Distinct learning, retention, and generalization patterns in de novo learning versus motor adaptation.

People correct for movement errors when acquiring new motor skills (de novo learning) or adapting well-known movements (motor adaptation). While de novo learning establishes new control policies, adaptation modifies existing ones, and previous work have distinguished behavioral and underlying brain mechanisms for each motor learning type. However, it is still unclear whether learning in each type interferes with the other. In study 1, we use a within-subjects design where participants train with both 30° visuomotor rotation and mirror reversal perturbations, to compare adaptation and de novo learning respectively. We find no perturbation order effects, and find no evidence for differences in learning rates and asymptotes for both perturbations. Explicit instructions also provide an advantage during early learning in both perturbations. However, mirror reversal learning shows larger inter-participant variability and slower movement initiation. Furthermore, we only observe reach aftereffects following rotation training. In study 2, we incorporate the mirror reversal in a browser-based task, to investigate under-studied de novo learning mechanisms like retention and generalization. Learning persists across three or more days, substantially transfers to the untrained hand, and to targets on both sides of the mirror axis. Our results extend insights for distinguishing motor skill acquisition from adapting well-known movements.

Movement-goal relevant object shape properties act as poor but viable cues for the attribution of motor errors to external objects.

When a context change is detected during motor learning, motor memories-internal models for executing movements within some context-may be created or existing motor memories may be activated and modified. Assigning credit to plausible causes of errors can allow for fast retrieval and activation of a motor memory, or a combination of motor memories, when the presence of such causes is detected. Features of the movement-context intrinsic to the movement dynamics, such as posture of the end effector, are often effective cues for detecting context change whereas features extrinsic to the movement dynamics, such as the colour of an object being moved, are often not. These extrinsic cues are typically not relevant to the motor task at hand and can be safely ignored by the motor system. We conducted two experiments testing if extrinsic but movement-goal relevant object-shape cues during an object-transport task can act as viable contextual cues for error assignment to the object, and the creation of new, object-shape-associated motor memories. In the first experiment we find that despite the object-shape cues, errors are primarily attributed to the hand transporting the object. In a second experiment, we find participants can execute differing movements cued by the object shape in a dual adaptation task, but the extent of adaptation is small, suggesting that movement-goal relevant object-shape properties are poor but viable cues for creating context specific motor memories.

Motor adaptation does not differ when a perturbation is introduced abruptly or gradually.

People continuously adapt their movements to ever-changing circumstances, and particularly in skills training and rehabilitation, it is crucial that we understand how to optimize implicit adaptation in order for these processes to require as little conscious effort as possible. Although it is generally assumed that the way to do this is by introducing perturbations gradually, the literature is ambivalent on the effectiveness of this approach. Here, we tested whether there are differences in motor performance when adapting to an abrupt compared to a ramped visuomotor rotation. Using a within-subjects design, we tested this question under 3 different rotation sizes: 30-degrees, 45-degrees, and 60-degrees, as well as in 3 different populations: younger adults, older adults, and patients with mild cerebellar ataxia. We find no significant differences in either the behavioural outcomes, or model fits, between abrupt and gradual learning across any of the different conditions. Neither age, nor cerebellar ataxia had any significant effect on error-sensitivity either. These findings together indicate that error-sensitivity is not modulated by introducing a perturbation abruptly compared to gradually, and is also unaffected by age or mild cerebellar ataxia.

Adapting to visuomotor rotations in stepped increments increases implicit motor learning.

Human motor adaptation relies on both explicit conscious strategies and implicit unconscious updating of internal models to correct motor errors. Implicit adaptation is powerful, requiring less preparation time before executing adapted movements, but recent work suggests it is limited to some absolute magnitude regardless of the size of a visuomotor perturbation when the perturbation is introduced abruptly. It is commonly assumed that gradually introducing a perturbation should lead to improved implicit learning beyond this limit, but outcomes are conflicting. We tested whether introducing a perturbation in two distinct gradual methods can overcome the apparent limit and explain past conflicting findings. We found that gradually introducing a perturbation in a stepped manner, where participants were given time to adapt to each partial step before being introduced to a larger partial step, led to ~ 80% higher implicit aftereffects of learning, but introducing it in a ramped manner, where participants adapted larger rotations on each subsequent reach, did not. Our results clearly show that gradual introduction of a perturbation can lead to substantially larger implicit adaptation, as well as identify the type of introduction that is necessary to do so.

Reduced feedback barely slows down proprioceptive recalibration.

Introducing altered visual feedback of the hand produces quick adaptation of reaching movements. Our lab has shown that the associated shifts in estimates of the felt position of the hand saturate within a few training trials. The current study investigates whether the rapid changes in felt hand position that occur during classic visuomotor adaptation are diminished or slowed when training feedback is reduced. We reduced feedback by either providing visual feedback only at the end of the reach (terminal feedback) or constraining hand movements to reduce motor adaptation-related error signals such as sensory prediction errors and task errors (exposure). We measured changes as participants completed reaches with a 30° rotation, a -30° rotation, and clamped visual feedback, with these two "impoverished" training conditions, along with classic visuomotor adaptation training, while continuously estimating their felt hand position. Training with terminal feedback slightly reduced the initial rate of change in overall adaptation. However, the rate of change in hand localization, as well as the asymptote of hand localization shifts in both the terminal feedback group and the exposure training group was not noticeably different from those in the classic training group. Taken together, shifts in felt hand position are rapid and robust responses to sensory mismatches and are at best slightly modulated when feedback is reduced. This suggests that given the speed and invariance to the quality of feedback of proprioceptive recalibration, it could immediately contribute to all kinds of reach adaptation.NEW & NOTEWORTHY Reaching to targets with altered visual feedback about hand position leads to adaptation of movements as well as shifts in estimates of felt hand position. Felt hand position can shift in as little as one trial, and here we show that there is no noticeable reduction in speed when the feedback about movements is impoverished, indicating the robustness of the process of recalibrating felt hand position.

Multisensory visual-vestibular training improves visual heading estimation in younger and older adults.

Self-motion perception (e.g., when walking/driving) relies on the integration of multiple sensory cues including visual, vestibular, and proprioceptive signals. Changes in the efficacy of multisensory integration have been observed in older adults (OA), which can sometimes lead to errors in perceptual judgments and have been associated with functional declines such as increased falls risk. The objectives of this study were to determine whether passive, visual-vestibular self-motion heading perception could be improved by providing feedback during multisensory training, and whether training-related effects might be more apparent in OAs vs. younger adults (YA). We also investigated the extent to which training might transfer to improved standing-balance. OAs and YAs were passively translated and asked to judge their direction of heading relative to straight-ahead (left/right). Each participant completed three conditions: (1) vestibular-only (passive physical motion in the dark), (2) visual-only (cloud-of-dots display), and (3) bimodal (congruent vestibular and visual stimulation). Measures of heading precision and bias were obtained for each condition. Over the course of 3 days, participants were asked to make bimodal heading judgments and were provided with feedback ("correct"/"incorrect") on 900 training trials. Post-training, participants' biases, and precision in all three sensory conditions (vestibular, visual, bimodal), and their standing-balance performance, were assessed. Results demonstrated improved overall precision (i.e., reduced JNDs) in heading perception after training. Pre- vs. post-training difference scores showed that improvements in JNDs were only found in the visual-only condition. Particularly notable is that 27% of OAs initially could not discriminate their heading at all in the visual-only condition pre-training, but subsequently obtained thresholds in the visual-only condition post-training that were similar to those of the other participants. While OAs seemed to show optimal integration pre- and post-training (i.e., did not show significant differences between predicted and observed JNDs), YAs only showed optimal integration post-training. There were no significant effects of training for bimodal or vestibular-only heading estimates, nor standing-balance performance. These results indicate that it may be possible to improve unimodal (visual) heading perception using a multisensory (visual-vestibular) training paradigm. The results may also help to inform interventions targeting tasks for which effective self-motion perception is important.

Measuring the double-drift illusion and its resets with hand trajectories.

If a Gabor pattern drifts in one direction while its internal texture drifts in the orthogonal direction, its perceived position deviates further and further away from its true path. We first evaluated the illusion using manual tracking. Participants followed the Gabor with a stylus on a drawing tablet that coincided optically with the horizontal monitor surface. Their hand and the stylus were not visible during the tracking. The magnitude of the tracking illusion corresponded closely to previous perceptual and pointing measures indicating that manual tracking is a valid measure for the illusion. This allowed us to use it in a second experiment to capture the behavior of the illusion as it eventually degrades and breaks down in single trials. Specifically, the deviation of the Gabor stops accumulating at some point and either stays at a fixed offset or resets toward the veridical position. To report the perceived trajectory of the Gabor, participants drew it after the Gabor was removed from the monitor. Resets were detected and analyzed and their distribution matches neither a temporal nor a spatial limit, but rather a broad gamma distribution over time. This suggests that resets are triggered randomly, about once per 1.3 seconds, possible by extraneous distractions or eye movements.

Sensing hand position in Ehlers-Danlos syndrome.

PURPOSE: To explore the effect of joint hypermobility on acuity, and precision, of hand proprioception. MATERIALS AND METHODS: We compared proprioceptive acuity, and precision, between EDS patients and controls. We then measured any changes in their estimates of hand position after participants adapted their reaches in response to altered visual feedback of their hand. The Beighton Scale was used to quantify the magnitude of joint hypermobility. RESULTS: There were no differences between the groups in the accuracy of estimates of hand location, nor in the visually induced changes in hand location. However, EDS patients' estimates were less precise when based purely on proprioception and could be partially predicted by Beighton score. CONCLUSIONS: EDS patients are less precise at estimating their hand's location when only afferent information is available, but the presence of efferent signalling may reduce this imprecision. Those who are more hypermobile are more likely to be imprecise.

Differential contributions of implicit and explicit learning mechanisms to various contextual cues in dual adaptation.

The ability to switch between different visuomotor maps accurately and efficiently is an invaluable feature to a flexible and adaptive human motor system. This can be examined in dual adaptation paradigms where the motor system is challenged to perform under randomly switching, opposing perturbations. Typically, dual adaptation doesn't proceed unless each mapping is trained in association with a predictive cue. To investigate this, we first explored whether dual adaptation occurs under a variety of contextual cues including active follow-through movements, passive follow-through movements, active lead-in movements, and static visual cues. In the second experiment, we provided one group with a compensatory strategy about the perturbations (30° CW and 30° CCW rotations) and their relationships to each context (static visual cues). We found that active, but not passive, movement cues elicited dual adaptation. Expectedly, we didn't find evidence for dual adaptation using static visual cues, but those in the Instruction group compensated by implementing aiming strategies. Then, across all experimental conditions, we explored the extent by which dual learning is supported by both implicit and explicit mechanisms, regardless of whether they elicited dual adaptation across all the various cues. To this end, following perturbed training, participants from all experiments were asked to either use or ignore the strategy as they reached without visual feedback. This Process Dissociation Procedure teased apart the implicit and explicit contributions to dual adaptation. Critically, we didn't find evidence for implicit learning for those given instructions, suggesting that when explicit aiming strategies are implemented in dual adaptation, implicit mechanisms are likely not involved. Thus, by implementing conscious strategies, dual adaptation can be easily facilitated even in cases where learning would not occur otherwise.

Proprioceptive recalibration following implicit visuomotor adaptation is preserved in Parkinson's disease.

Individuals with Parkinson's disease (PD) and healthy adults demonstrate similar levels of visuomotor adaptation provided that the distortion is small or introduced gradually, and hence, implicit processes are engaged. Recently, implicit processes underlying visuomotor adaptation in healthy individuals have been proposed to include proprioceptive recalibration (i.e., shifts in one's proprioceptive sense of felt hand position to match the visual estimate of their hand experienced during reaches with altered visual feedback of the hand). In the current study, we asked if proprioceptive recalibration is preserved in PD patients. PD patients tested during their "off" and "on" medication states and age-matched healthy controls reached to visual targets, while visual feedback of their unseen hand was gradually rotated 30° clockwise or translated 4 cm rightwards of their actual hand trajectory. As expected, PD patients and controls produced significant reach aftereffects, indicating visuomotor adaptation after reaching with the gradually introduced visuomotor distortions. More importantly, following visuomotor adaptation, both patients and controls showed recalibration in hand position estimates, and the magnitude of this recalibration was comparable between PD patients and controls. No differences for any measures assessed were observed across medication status (i.e., PD off vs PD on). Results reveal that patients are able to adjust their sensorimotor mappings and recalibrate proprioception following adaptation to a gradually introduced visuomotor distortion, and that dopaminergic intervention does not affect this proprioceptive recalibration. These results suggest that proprioceptive recalibration does not involve striatal dopaminergic pathways and may contribute to the preserved visuomotor adaptation that arises implicitly in PD patients.

Modeling inter-trial variability of pointing movements during visuomotor adaptation.

Trial-to-trial variability during visuomotor adaptation is usually explained as the result of two different sources, planning noise and execution noise. The estimation of the underlying variance parameters from observations involving varying feedback conditions cannot be achieved by standard techniques (Kalman filter) because they do not account for recursive noise propagation in a closed-loop system. We therefore developed a method to compute the exact likelihood of the output of a time-discrete and linear adaptation system as has been used to model visuomotor adaptation (Smith et al. in PLoS Biol 4(6):e179, 2006), observed under closed-loop and error-clamp conditions. We identified the variance parameters by maximizing this likelihood and compared the model prediction of the time course of variance and autocovariance with empiric data. The observed increase in variability during the early training phase could not be explained by planning noise and execution noise with constant variances. Extending the model by signal-dependent components of either execution noise or planning noise showed that the observed temporal changes of the trial-to-trial variability can be modeled by signal-dependent planning noise rather than signal-dependent execution noise. Comparing the variance time course between different training schedules showed that the signal-dependent increase of planning variance was specific for the fast adapting mechanism, whereas the assumption of constant planning variance was sufficient for the slow adapting mechanisms.

Implicit motor learning within three trials.

In motor learning, the slow development of implicit learning is traditionally taken for granted. While much is known about training performance during adaptation to a perturbation in reaches, saccades and locomotion, little is known about the time course of the underlying implicit processes during normal motor adaptation. Implicit learning is characterized by both changes in internal models and state estimates of limb position. Here, we measure both as reach aftereffects and shifts in hand localization in our participants, after every training trial. The observed implicit changes were near asymptote after only one to three perturbed training trials and were not predicted by a two-rate model's slow process that is supposed to capture implicit learning. Hence, we show that implicit learning is much faster than conventionally believed, which has implications for rehabilitation and skills training.

External error attribution dampens efferent-based predictions but not proprioceptive changes in hand localization.

In learning and adapting movements in changing conditions, people attribute the errors they experience to a combined weighting of internal or external sources. As such, error attribution that places more weight on external sources should lead to decreased updates in our internal models for movement of the limb or estimating the position of the effector, i.e. there should be reduced implicit learning. However, measures of implicit learning are the same whether or not we induce explicit adaptation with instructions about the nature of the perturbation. Here we evoke clearly external errors by either demonstrating the rotation on every trial, or showing the hand itself throughout training. Implicit reach aftereffects persist, but are reduced in both groups. Only for the group viewing the hand, changes in hand position estimates suggest that predicted sensory consequences are not updated, but only rely on recalibrated proprioception. Our results show that estimating the position of the hand incorporates source attribution during motor learning, but recalibrated proprioception is an implicit process unaffected by external error attribution.

The effect of age on visuomotor learning processes.

Knowing where our limbs are in space is essential for moving and for adapting movements to various changes in our environments and bodies. The ability to adapt movements declines with age, and age-related cognitive decline can explain a decreased ability to adopt and deploy explicit, cognitive strategies in motor learning. Age-related sensory decline could also lead to a reduced fidelity of sensory position signals and error signals, each of which can affect implicit motor adaptation. Here we investigate two estimates of limb position; one based on proprioception, the other on predicted sensory consequences of movements. Each is considered a measure of an implicit adaptation process and may be affected by both age and cognitive strategies. Both older (n = 38) and younger (n = 42) adults adapted to a 30° visuomotor rotation in a centre-out reaching task. We make an explicit, cognitive strategy available to half of participants in each age group with a detailed instruction. After training, we first quantify the explicit learning elicited by instruction. Instructed older adults initially use the provided strategy slightly less than younger adults but show a similar ability to evoke it after training. This indicates that cognitive explanations for age-related decline in motor learning are limited. In contrast, training induced much larger shifts of state estimates of hand location in older adults compared to younger adults. This is not modulated by strategy instructions, and appears driven by recalibrated proprioception, which is almost twice as large in older adults, while predictions might not be updated in older adults. This means that in healthy aging, some implicit processes may be compensating for other changes to maintain motor capabilities, while others also show age-related decline (data: https://osf.io/qzhmy).

Motor learning without moving: Proprioceptive and predictive hand localization after passive visuoproprioceptive discrepancy training.

An accurate estimate of limb position is necessary for movement planning, before and after motor learning. Where we localize our unseen hand after a reach depends on felt hand position, or proprioception, but in studies and theories on motor adaptation this is quite often neglected in favour of predicted sensory consequences based on efference copies of motor commands. Both sources of information should contribute, so here we set out to further investigate how much of hand localization depends on proprioception and how much on predicted sensory consequences. We use a training paradigm combining robot controlled hand movements with rotated visual feedback that eliminates the possibility to update predicted sensory consequences ('exposure training'), but still recalibrates proprioception, as well as a classic training paradigm with self-generated movements in another set of participants. After each kind of training we measure participants' hand location estimates based on both efference-based predictions and afferent proprioceptive signals with self-generated hand movements ('active localization') as well as based on proprioception only with robot-generated movements ('passive localization'). In the exposure training group, we find indistinguishable shifts in passive and active hand localization, but after classic training, active localization shifts more than passive, indicating a contribution from updated predicted sensory consequences. Both changes in open-loop reaches and hand localization are only slightly smaller after exposure training as compared to after classic training, confirming that proprioception plays a large role in estimating limb position and in planning movements, even after adaptation. (data: https://doi.org/10.17605/osf.io/zfdth, preprint: https://doi.org/10.1101/384941).

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).

The fast contribution of visual-proprioceptive discrepancy to reach aftereffects and proprioceptive recalibration.

Adapting reaches to altered visual feedback not only leads to motor changes, but also to shifts in perceived hand location; "proprioceptive recalibration". These changes are robust to many task variations and can occur quite rapidly. For instance, our previous study found both motor and sensory shifts arise in as few as 6 rotated-cursor training trials. The aim of this study is to investigate one of the training signals that contribute to these rapid sensory and motor changes. We do this by removing the visuomotor error signals associated with classic visuomotor rotation training; and provide only experience with a visual-proprioceptive discrepancy for training. While a force channel constrains reach direction 30o away from the target, the cursor representing the hand unerringly moves straight to the target. The resulting visual-proprioceptive discrepancy drives significant and rapid changes in no-cursor reaches and felt hand position, again within only 6 training trials. The extent of the sensory change is unexpectedly larger following the visual-proprioceptive discrepancy training. Not surprisingly the size of the reach aftereffects is substantially smaller than following classic visuomotor rotation training. However, the time course by which both changes emerge is similar in the two training types. These results suggest that even the mere exposure to a discrepancy between felt and seen hand location is a sufficient training signal to drive robust motor and sensory plasticity.

Context-dependent concurrent adaptation to static and moving targets.

Is the neural control of movements towards moving targets independent to that of static targets? In the following experiments, we used a visuomotor rotation adaptation paradigm to examine the extent to which adapting arm movements to static targets generalize to that of moving targets (i.e. pursuit or tracking). In the first and second experiments, we showed that adaptation to perturbed tracking movements generalizes to reaching movements; reach aftereffects following perturbed tracking were about half the size (≈9°) of those produced following reach training (≈ 19°). Given these findings, in the final experiment we associated opposing perturbations (-30° and +30°) with either reaching or tracking movements and presented them within the same experimental block to determine whether these contexts allow for dual adaptation. We found that the group that experienced opposing perturbations was able to reduce both reaching and tracking errors, as well as produce reach aftereffects following dual training of ≈7°, which were substantially smaller than those produced when reach training was not concurrent with tracking training. This reduction in reach aftereffects is consistent with the extent of the interference from tracking training as measured by the reach aftereffects produced when only that condition was performed. These results suggest partial, but not complete, overlap in the learning processes involved in the acquisition of tracking and reaching movements.

Correction: Separating Predicted and Perceived Sensory Consequences of Motor Learning.

[This corrects the article DOI: 10.1371/journal.pone.0163556.].