct neural underpinnings for sequence learning and dynamic adaptation consolidation during wakefulness, with significant implications for motor skill enhancement and rehabilitation.

Off-line learning in a rhythmic bimanual task: early feedback dependency is reduced over wakefulness.

Research has supported two distinct forms of motor skill consolidation that can occur between practice sessions: (1) off-line learning, and (2) memory stabilization. Off-line learning describes performance improvement between practice sessions that is above the gain observed at the end of practice, while memory stabilization describes a gain in performance that is maintained between practice sessions. This study used a Lissajous plot to provide concurrent feedback to train participants to produce a 90° relative phase between the index fingers (flexion/extension motion). Significant improvements in performance emerged after ten trials (5 min) of practice. At the end of training, participants were divided into two delay interval groups before retesting, 2-h and 6-h. The retesting session started with participants performing an interference task (10 trials, 5 min) that required training on a 45° relative phase between the fingers with concurrent feedback from the Lissajous plot. When training with the interference task was completed participants were retested with the 90° relative phase without the Lissajous plot feedback. In the retest of the 90° pattern, a performance loss was found in the 2-h delay group, whereas the 6-h delay group maintained the end of practice performance level. Maintenance of the same level of performance without the Lissajous plot represents memory stabilization of the initially trained 90° pattern. The findings are discussed within the context of current positions regarding procedural consolidation and the coordination dynamics framework wherein action and perception are linked through the informational nature of relative phase.

Motor and spatial representations of action: corticospinal excitability in M1 after training with a bimanual skill.

The purpose of the study was twofold: (1) determine if different time delays (30 min or 6 h) between training and a post-training test with a rhythmic bimanual pattern (90° relative phase) would be associated with different levels of consolidation for the motor and spatial representations of the pattern; and (2) determine if training with the rhythmic bimanual pattern would lead to enhanced corticospinal excitability in M1 linked to changes in motor and spatial performance measures. Coordination accuracy and stability of the 90° pattern improved over practice. Coordination accuracy and stability were the same after a 30-min or 6-h delay between training and the post-training test, indicating equivalent levels of consolidation in the motor representation. The 6-h delay interval resulted in shorter visual recognition times compared to the 30-min delay and was centered on the trained 90° pattern. These findings indicate the consolidation of the spatial representation was more time sensitive compared to the motor representation in the current task. Motor evoked potentials (MEPs) from the first dorsal interosseous muscle (FDI) generated by single-pulse transcranial magnetic stimulation (TMS) were measured at baseline (before training) and at 6-min and 21-min intervals post-training with the 90° pattern. Increased corticospinal excitability in M1 was evidenced by larger MEPs of the FDI muscle at the 6-min interval. This increased excitability after training is a novel finding after training with a difficult and initially unstable rhythmic bimanual pattern. No significant correlations were found between the MEP data and behavioral data; thus, the increased excitability in M1 may have been linked to the difficulty in performing the pattern, consolidation processes, or both.

Application of anodal tDCS at primary motor cortex immediately after practice of a motor sequence does not improve offline gain.

Tecchio et al. (J Neurophysiology 104: 1134-1140, 2010) reported that the application of anodal tDCS at primary motor cortex (M1) immediately after practice of a procedural motor skill enhanced consolidation, which in turn improved offline gain. Tecchio et al. noted, however, that this study did not account for known after-effects associated with this form of non-invasive stimulation. The present study was designed to explicitly reevaluate Tecchio et al.'s claim. As in the original study, individuals experienced either anodal or sham stimulation at M1 after practice of a serial reaction time task (SRTT) followed by test trials 15-min later. Two additional novel conditions experienced the test trials after 120-min rather than 15-min thus allowing potential stimulation after-effects to dissipate. The expectation was that if anodal stimulation influences post-practice consolidation leading to offline gain, this effect would be present not only at 15-min but also after 120-min. In agreement with the working hypothesis, findings revealed offline gain at both 15-min and the longer 2-h time period. Unexpectedly, we found no interaction between real and sham conditions. The lack of difference between Real and Sham effects weakens confidence in the potential of post-practice tDCS for consolidation enhancement, while it is more consistent with other claims that decoupling practice and anodal tDCS stimulation in time can reduce the effectiveness of exogenous stimulation for procedural skill gain.

Mirror-hand selection is influenced by training perspective and model skill level in a motor-learning task.

This study examined mirror and non-mirror arm selection processes in an observational learning context. Observer groups watched either a novice (instruction or discovery) or skilled model performing a bimanual task with the right arm leading the left arm. The models were viewed from a third-person perspective. Observers of the skilled model more often selected a mirror-image (left-hand) hand-lead in post-observations tests, while observers of the novice models more often selected a non-mirror image (right hand) hand-lead in post-observation tests. This is a novel finding regarding arm selection processes in a learning context, yet it is consistent with imaging data that has revealed specific neural areas linked to the selection of mirror and non-mirror imitation processes for first- and third-person viewing perspectives. The skilled model also supported more accurate and stable performance of the bimanual task in observers compared to the instruction and novice models. It is concluded that a skilled model supports attention focus being directed at pattern analysis, while novice models support attention focus being allocated to strategy identification first, followed by pattern analysis.

Bimanual coordination patterns are stabilized under monitoring-pressure.

The influence of monitoring-pressure on the performance of anti-phase and in-phase bimanual coordination was examined. The two bimanual patterns were produced under no-monitoring and monitoring-pressure conditions at self-paced frequencies. Anti-phase coordination was always less stable than in-phase coordination, with or without monitoring. When performed under monitoring-pressure, the coordination patterns were performed with less variability in relative phase for both patterns across a range of self-paced movement frequencies compared to performance without monitoring. Thus, while monitoring-pressure did induce a behavioral change, it consisted of performance stabilization rather than degradation, a finding inconsistent with explicit-monitoring theory. However, the findings are consistent with the theory of coordination dynamics and studies that have revealed increased stability for the system's intrinsic dynamics as a result of attentional focus and intentional control.

Observation and physical practice: different practice contexts lead to similar outcomes for the acquisition of kinematic information.

This study differentiated the contributions of physical and observational practice to the learning of a single-limb multi-joint coordination pattern. Three groups (physical-practice, observation-practice, observation-physical) practiced for 2 days and were given two performance tests 24 h after the second practice session. The performance tests revealed that physical and observational practice contributed similarly to identifying and using kinematic information related to the relative motion direction between joints (lead/lag relationship) and to the to-be-learned relative phase pattern (ϕ = 90°). Physical practice resulted in more stable coordination during performance tests and in the ability to produce different joint amplitudes with less variability. A serendipitous finding was that maximum elbow flexion (point of movement reversal) emerged as a kinematic event around which elbow and wrist coordination were organized. Movement reversals often serve to anchor the movement dynamics, and this anchoring effect was evident following both physical and observational practice, yet physical practice resulted in an advantage with regard to this anchor point on several kinematic measures. The results are discussed within the context of contemporary behavioral theories (coordination dynamics, visual perception perspective) of observational learning.

The Coordination Dynamics of Observational Learning: Relative Motion Direction and Relative Phase as Informational Content Linking Action-Perception to Action-Production.

The primary goal of this chapter is to merge together the visual perception perspective of observational learning and the coordination dynamics theory of pattern formation in perception and action. Emphasis is placed on identifying movement features that constrain and inform action-perception and action-production processes. Two sources of visual information are examined, relative motion direction and relative phase. The visual perception perspective states that the topological features of relative motion between limbs and joints remains invariant across an actor's motion and therefore are available for pickup by an observer. Relative phase has been put forth as an informational variable that links perception to action within the coordination dynamics theory. A primary assumption of the coordination dynamics approach is that environmental information is meaningful only in terms of the behavior it modifies. Across a series of single limb tasks and bimanual tasks it is shown that the relative motion and relative phase between limbs and joints is picked up through visual processes and supports observational learning of motor skills. Moreover, internal estimations of motor skill proficiency and competency are linked to the informational content found in relative motion and relative phase. Thus, the chapter links action to perception and vice versa and also links cognitive evaluations to the coordination dynamics that support action-perception and action-production processes.

The perception-action dynamics of action competency are altered by both physical and observational training.

Action competency is defined as the ability of an individual to self-evaluate their own performance capabilities. The current experiment demonstrated that physical and observational training with a motor skill alters action competency ratings in a similar manner. Using a pre-test and post-test protocol, the results revealed that action competency is constrained prior to training by the intrinsic dynamics of relative phase (ϕ), with in-phase (ϕ = 0°) and anti-phase (ϕ = 180°) patterns receiving higher competency ratings than other relative phase patterns. After 2 days of training, action competency ratings for two trained relative phase patterns, +60° and +120°, increased following physical practice or observational practice. A transfer test revealed that both physical performance ability and action competency ability transferred to the symmetry partners (-60° and -120°) of the two trained relative phase patterns following physical or observational training. The findings also revealed that relative motion direction acts as categorical information that helps to organize action production and facilitate action competency. The results are interpreted based on the coordination dynamics theory of perception-action coupling, and extend this theory by showing that visual perception, action production, and action competency are all constrained in a consistent manner by the dynamics of the order parameter relative phase. As a whole, the findings revealed that relative motion, relative phase, and possibly relative amplitude information are all distinct sources of information that contribute to the emergence of a kinematic understanding of action in the nervous system.

Spontaneity competes with intention to influence the coordination dynamics of interpersonal performance tendencies.

Research has shown that spontaneous visual coupling supports frequency entrainment, phase attraction, and intermittent interpersonal coordination when co-actors are switched from a no-vision (NV) to vision (V) context. In two experiments, co-actors started in a NV context while producing the same or different amplitude movements. The same amplitude resulted in similar self-paced frequencies, while different amplitudes resulted in disparate frequencies. In experiment 1, co-actors were instructed to maintain amplitude while receiving no instructions to coordinate their actions. Frequency and phase entrainment was limited in the V context even when co-actors started the NV context with the same amplitude. In experiment 2, co-actors were instructed to maintain amplitude and intentionally coordinate together, but not at a specific pattern. Significant frequency modulations occurred to maintain amplitude as the co-actors sought to coordinate their actions. With the open-ended instructions, co-actors produced in-phase and anti-phase coordination along with intermittent performance exhibited by shifts between a variety of stable relative phase patterns. The proposed hypotheses and findings are discussed within the context of a shared manifold representation for joint action contexts, with the coordination dynamics expressed by the HKB model of relative phase serving to conceptualization the representations in the shared manifold.

Timing of transcranial direct current stimulation at M1 does not affect motor sequence learning.

Administering anodal transcranial direct current stimulation (tDCS) at the primary motor cortex (M1) at various temporal loci relative to motor training is reported to affect subsequent performance gains. Stimulation administered in conjunction with motor training appears to offer the most robust benefit that emerges during offline epochs. This conclusion is made, however, based on between-experiment comparisons that involved varied methodologies. The present experiment addressed this shortcoming by administering the same 15-minute dose of anodal tDCS at M1 before, during, or after practice of a serial reaction time task (SRTT). It was anticipated that exogenous stimulation during practice with a novel SRTT would facilitate offline gains. Ninety participants were randomly assigned to one of four groups: tDCS before practice, tDCS during practice, tDCS after practice, or no tDCS. Each participant was exposed to 15 min of 2 mA of tDCS and motor training of an eight-element SRTT. The anode was placed at the right M1 with the cathode at the left M1, and the left hand was used to execute the SRTT. Test blocks were administered 1 and 24 h after practice concluded. The results revealed significant offline gain for all conditions at the 1-hour and 24-hour test blocks. Importantly, exposure to anodal tDCS at M1 at any point before, during, or after motor training failed to change the trajectory of skill development as compared to the no-stimulation control condition. These data add to the growing body of evidence questioning the efficacy of a single bout of exogenous stimulation as an adjunct to motor training for fostering skill learning.

Flexibility in the control of rapid aiming actions.

Across three different task conditions, the adaptability of reciprocal aiming movements was investigated. Task difficulty was manipulated by changing ID, with 9 IDs between 2.5 and 6.5 tested. Reciprocal aiming movements were performed with ID scaled (predictable) in a trial in a decreasing (high 6.5-low 2.5) or increasing manner (low 2.5-high 6.5) or with ID constant in a trial and changed randomly across trials. Movement time scaled linearly with ID in both the scaling ID and control ID presentations. A critical ID boundary (IDC) was identified, and the adaptation of aiming movements was a function of this critical boundary. For IDs < IDC, the results are interpreted as representing a predominance for pre-planned control based on a dwell time measure and a symmetry ratio measure (time spent accelerating-decelerating the limb). Within this ID range, movement harmonicity was changed to a greater extent when ID was scaled in a predictable direction as compared to being presented in a random manner. For IDs > IDC, the findings suggest a predominance for feedback control based on the dwell time and symmetry ratio measure. Within this ID range, the absolute time spent decelerating was increased, possibly to insure accuracy and minimize MT, with the predictable changes associated with an increase in ID needing less time devoted to feedback processing compared to the other ID presentations. The results are consistent with the theoretical position that aiming motions may be controlled by a limit cycle mechanism with ID < IDC, while aiming motions may be controlled by a fixed-point mechanism with ID > IDC. The results suggest that the ability of the motor system to adapt to both scaled and random changes in ID revolves around a modulation of pre-planned and feedback-based control processes.

Effects of transcranial direct current stimulation over human motor cortex on cognitive-motor and sensory-motor functions.

The primary motor cortex (M1) is broadly acknowledged for its crucial role in executing voluntary movements. Yet, its contributions to cognitive and sensory functions remain largely unexplored. Transcranial direct current stimulation (tDCS) is a noninvasive neurostimulation method that can modify brain activity, thereby enabling the establishment of a causal link between M1 activity and behavior. This study aimed to investigate the online effects of tDCS over M1 on cognitive-motor and sensory-motor functions. Sixty-four healthy participants underwent either anodal or sham tDCS while concurrently performing a set of standardized robotic tasks. These tasks provided sensitive and objective assessments of brain functions, including action selection, inhibitory control, cognitive control of visuomotor skills, proprioceptive sense, and bimanual coordination. Our results revealed that anodal tDCS applied to M1 enhances decision-making capacity in selecting appropriate motor actions and avoiding distractors compared to sham stimulation, suggesting improved action selection and inhibitory control capabilities. Furthermore, anodal tDCS reduces the movement time required to accomplish bimanual movements, suggesting enhanced bimanual performance. However, we found no impact of anodal tDCS on cognitive control of visuomotor skills and proprioceptive sense. This study suggests that augmenting M1 activity via anodal tDCS influences cognitive-motor and sensory-motor functions in a task-dependent manner.

Overcoming the guidance effect in motor skill learning: feedback all the time can be beneficial.

Extensive research has shown that augmented feedback presented too often can create a dependency on the feedback and hinder long-term memory formation of a motor skill. This dependency has been labeled the guidance effect, and one way to overcome the guidance effect is to reduce how often augmented feedback is presented during training. In two experiments, participants were presented with visual augmented feedback during every trial in a 5-min training interval. Participants were provided visual augmented feedback in the form of a Lissajous template of a 1:2 multi-frequency pattern and a cursor representing the coordination between the limbs. Some participants were trained with the cursor superimposed (behind group) on the Lissajous template, and others were trained with the cursor presented in a separate window (side group) from the Lissajous template. In experiment 1, motion of the end-effectors was constrained to the medial-lateral direction in the horizontal plane. In experiment 2, end-effector motion was possible in both the medial-lateral and anterior-posterior directions in the horizontal plane. The location of the cursor did not influence performance during the 5-min training interval in either experiment. After a 15-min break, a retention test performed without the visual feedback provided by the cursor revealed that the behind groups' performance was guided by the visual feedback in both experiments, whereas the side groups were able to perform without visual feedback. In experiment two, the side group's performance without feedback was influenced when anterior-posterior motion was not constrained; however, the extent of the guidance effect was significantly less compared to the behind trained group in both experiments. The results show that the emergence of guided motor performance depends on the format of the display that provides visually based augmented feedback, and not just on how often the feedback is provided. In conclusion, visually based augmented feedback leads to the simultaneous development of a spatial and motor representation of the task. The behind format led to a dependence on the spatial representation developed during training, while the side format facilitated the development of the motor representation as a means to overcome guidance.

Individual goals interact with dyad goals to constrain and facilitate the formation of interpersonal patterns of coordination.

Two experiments were undertaken to examine the spontaneous and intentional formation of interpersonal coordination patterns within dyads. In both experiments, each individual in a dyad was given a pre-set amplitude goal of tracing a 3 cm or 15 cm line to maintain over a trial. Smaller amplitudes were associated with faster movement frequencies compared to larger amplitudes in both experiments. All trials started with the partners in the dyads not seeing each other, and at the half-way point within a trial vision of the partner was provided. In experiment 1, each individual was told to watch their partners hand in the view segment, yet maintain the amplitude goal. The pre-set amplitude goals limited the emergence of spontaneous interpersonal coordination in the form of frequency-locking and phase-entrainment. In experiment 2, the individuals in the dyad were told to intentionally coordinate at either a defined in-phase or anti-phase pattern of coordination when entering the view segment of a trial. All dyads formed the required coordination patterns at a 1:1 frequency-locking across 90% of trials when entering the view segment. However, the pre-set amplitudes still influenced performance of individuals in terms of movement amplitude and frequency modulations when intentionally forming the required coordination patterns. The proposed hypotheses and the interpretation of the results are framed within the coordination dynamics theory of perception-action processes.

Differences in motor unit recruitment patterns and low frequency oscillation of discharge rates between unilateral and bilateral isometric muscle contractions.

INTRODUCTION: Distinct cortical activities contribute to unilateral and bilateral motor control. However, it remains largely unknown whether the behavior of motor neurons differs between unilateral and bilateral isometric force generation. Here, we first investigated motor units (MUs) recruitment patterns during unilateral and bilateral force generation. Considering that the force control is primarily regulated by low-frequency synaptic inputs to motor neurons, we also examined the relation between MU discharge rate and force output during unilateral and bilateral muscle contractions. METHODS: Using advanced electromyography (EMG) sensor arrays and spike-triggered averaging techniques, we examined a large population of MUs in the right first dorsal interosseous (FDI) muscle during unilateral and bilateral force tracking tasks. Using the principal component analysis, we analyzed the first common component (FCC) of MU discharge rate to describe the force fluctuations during unilateral and bilateral contractions. RESULTS: We found that MU discharge rate decreased during bilateral compared with unilateral contractions. MU recruitment threshold increased, while the amplitude and duration of MU action potential (MUAP) remained unchanged during bilateral compared with unilateral contractions. We found that the coefficients of variation (CV) for the force and FCC signal increased during bilateral compared with unilateral contractions. Notably, the FCC signal captured a great amount of MU discharge variability, and its CV correlated with the CV of the force signal. CONCLUSION: Our findings suggest that MU recruitment patterns are altered during bilateral compared with unilateral isometric force generation, likely related to changes at the low-frequency portion of the synaptic drive.

The Interactions Between Primary Somatosensory and Motor Cortex during Human Grasping Behaviors.

Afferent inputs to the primary somatosensory cortex (S1) are differentially processed during precision and power grip in humans. However, it remains unclear how S1 interacts with the primary motor cortex (M1) during these two grasping behaviors. To address this question, we measured short-latency afferent inhibition (SAI), reflecting S1-M1 interactions via thalamo-cortical pathways, using paired-pulse transcranial magnetic stimulation (TMS) during precision and power grip. The TMS coil over the hand representation of M1 was oriented in the posterior-anterior (PA) and anterior-posterior (AP) direction to activate distinct sets of corticospinal neurons. We found that SAI increased during precision compared with power grip when AP, but not PA, currents were applied. Notably, SAI tested in the AP direction were similar during two-digit than five-digit precision grip. The M1 receives movement information from S1 through direct cortico-cortical pathways, so intra-hemispheric S1-M1 interactions using dual-site TMS were also evaluated. Stimulation of S1 attenuated M1 excitability (S1-M1 inhibition) during precision and power grip, while the S1-M1 inhibition ratio remained similar across tasks. Taken together,our findings suggest that distinct neural mechanisms for S1-M1 interactions mediate precision and power grip, presumably by modulating neural activity along thalamo-cortical pathways.

The decay and consolidation of effector-independent motor memories.

Learning a motor adaptation task produces intrinsically unstable or transient motor memories. Despite the presence of effector-independent motor memories following the learning of novel environmental dynamics, it remains largely unknown how those memory traces decay in different contexts and whether an "offline" consolidation period protects memories against decay. Here, we exploit inter-effector transfer to address these questions. We found that newly acquired motor memories formed with one effector could be partially retrieved by the untrained effector to enhance its performance when the decay occurred with the passage of time or "washout" trials on which error feedback was provided. The decay of motor memories was slower following "error-free" trials, on which errors were artificially clamped to zero or removed, compared with "washout" trials. However, effector-independent memory components were abolished following movements made in the absence of task errors, resulting in no transfer gains. The brain can stabilize motor memories during daytime wakefulness. We found that 6 h of wakeful resting increased the resistance of effector-independent memories to decay. Collectively, our results suggest that the decay of effector-independent motor memories is context-dependent, and offline processing preserves those memories against decay, leading to improvements of the subsequent inter-effector transfer.

Improving online and offline gain from repetitive practice using anodal tDCS at dorsal premotor cortex.

Administering anodal transcranial direct current stimulation at the left dorsal premotor cortex (PMd) but not right PMd throughout the repetitive practice of three novel motor sequences resulted in improved offline performance usually only observed after interleaved practice. This gain only emerged following overnight sleep. These data are consistent with the proposed proprietary role of left PMd for motor sequence learning and the more recent claim that PMd is central to sleep-related consolidation of novel skill memory.

Impossible is nothing: 5:3 and 4:3 multi-frequency bimanual coordination.

The present findings demonstrate that when participants are provided a Lissajous display with cursor indicating the position of the limbs and a template illustrating the desired movement pattern they can rapidly (10 min) and effectively (continuous relative phase errors and variability ~10 degrees ) tune in a difficult 5:3 bimanual coordination pattern and without additional practice re-tune their responding to an equally difficult 4:3 coordination pattern. The findings indicate the extreme difficulty associated with producing complex polyrhythms in previous experiments has been due to split attention when Lissajous feedback has been provided and inability of the participant to detect and correct coordination errors when only provided vision of the limbs. Effective transfer to the 4:3 polyrhythm without previous practice suggests that the perception-action system's capabilities are extensive. The present findings when viewed in the context of recent experiments using similar protocols suggest that much, but not all, of the difficulty associated with producing a variety of bimanual coordination tasks should be viewed in terms of perceptual constraints imposed by the testing environment.