Visuomotor Rotation Research Articles

Motor imagery and action observation for predictive control in developmental coordination disorder.

In 2019, international clinical practice recommendations on the definition, diagnosis, assessment, intervention, and psychosocial aspects of developmental coordination disorder (DCD) were published. Informing our understanding of mechanisms, recent systematic reviews have shown that children with DCD have difficulties with the predictive control of movements, including aspects of motor planning, which is expressed as the internal modeling deficit hypothesis. This motor control deficit is most evident when the spatial and temporal demands of a task increase. An increasing number of empirical studies suggest that motor planning problems can be remediated through training based on one or a combination of motor imagery and action observation. In this review, we show evidence of motor planning problems in children with DCD and show that task demands or complexity affects its appearance. Implications of these findings are treatments based on motor imagery and action observation to remediate motor planning issues. The article concludes with recommendations for future research.

Cerebellar – Premotor cortex interactions underlying visuomotor adaptation

Visuomotor adaptation (VMA) is a form of motor learning essential for performing day to day routines. Theoretical models and empirical evidence suggest a specific cortico-striato-cerebellar loop that mediates early and late learning in VMA. Here, we investigated dynamic changes in neural activity and connectivity when learning a novel visuomotor rotation using fMRI. We found that motor cortical regions, parietal cortex and cerebellum are recruited in the early phase of VMA, gradually reduce their activity as learning reaches plateau and rebound when the visuomotor rotation is removed. At this phase, dubbed de-adaptation, individual performance correlated with activity in motor and parietal cortex such that stronger activity was associated with better performance. Theory suggests that VMA is governed by the cortico-striato-cerebellar network during the early phase of learning and by the cortico-cerebellar loop at later stages. We tested this hypothesis using dynamic causal modelling and found distinct modulation of a cerebellar to dorsal premotor cortex (dPMC) loop. Specifically, the cerebellar to dPMC connection was modulated during adaptation, suggesting a release of inhibition and net excitatory effect of cerebellum on dPMC. The modulation of cerebellar to dPMC connection during de-adaptation was specifically related to behavioral learning parameter: stronger release of inhibition of the cerebellar to dPMC connection was associated with better de-adaptation. We interpret these findings to reflect dynamic interactions between representation of movement in cerebellum and visuomotor integration in dPMC.

Characterization of the Adaptation to Visuomotor Rotations in the Muscle Synergies Space.

The adaptation to visuomotor rotations is one of the most studied paradigms of motor learning. Previous literature has presented evidence of a dependency between the process of adaptation to visuomotor rotations and the constrains dictated by the workspace of the biological actuators, the muscles, and their co-activation strategies, modeled using muscle synergies analysis. To better understand this relationship, we asked a sample of healthy individuals (N = 7) to perform two experiments aiming at characterizing the adaptation to visuomotor rotations in terms of rotations of the activation space of the muscle synergies during isometric reaching tasks. In both experiments, subjects were asked to adapt to visual rotations altering the position mapping between the force exerted on a fixed manipulandum and the movement of a cursor on a screen. In the first experiment subjects adapted to three different visuomotor rotation angles (30°, 40°, and 50° clockwise) applied to the whole experimental workspace. In the second experiment subjects adapted to a single visuomotor rotation angle (45° clockwise) applied to eight different sub-spaces of the whole workspace, while also performing movements in the rest of the unperturbed workspace. The results from the first experiment confirmed the hypothesis that visuomotor rotations induce rotations in the synergies activation workspace that are proportional to the visuomotor rotation angle. The results from the second experiment showed that rotations affecting limited sub-spaces of the whole workspace are adapted for by rotating only the synergies involved in the movement, with an angle proportional to the distance between the preferred angle of the synergy and the sub-space covered by the rotation. Moreover, we show that the activation of a synergy is only rotated when the sub-space covered by the visual perturbation is applied at the boundaries of the workspace of the synergy. We found these results to be consistent across subjects, synergies and sub-spaces. Moreover, we found a correlation between synergies and muscle rotations further confirming that the adaptation process can be well described, at the neuromuscular level, using the muscle synergies model. These results provide information on how visuomotor rotations can be used to induce a desired neuromuscular response.

A condition that produces sensory recalibration and abolishes multisensory integration

We examined the influence of extended exposure to a visuomotor rotation, which induces both motor adaptation and sensory recalibration, on (partial) multisensory integration in a cursor-control task. Participants adapted to a 30° (adaptation condition) or 0° (control condition) visuomotor rotation by making center-out movements to remembered targets. In subsequent test trials of sensory integration, they made center-out movements with variable visuomotor rotations and judged the position of hand or cursor at the end of these movements. Test trials were randomly embedded among twice the number of maintenance trials with 30° or 0° rotation. The biases of perceived hand (or cursor) position toward the cursor (or hand) position were measured. We found motor adaptation together with proprioceptive and visual recalibrations in the adaptation condition. Unexpectedly, multisensory integration was absent in both the adaptation and control condition. The absence stemmed from the extensive experience of constant visuomotor rotations of 30° or 0°, which probably produced highly precise predictions of the visual consequences of hand movements. The frequently confirmed predictions then dominated the estimate of the visual movement consequences, leaving no influence of the actual visuomotor rotations in the minority of test trials. Conversely, multisensory integration was present for sensed hand positions when these were indirectly assessed from movement characteristics, indicating that the relative weighting of discrepant estimates of hand position was different for motor control. The existence of a condition that abolishes multisensory integration while keeping sensory recalibration suggests that mechanisms that reduce sensory discrepancies (partly) differ between integration and recalibration.

Human decision making anticipates future performance in motor learning.

It is well-established that people can factor into account the distribution of their errors in motor performance so as to optimize reward. Here we asked whether, in the context of motor learning where errors decrease across trials, people take into account their future, improved performance so as to make optimal decisions to maximize reward. One group of participants performed a virtual throwing task in which, periodically, they were given the opportunity to select from a set of smaller targets of increasing value. A second group of participants performed a reaching task under a visuomotor rotation in which, after performing a initial set of trials, they selected a reward structure (ratio of points for target hits and misses) for different exploitation horizons (i.e., numbers of trials they might be asked to perform). Because movement errors decreased exponentially across trials in both learning tasks, optimal target selection (task 1) and optimal reward structure selection (task 2) required taking into account future performance. The results from both tasks indicate that people anticipate their future motor performance so as to make decisions that will improve their expected future reward.

Single-Pulse TMS over the Parietal Cortex Does Not Impair Sensorimotor Perturbation-Induced Changes in Motor Commands.

Intermittent exposure to a sensorimotor perturbation, such as a visuomotor rotation, is known to cause a directional bias on the subsequent movement that opposes the previously experienced perturbation. To date, it is unclear whether the parietal cortex is causally involved in this postperturbation movement bias. In a recent electroencephalogram study, Savoie et al. (2018) observed increased parietal activity in response to an intermittent visuomotor perturbation, raising the possibility that the parietal cortex could subserve this change in motor behavior. The goal of the present study was to causally test this hypothesis. Human participants (N = 28) reached toward one of two visual targets located on either side of a fixation point, while being pseudorandomly submitted to a visuomotor rotation. On half of all rotation trials, single-pulse transcranial magnetic stimulation (TMS) was applied over the right (N = 14) or left (N = 14) parietal cortex 150 ms after visual feedback provision. To determine whether TMS influenced the postperturbation bias, reach direction was compared on trials that followed rotation with (RS + 1) and without (R + 1) TMS. It was hypothesized that interfering with parietal activity would reduce the movement bias following rotated trials. Results revealed a significant and robust postrotation directional bias compared with both rotation and null rotation trials. Contrary to our hypothesis, however, neither left nor right parietal stimulation significantly impacted the postrotation bias. These data suggest that the parietal areas targeted here may not be critical for perturbation-induced motor output changes to emerge.

Targeted tDCS selectively improves motor adaptation with the proximal and distal upper limb

BackgroundThe cerebellum and primary motor cortex (M1) are crucial to coordinated and accurate movements of the upper limbs. There is also appreciable evidence that these two structures exert somewhat divergent influences upon proximal versus distal upper limb control. Here, we aimed to differentially regulate the contribution of the cerebellum and M1 to proximal and distal effectors during motor adaptation, with transcranial direct current stimulation (tDCS). For this, we employed tasks that promote similar motor demands, but isolate whole arm from hand/finger movements, in order to functionally segregate the hierarchy of upper limb control. MethodsBoth young and older adults took part in a visuomotor rotation task; where they adapted to a 60° visuomotor rotation using either a hand-held joystick (requiring finger/hand movements) or a 2D robotic manipulandum (requiring whole-arm reaching movements), while M1, cerebellar or sham tDCS was applied. ResultsWe found that cerebellar stimulation improved adaptation performance when arm movements were required to complete the task, while in contrast stimulation of M1 enhanced adaptation during hand and finger movements only. This double-dissociation was replicated in an independent group of older adults, demonstrating that the behaviour remains intact in ageing. ConclusionsThese results suggest that stimulation of distinct motor areas can selectively improve motor adaptation in the proximal and distal upper limb. This also highlights new ways in which tDCS might be best applied to achieve reliable rehabilitation of upper limb motor deficits.

Neurophysiological Correlates of Adaptation and Interference during Asymmetrical Bimanual Movements

In this study, we investigated brain dynamics during interference between hands during bimanual movements. Participants performed a bimanual center-out reaching task in which a visuomotor rotation was applied to the right hand while the left hand did not receive visual feedback of its movements. This manipulation resulted in interference from the adapting right hand to the kinesthetically guided left hand. Electroencephalography (EEG) recordings during the task showed that spectral power in the high and low beta frequency bands was elevated early in exposure, but decreased throughout learning. This may be representative of error-based updating of internal models of movement. Additionally, coherence, a measure of neural functional connectivity, was elevated both within and between hemispheres in the beta frequencies during the initial presentation of the visuomotor rotation, and then decreased throughout adaptation. This suggests that beta oscillatory neural activity may be marker for transmission of conflicting motor information between hemispheres, which manifests in interference between the hands during asymmetrical bimanual movements.

Combined action observation and motor imagery facilitates visuomotor adaptation in children with developmental coordination disorder

The internal modelling deficit (IMD) hypothesis suggests that motor control issues associated with Developmental Coordination Disorder (DCD) are the result of impaired predictive motor control. In this study, we examined the benefits of a combined action observation and motor imagery (AO + MI) intervention designed to alleviate deficits in internal modelling and improve eye-hand coordination during a visuomotor rotation task. Twenty children with DCD were randomly assigned to either an AO + MI group (who watched a video of a performer completing the task whilst simultaneously imagining the kinaesthetic sensations associated with action execution) or a control group (who watched unrelated videos involving no motor content). Each group then attempted to learn a 90° visuomotor rotation while measurements of completion time, eye-movement behaviour and movement kinematics were recorded. As predicted, after training, the AO + MI group exhibited quicker completion times, more target-focused eye-movement behaviour and smoother movement kinematics compared to the control group. No significant after-effects were present. These results offer further support for the IMD hypothesis and suggest that AO + MI interventions may help to alleviate such deficits and improve motor performance in children with DCD.

Activity in Primary Motor Cortex Related to Visual Feedback

Neural modulation in primate motor cortex exhibits complex patterns. We found that modulation during reaching could be separated into discrete temporal epochs. To determine if these epochs are driven by behavioral events, monkeys performed variations of a center-out reaching task. Monkeys viewed a computer cursor matched to hand position and a radial target at 1 of 16 locations. In some trials, they performed a visuomotor rotation (the cursor moved at an angle to the hand). After adaptation, encoding changes for single units are temporally structured: adaptation could affect one temporal component of a unit's response but not another. In half the normal and perturbed trials, we removed visual feedback before movement. Adaptation-sensitive firing components toward the end of movement are often weak or absent during reaches without feedback. These results show that temporal structure in motor cortical activity is driven by behavior, with a discrete component related to visual feedback.

How different effectors and action effects modulate the formation of separate motor memories

Humans can operate a variety of modern tools, which are often associated with different visuomotor transformations. Studies investigating this ability have shown that separate motor memories can be acquired implicitly when different sensorimotor transformations are associated with distinct (intended) postures or explicitly when abstract contextual cues are leveraged by aiming strategies. It still remains unclear how different transformations are remembered implicitly when postures are similar. We investigated whether features of planning to manipulate a visual tool, such as its visual identity or the environmental effect intended by its use (i.e. action effect) would enable implicit learning of opposing visuomotor rotations. Results show that neither contextual cue led to distinct implicit motor memories, but that cues only affected implicit adaptation indirectly through generalization around explicit strategies. In contrast, a control experiment where participants practiced opposing transformations with different hands did result in contextualized aftereffects differing between hands across generalization targets. It appears that different (intended) body states are necessary for separate aftereffects to emerge, suggesting that the role of sensory prediction error-based adaptation may be limited to the recalibration of a body model, whereas establishing separate tool models may proceed along a different route.

The effects of awareness of the perturbation during motor adaptation on hand localization.

Awareness of task demands is often used during rehabilitation and sports training by providing instructions which appears to accelerate learning and improve performance through explicit motor learning. However, the effects of awareness of perturbations on the changes in estimates of hand position resulting from motor learning are not well understood. In this study, people adapted their reaches to a visuomotor rotation while either receiving instructions on the nature of the perturbation, experiencing a large rotation, or both to generate awareness of the perturbation and increase the contribution of explicit learning. We found that instructions and/or larger rotations allowed people to activate or deactivate part of the learned strategy at will and elicited explicit changes in open-loop reaches, while a small rotation without instructions did not. However, these differences in awareness, and even manipulations of awareness and perturbation size, did not appear to affect learning-induced changes in hand-localization estimates. This was true when estimates of the adapted hand location reflected changes in proprioception, produced when the hand was displaced by a robot, and also when hand location estimates were based on efferent-based predictions of self-generated hand movements. In other words, visuomotor adaptation led to significant shifts in predicted and perceived hand location that were not modulated by either instruction or perturbation size. Our results indicate that not all outcomes of motor learning benefit from an explicit awareness of the task. Particularly, proprioceptive recalibration and the updating of predicted sensory consequences appear to be largely implicit. (data: https://doi.org/10.17605/osf.io/mx5u2, preprint: https://doi.org/10.31234/osf.io/y53c2)

Practice induces a qualitative change in the memory representation for visuomotor learning.

Adaptation of our movements to changes in the environment is known to be supported by multiple learning processes that operate in parallel. One is an implicit recalibration process driven by sensory-prediction errors; the other process counters the perturbation through more deliberate compensation. Prior experience is known to enable adaptation to occur more rapidly, a phenomenon known as "savings," but exactly how experience alters each underlying learning process remains unclear. We measured the relative contributions of implicit recalibration and deliberate compensation to savings across 2 days of practice adapting to a visuomotor rotation. The rate of implicit recalibration showed no improvement with repeated practice. Instead, practice led to deliberate compensation being expressed even when preparation time was very limited. This qualitative change is consistent with the proposal that practice establishes a cached association linking target locations to appropriate motor output, facilitating a transition from deliberate to automatic action selection.NEW & NOTEWORTHY Recent research has shown that savings for visuomotor adaptation is attributable to retrieval of intentional, strategic compensation. This does not seem consistent with the implicit nature of memory for motor skills and calls into question the validity of visuomotor adaptation of reaching movements as a model for motor skill learning. Our findings suggest a solution: that additional practice adapting to a visuomotor perturbation leads to the caching of the initially explicit strategy for countering it.

Motor Adaptation Impairment in Chronic Cannabis Users Assessed by a Visuomotor Rotation Task.

Background—The cerebellum has been recently suggested as an important player in the addiction brain circuit. Cannabis is one of the most used drugs worldwide, and its long-term effects on the central nervous system are not fully understood. No valid clinical evaluations of cannabis impact on the brain are available today. The cerebellum is expected to be one of the brain structures that are highly affected by prolonged exposure to cannabis, due to its high density in endocannabinoid receptors. We aim to use a motor adaptation paradigm to indirectly assess cerebellar function in chronic cannabis users (CCUs). Methods—We used a visuomotor rotation (VMR) task that probes a putatively-cerebellar implicit motor adaptation process together with the learning and execution of an explicit aiming rule. We conducted a case-control study, recruiting 18 CCUs and 18 age-matched healthy controls. Our main measure was the angular aiming error. Results—Our results show that CCUs have impaired implicit motor adaptation, as they showed a smaller rate of adaptation compared with healthy controls (drift rate: 19.3 +/− 6.8° vs. 27.4 +/− 11.6°; t(26) = −2.1, p = 0.048, Cohen’s d = −0.8, 95% CI = (−1.7, −0.15)). Conclusions—We suggest that a visuomotor rotation task might be the first step towards developing a useful tool for the detection of alterations in implicit learning among cannabis users.

Basal ganglia contributions during the learning of a visuomotor rotation: Effect of dopamine, deep brain stimulation and reinforcement.

It is commonly thought that visuomotor adaptation is mediated by the cerebellum while reinforcement learning is mediated by the basal ganglia. In contrast to this strict dichotomy, we demonstrate a role for the basal ganglia in visuomotor adaptation (error-based motor learning) in patients with Parkinson's disease (PD) by comparing the degree of motor learning in the presence and absence of dopamine medication. We further show similar modulation of learning rates in the presence and absence of subthalamic deep brain stimulation. We also report that reinforcement is an essential component of visuomotor adaptation by demonstrating the lack of motor learning in patients with PD during the ON-dopamine state relative to the OFF-dopamine state in the absence of a reinforcement signal. Taken together, these results raise the possibility that the basal ganglia modulate the gain of visuomotor adaptation based on the reinforcement received at the end of the trial.

Rewards interact with repetition-dependent learning to enhance long-term retention of motor memories.

The combination of behavioral experiences that enhance long-term retention remains largely unknown. Informed by neurophysiological lines of work, this study tested the hypothesis that performance-contingent monetary rewards potentiate repetition-dependent forms of learning, as induced by extensive practice at asymptote, to enhance long-term retention of motor memories. To this end, six groups of 14 participants (n=84) acquired novel motor behaviors by adapting to a gradual visuomotor rotation while these factors were manipulated. Retention was assessed 24 h later. While all groups similarly acquired the novel motor behaviors, results from the retention session revealed an interaction indicating that rewards enhanced long-term retention, but only when practice was extended to asymptote. Specifically, the interaction indicated that this effect selectively occurred when rewards were intermittently available (i.e., 50%), but not when they were absent (i.e., 0%) or continuously available (i.e., 100%) during acquisition. This suggests that the influence of rewards on extensive practice and long-term retention is nonlinear, as continuous rewards did not further enhance retention as compared with intermittent rewards. One possibility is that rewards' intermittent availability allows to maintain their subjective value during acquisition, which may be key to potentiate long-term retention.

Combining Action Observation and Motor Imagery Improves Eye–Hand Coordination during Novel Visuomotor Task Performance

In this study, we compared the effectiveness of concurrent action observation and motor imagery (AO + MI), observing with the intent to imitate (active observation; AO), and passive observation (PO) training interventions for improving eye–hand coordination. Fifty participants were assigned to five groups [AO + MI, AO, PO, physical practice (PP); control] and performed a visuomotor rotation task, whilst eye movements were recorded. Each participant then performed 20 task trials in a training intervention before repeating the visuomotor rotation task in a post-test. As expected, PP produced the greatest improvement in task performance and eye–hand coordination. However, in comparison to the control group, AO + MI training produced a statistically significant increase in both task performance and eye–hand coordination, but no such improvements were found following AO or PO.

Visual and proprioceptive recalibrations after exposure to a visuomotor rotation.

Adaptation to a visuomotor rotation in a cursor-control task is accompanied by proprioceptive recalibration, whereas the existence of visual recalibration is uncertain and has even been doubted. In the present study, we tested both visual and proprioceptive recalibration; proprioceptive recalibration was not only assessed by means of psychophysical judgments of the perceived position of the hand, but also by an indirect procedure based on movement characteristics. Participants adapted to a gradually introduced visuomotor rotation of 30° by making center-out movements to remembered targets. In subsequent test trials, they made center-out movements without visual feedback or observed center-out motions of a cursor without moving the hand. In each test trial, they judged the endpoint of hand or cursor by matching the position of the hand or of a visual marker, respectively, moving along a semicircular path. This path ran through all possible endpoints of the center-out movements. We observed proprioceptive recalibration of 7.3° (3.1° with the indirect procedure) and a smaller, but significant, visual recalibration of 1.3°. Total recalibration of 8.6° was about half as strong as motor adaptation, the adaptive shift of the movement direction. The evidence of both proprioceptive and visual recalibration was obtained with a judgment procedure that suggests that recalibration is restricted to the type of movement performed during exposure to a visuomotor rotation. Consequently, identical physical positions of the hand can be perceived differently depending on how they have been reached, and similarly identical positions of a cursor on a monitor can be perceived differently.

The effect of skill level matching in dyadic interaction on learning of a tracing task.

Dyadic interaction between humans has gained great research interest in the last years. The effects of factors that influence the interaction, as e.g. roles or skill level matching, are still not well understood. In this paper, we further investigated the effect of skill level matching between partners on learning of a visuo-motor task. Understanding the effect of skill level matching is crucial for applications in collaborative rehabilitation. Fifteen healthy participants were asked to trace a path while being subjected to a visuo-motor rotation (Novice). The Novices were paired with a partner, forming one of the three Dyad Types: a) haptic connection to another Novice, b) haptic connection to an Expert (no visuo-motor rotation), or c) no haptic. The intervention consisted of a Familiarization phase, followed by a Training phase, in which the Novices were learning the task in the respective Dyad Type, and a Test phase in which the learning was assessed (haptic connection removed, if any). Results suggest that learning of the task with a haptic connection to an Expert was least beneficial. However, during the Training phase the dyads comprising an Expert clearly outperformed the dyads with matched skill levels. The results point towards the same direction as previous findings in literature and can be explained by current motor-learning theories. Future work needs to corroborate these preliminary results.

Combining reward and M1 transcranial direct current stimulation enhances the retention of newly learnt sensorimotor mappings

BackgroundReward-based feedback given during motor learning has been shown to improve the retention of the behaviour being acquired. Interestingly, applying transcranial direct current stimulation (tDCS) during learning over the primary motor cortex (M1), an area associated with motor retention, also results in enhanced retention of the newly formed motor memories. However, it remains unknown whether combining these distinct interventions result in an additive benefit of motor retention. MethodsWe investigated whether combining both interventions while participants learned to account for a visuomotor transformation results in enhanced motor retention (total n = 56; each group n = 14). To determine whether these interventions share common physiological mechanisms underpinning learning, we assessed motor cortical excitability and inhibition (i.e. SICI) on a hand muscle before and after all participants learned the visuomotor rotation using their entire arm and hand. ResultsWe found that both the Reward-Stim (i.e. reward + tDCS) and Reward-Sham (i.e. reward-only) groups had increased retention at the beginning of the retention phase, indicating an immediate effect of reward on behaviour. However, each intervention on their own did not enhance retention when compared to sham, but rather, only the combination of both reward and tDCS demonstrated prolonged retention. We also found that only the Reward-Stim group had a significant reduction in SICI after exposure to the perturbation. ConclusionsWe show that combining both interventions are additive in providing stronger retention of motor adaptation. These results indicate that the reliability and validity of using tDCS within a clinical context may depend on the type of feedback individuals receive when learning a new motor pattern.