Working memory constraints for visuomotor retrieval strategies.

Recent work has shown the fundamental role that cognitive strategies play in visuomotor adaptation. While algorithmic strategies, such as mental rotation, are flexible and generalizable, they are computationally demanding. To avoid this computational cost, people can instead rely on memory retrieval of previously successful visuomotor solutions. However, such a strategy is likely subject to strict stimulus-response associations and rely heavily on working memory. In a series of five experiments, we sought to estimate the constraints in terms of capacity and precision of working memory retrieval for visuomotor adaptation. This was accomplished by leveraging different variations of visuomotor item-recognition and visuomotor rotation tasks where we associated unique rotations with specific targets in the workspace and manipulated the set size (i.e., number of rotation-target associations). Notably, from Experiment 1 to 4, we found key signatures of working memory retrieval and not mental rotation. In particular, participants were less accurate and slower for larger set sizes and less recent items. Using a Bayesian latent-mixture model, we found that such decrease in performance was the result of increasing guessing behavior and less precise memories. In addition we estimated that participants' working memory capacity was limited to 2-5 items, after which guessing increasingly dominated performance. Finally, in Experiment 5, we showed how the constraints observed across Experiments 1 to 4 can be overcome when relying on long-term memory retrieval. Our results point to the opportunity of studying other sources of memories where visuomotor solutions can be stored (e.g., episodic memories) to achieve successful adaptation.

Exploring the role of task success in implicit motor adaptation.

Although implicit motor adaptation is driven by sensory-prediction errors (SPEs), recent work has shown that task success modulates this process. Task success has typically been defined as hitting a target, which signifies the goal of the movement. Visuomotor adaptation tasks are uniquely situated to experimentally manipulate task success independently from SPE by changing the target size or the location of the target. These two, distinct manipulations may influence implicit motor adaptation in different ways, so, over four experiments, we sought to probe the efficacy of each manipulation. We found that changes in target size, which caused the target to fully envelop the cursor, only affected implicit adaptation for a narrow range of SPE sizes, while jumping the target to overlap with the cursor more reliably and robustly affected implicit adaptation. Taken together, our data indicate that, while task success exerts a small effect on implicit adaptation, these effects are susceptible to methodological variations. Future investigations of the effect of task success on implicit adaptation could benefit from employing target jump manipulations instead of target size manipulations.NEW & NOTEWORTHY Recent work has suggested that task success, namely, hitting a target, influences implicit motor adaptation. Here, we observed that implicit adaptation is modulated by target jump manipulations, where the target abruptly "jumps" to meet the cursor; however, implicit adaptation was only weakly modulated by target size manipulations, where a static target either envelops or excludes the cursor. We discuss how these manipulations may exert their effects through different mechanisms.

Continuous manipulation of mental representations is compromised in cerebellar degeneration.

We introduce a novel perspective on how the cerebellum might contribute to cognition, hypothesizing that this structure supports dynamic transformations of mental representations. In support of this hypothesis, we report a series of neuropsychological experiments comparing the performance of individuals with degenerative cerebellar disorders on tasks that either entail continuous, movement-like mental operations or more discrete mental operations. In the domain of visual cognition, the cerebellar disorders group exhibited an impaired rate of mental rotation, an operation hypothesized to require the continuous manipulation of a visual representation. In contrast, the cerebellar disorders group showed a normal processing rate when scanning items in visual working memory, an operation hypothesized to require the maintenance and retrieval of remembered items. In the domain of mathematical cognition, the cerebellar disorders group was impaired at single-digit addition, an operation hypothesized to primarily require iterative manipulations along a mental number-line; this group was not impaired on arithmetic tasks linked to memory retrieval (e.g. single-digit multiplication). These results, obtained in tasks from two disparate domains, point to a potential constraint on the contribution of the cerebellum to cognitive tasks. Paralleling its role in motor control, the cerebellum may be essential for coordinating dynamic, movement-like transformations in a mental workspace.

Revisiting the Role of the Medial Temporal Lobe in Motor Learning.

Classic taxonomies of memory distinguish explicit and implicit memory systems, placing motor skills squarely in the latter branch. This assertion is in part a consequence of foundational discoveries showing significant motor learning in amnesics. Those findings suggest that declarative memory processes in the medial temporal lobe (MTL) do not contribute to motor learning. Here, we revisit this issue, testing an individual (L. S. J.) with severe MTL damage on four motor learning tasks and comparing her performance to age-matched controls. Consistent with previous findings in amnesics, we observed that L. S. J. could improve motor performance despite having significantly impaired declarative memory. However, she tended to perform poorly relative to age-matched controls, with deficits apparently related to flexible action selection. Further supporting an action selection deficit, L. S. J. fully failed to learn a task that required the acquisition of arbitrary action-outcome associations. We thus propose a modest revision to the classic taxonomic model: Although MTL-dependent memory processes are not necessary for some motor learning to occur, they play a significant role in the acquisition, implementation, and retrieval of action selection strategies. These findings have implications for our understanding of the neural correlates of motor learning, the psychological mechanisms of skill, and the theory of multiple memory systems.

Distinct Neural Signatures of Outcome Monitoring After Selection and Execution Errors.

Losing a point in tennis could result from poor shot selection or faulty stroke execution. To explore how the brain responds to these different types of errors, we examined feedback-locked EEG activity while participants completed a modified version of a standard three-armed bandit probabilistic reward task. Our task framed unrewarded outcomes as the result of either errors of selection or errors of execution. We examined whether amplitude of a medial frontal negativity (the feedback-related negativity [FRN]) was sensitive to the different forms of error attribution. Consistent with previous reports, selection errors elicited a large FRN relative to rewards, and amplitude of this signal correlated with behavioral adjustment after these errors. A different pattern was observed in response to execution errors. These outcomes produced a larger FRN, a frontocentral attenuation in activity preceding this component, and a subsequent enhanced error positivity in parietal sites. Notably, the only correlations with behavioral adjustment were with the early frontocentral attenuation and amplitude of the parietal signal; FRN differences between execution errors and rewarded trials did not correlate with subsequent changes in behavior. Our findings highlight distinct neural correlates of selection and execution error processing, providing insight into how the brain responds to the different classes of error that determine future action.

Implicit adaptation to mirror reversal is in the correct coordinate system but the wrong direction.

Learning in visuomotor adaptation tasks is the result of both explicit and implicit processes. Explicit processes, operationalized as reaiming an intended movement to a new goal, account for a significant proportion of learning. However, implicit processes, operationalized as error-dependent learning that gives rise to aftereffects, appear to be highly constrained. The limitations of implicit learning are highlighted in the mirror-reversal task, where implicit corrections act in opposition to performance. This is surprising given the mirror-reversal task has been viewed as emblematic of implicit learning. One potential issue not being considered in these studies is that both explicit and implicit processes were allowed to operate concurrently, which may interact, potentially in opposition. Therefore, we sought to further characterize implicit learning in a mirror-reversal task with a clamp design to isolate implicit learning from explicit strategies. We confirmed that implicit adaptation is in the wrong direction for mirror reversal and operates as if the perturbation were a rotation and only showed a moderate attenuation after 3 days of training. This result raised the question of whether implicit adaptation blindly operates as though perturbations were a rotation. In a separate experiment, which directly compared a mirror reversal and a rotation, we found that implicit adaptation operates in a proper coordinate system for different perturbations: adaptation to a mirror reversal and rotational perturbation is more consistent with Cartesian and polar coordinate systems, respectively. It remains an open question why implicit process would be flexible to the coordinate system of a perturbation but continue to be directed inappropriately.NEW & NOTEWORTHY Recent studies have found that implicit learning may operate inappropriately in some motor tasks, requiring explicit strategies to improve performance. However, this inappropriate adaptation could be attributable to competitive interactions between explicit and implicit processes. After isolating implicit processes, we found that implicit adaptation remained in the wrong direction for a mirror reversal, acting as if it were a rotation. Interestingly, however, the implicit system is sensitive to a particular coordinate system, treating mirror reversal and rotation differently.

Taking aim at the perceptual side of motor learning: exploring how explicit and implicit learning encode perceptual error information through depth vision.

Motor learning in visuomotor adaptation tasks results from both explicit and implicit processes, each responding differently to an error signal. Although the motor output side of these processes has been extensively studied, the visual input side is relatively unknown. We investigated if and how depth perception affects the computation of error information by explicit and implicit motor learning. Two groups of participants made reaching movements to bring a virtual cursor to a target in the frontoparallel plane. The Delayed group was allowed to reaim and their feedback was delayed to emphasize explicit learning, whereas the camped group received task-irrelevant clamped cursor feedback and continued to aim straight at the target to emphasize implicit adaptation. Both groups played this game in a highly detailed virtual environment (depth condition), leveraging a cover task of playing darts in a virtual tavern, and in an empty environment (no-depth condition). The delayed group showed an increase in error sensitivity under depth relative to no-depth. In contrast, the clamped group adapted to the same degree under both conditions. The movement kinematics of the delayed participants also changed under the depth condition, consistent with the target appearing more distant, unlike the Clamped group. A comparison of the delayed behavioral data with a perceptual task from the same individuals showed that the greater reaiming in the depth condition was consistent with an increase in the scaling of the error distance and size. These findings suggest that explicit and implicit learning processes may rely on different sources of perceptual information.NEW & NOTEWORTHY We leveraged a classic sensorimotor adaptation task to perform a first systematic assessment of the role of perceptual cues in the estimation of an error signal in the 3-D space during motor learning. We crossed two conditions presenting different amounts of depth information, with two manipulations emphasizing explicit and implicit learning processes. Explicit learning responded to the visual conditions, consistent with perceptual reports, whereas implicit learning appeared to be independent of them.

Direct and indirect cues can enable dual adaptation, but through different learning processes.

Switching between motor tasks requires accurate adjustments for changes in dynamics (grasping a cup) or sensorimotor transformations (moving a computer mouse). Dual-adaptation studies have investigated how learning of context-dependent dynamics or transformations is enabled by sensory cues. However, certain cues, such as color, have shown mixed results. We propose that these mixed results may arise from two major classes of cues: "direct" cues, which are part of the dynamic state and "indirect" cues, which are not. We hypothesized that explicit strategies would primarily account for the adaptation of an indirect color cue but would be limited to simple tasks, whereas a direct visual separation cue would allow implicit adaptation regardless of task complexity. To test this idea, we investigated the relative contribution of implicit and explicit learning in relation to contextual cue type (colored or visually shifted workspace) and task complexity (1 or 8 targets) in a dual-adaptation task. We found that the visual workspace location cue enabled adaptation across conditions primarily through implicit adaptation. In contrast, we found that the color cue was largely ineffective for dual adaptation, except in a small subset of participants who appeared to use explicit strategies. Our study suggests that the previously inconclusive role of color cues in dual adaptation may be explained by differential contribution of explicit strategies across conditions.NEW & NOTEWORTHY We present evidence that learning of context-dependent dynamics proceeds via different processes depending on the type of sensory cue used to signal the context. Visual workspace location enabled learning different dynamics implicitly, presumably because it directly enters the dynamic state estimate. In contrast, a color cue was only successful where learners were apparently able to leverage explicit strategies to account for changed dynamics. This suggests a unification for the previously inconclusive role of color cues.

Sensorimotor adaptation and cue reweighting compensate for distorted 3D shape information, accounting for paradoxical perception-action dissociations.

Visually guided movements can show surprising accuracy even when the perceived three-dimensional (3D) shape of the target is distorted. One explanation of this paradox is that an evolutionarily specialized "vision-for-action" system provides accurate shape estimates by relying selectively on stereo information and ignoring less reliable sources of shape information like texture and shading. However, the key support for this hypothesis has come from studies that analyze average behavior across many visuomotor interactions where available sensory feedback reinforces stereo information. The present study, which carefully accounts for the effects of feedback, shows that visuomotor interactions with slanted surfaces are actually planned using the same cue-combination function as slant perception and that apparent dissociations can arise due to two distinct supervised learning processes: sensorimotor adaptation and cue reweighting. In two experiments, we show that when a distorted slant cue biases perception (e.g., surfaces appear flattened by a fixed amount), sensorimotor adaptation rapidly adjusts the planned grip orientation to compensate for this constant error. However, when the distorted slant cue is unreliable, leading to variable errors across a set of objects (i.e., some slants are overestimated, others underestimated), then relative cue weights are gradually adjusted to reduce the misleading effect of the unreliable cue, consistent with previous perceptual studies of cue reweighting. The speed and flexibility of these two forms of learning provide an alternative explanation of why perception and action are sometimes found to be dissociated in experiments where some 3D shape cues are consistent with sensory feedback while others are faulty.NEW & NOTEWORTHY When interacting with three-dimensional (3D) objects, sensory feedback is available that could improve future performance via supervised learning. Here we confirm that natural visuomotor interactions lead to sensorimotor adaptation and cue reweighting, two distinct learning processes uniquely suited to resolve errors caused by biased and noisy 3D shape cues. These findings explain why perception and action are often found to be dissociated in experiments where some cues are consistent with sensory feedback while others are faulty.

Assessing explicit strategies in force field adaptation.

In recent years, it has become increasingly clear that a number of learning processes are at play in visuomotor adaptation tasks. In addition to implicitly adapting to a perturbation, learners can develop explicit knowledge allowing them to select better actions in responding to it. Advances in visuomotor rotation experiments have underscored the important role of such "explicit learning" in shaping adaptation to kinematic perturbations. Yet, in adaptation to dynamic perturbations, its contribution has been largely overlooked. We therefore sought to approach the assessment of explicit learning in adaptation to dynamic perturbations, by developing two novel modifications of a force field experiment. First, we asked learners to abandon any cognitive strategy before selected force channel trials to expose consciously accessible parts of overall learning. Here, learners indeed reduced compensatory force compared with standard Catch channels. Second, we instructed a group of learners to mimic their right hand's adaptation by moving with their naïve left hand. While a control group displayed negligible left hand force compensation, the mimicking group reported forces that approximated right hand adaptation but appeared to under-report the velocity component of the force field in favor of a more position-based component. Our results highlight the viability of explicit learning as a potential contributor to force field adaptation, though the fraction of learning under participants' deliberate control on average remained considerably smaller than that of implicit learning, despite task conditions favoring explicit learning. The methods we employed provide a starting point for investigating the contribution of explicit strategies to force field adaptation.NEW & NOTEWORTHY While the contribution of explicit learning has been increasingly studied in visuomotor adaptation, its contribution to force field adaptation has not been studied extensively. We employed two novel methods to assay explicit learning in a force field adaptation task and found that learners can voluntarily control aspects of compensatory force production and manually report it with their untrained limb. This supports the general viability of the contribution of explicit learning also in force field adaptation.

Can patients with cerebellar disease switch learning mechanisms to reduce their adaptation deficits?

Systematic perturbations in motor adaptation tasks are primarily countered by learning from sensory-prediction errors, with secondary contributions from other learning processes. Despite the availability of these additional processes, particularly the use of explicit re-aiming to counteract observed target errors, patients with cerebellar degeneration are surprisingly unable to compensate for their sensory-prediction error deficits by spontaneously switching to another learning mechanism. We hypothesized that if the nature of the task was changed-by allowing vision of the hand, which eliminates sensory-prediction errors-patients could be induced to preferentially adopt aiming strategies to solve visuomotor rotations. To test this, we first developed a novel visuomotor rotation paradigm that provides participants with vision of their hand in addition to the cursor, effectively setting the sensory-prediction error signal to zero. We demonstrated in younger healthy control subjects that this promotes a switch to strategic re-aiming based on target errors. We then showed that with vision of the hand, patients with cerebellar degeneration could also switch to an aiming strategy in response to visuomotor rotations, performing similarly to age-matched participants (older controls). Moreover, patients could retrieve their learned aiming solution after vision of the hand was removed (although they could not improve beyond what they retrieved), and retain it for at least 1 year. Both patients and older controls, however, exhibited impaired overall adaptation performance compared to younger healthy controls (age 18-33 years), likely due to age-related reductions in spatial and working memory. Patients also failed to generalize, i.e. they were unable to adopt analogous aiming strategies in response to novel rotations. Hence, there appears to be an inescapable obligatory dependence on sensory-prediction error-based learning-even when this system is impaired in patients with cerebellar disease. The persistence of sensory-prediction error-based learning effectively suppresses a switch to target error-based learning, which perhaps explains the unexpectedly poor performance by patients with cerebellar degeneration in visuomotor adaptation tasks.

Credit Assignment in a Motor Decision Making Task Is Influenced by Agency and Not Sensory Prediction Errors.

Failures to obtain reward can occur from errors in action selection or action execution. Recently, we observed marked differences in choice behavior when the failure to obtain a reward was attributed to errors in action execution compared with errors in action selection (McDougle et al., 2016). Specifically, participants appeared to solve this credit assignment problem by discounting outcomes in which the absence of reward was attributed to errors in action execution. Building on recent evidence indicating relatively direct communication between the cerebellum and basal ganglia, we hypothesized that cerebellar-dependent sensory prediction errors (SPEs), a signal indicating execution failure, could attenuate value updating within a basal ganglia-dependent reinforcement learning system. Here we compared the SPE hypothesis to an alternative, "top-down" hypothesis in which changes in choice behavior reflect participants' sense of agency. In two experiments with male and female human participants, we manipulated the strength of SPEs, along with the participants' sense of agency in the second experiment. The results showed that, whereas the strength of SPE had no effect on choice behavior, participants were much more likely to discount the absence of rewards under conditions in which they believed the reward outcome depended on their ability to produce accurate movements. These results provide strong evidence that SPEs do not directly influence reinforcement learning. Instead, a participant's sense of agency appears to play a significant role in modulating choice behavior when unexpected outcomes can arise from errors in action execution.SIGNIFICANCE STATEMENT When learning from the outcome of actions, the brain faces a credit assignment problem: Failures of reward can be attributed to poor choice selection or poor action execution. Here, we test a specific hypothesis that execution errors are implicitly signaled by cerebellar-based sensory prediction errors. We evaluate this hypothesis and compare it with a more "top-down" hypothesis in which the modulation of choice behavior from execution errors reflects participants' sense of agency. We find that sensory prediction errors have no significant effect on reinforcement learning. Instead, instructions influencing participants' belief of causal outcomes appear to be the main factor influencing their choice behavior.

Generalization via superposition: combined effects of mixed reference frame representations for explicit and implicit learning in a visuomotor adaptation task.

Studies on generalization of learned visuomotor perturbations have generally focused on whether learning is coded in extrinsic or intrinsic reference frames. This dichotomy, however, is challenged by recent findings showing that learning is represented in a mixed reference frame. Overlooked in this framework is how learning appears to consist of multiple processes, such as explicit reaiming and implicit motor adaptation. Therefore, the proposed mixed representation may simply reflect the superposition of explicit and implicit generalization functions, each represented in different reference frames. Here we characterized the individual generalization functions of explicit and implicit learning in relative isolation to determine whether their combination could predict the overall generalization function when both processes are in operation. We modified the form of feedback in a visuomotor rotation task in an attempt to isolate explicit and implicit learning and tested generalization across new limb postures to dissociate the extrinsic/intrinsic representations. We found that the amplitude of explicit generalization was reduced with postural change and was only marginally shifted, resembling an extrinsic representation. In contrast, implicit generalization maintained its amplitude but was significantly shifted, resembling a mixed representation. A linear combination of individual explicit and implicit generalization functions accounted for nearly 85% of the variance associated with the generalization function in a typical visuomotor rotation task, where both processes are in operation. This suggests that each form of learning results from a mixed representation with distinct extrinsic and intrinsic contributions and the combination of these features shapes the generalization pattern observed at novel limb postures. NEW & NOTEWORTHY Generalization following learning in visuomotor adaptation tasks can reflect how the brain represents what it learns. In this study, we isolated explicit and implicit forms of learning and showed that they are derived from a mixed reference frame representation with distinct extrinsic and intrinsic contributions. Furthermore, we showed that the overall generalization pattern at novel workspaces is due to the superposition of independent generalization effects developed by explicit and implicit learning processes.

Credit assignment in movement-dependent reinforcement learning.

When a person fails to obtain an expected reward from an object in the environment, they face a credit assignment problem: Did the absence of reward reflect an extrinsic property of the environment or an intrinsic error in motor execution? To explore this problem, we modified a popular decision-making task used in studies of reinforcement learning, the two-armed bandit task. We compared a version in which choices were indicated by key presses, the standard response in such tasks, to a version in which the choices were indicated by reaching movements, which affords execution failures. In the key press condition, participants exhibited a strong risk aversion bias; strikingly, this bias reversed in the reaching condition. This result can be explained by a reinforcement model wherein movement errors influence decision-making, either by gating reward prediction errors or by modifying an implicit representation of motor competence. Two further experiments support the gating hypothesis. First, we used a condition in which we provided visual cues indicative of movement errors but informed the participants that trial outcomes were independent of their actual movements. The main result was replicated, indicating that the gating process is independent of participants' explicit sense of control. Second, individuals with cerebellar degeneration failed to modulate their behavior between the key press and reach conditions, providing converging evidence of an implicit influence of movement error signals on reinforcement learning. These results provide a mechanistically tractable solution to the credit assignment problem.

Plan-based generalization shapes local implicit adaptation to opposing visuomotor transformations.

The human ability to use different tools demonstrates our capability of forming and maintaining multiple, context-specific motor memories. Experimentally, this has been investigated in dual adaptation, where participants adjust their reaching movements to opposing visuomotor transformations. Adaptation in these paradigms occurs by distinct processes, such as strategies for each transformation or the implicit acquisition of distinct visuomotor mappings. Although distinct, transformation-dependent aftereffects have been interpreted as support for the latter, they could reflect adaptation of a single visuomotor map, which is locally adjusted in different regions of the workspace. Indeed, recent studies suggest that explicit aiming strategies direct where in the workspace implicit adaptation occurs, thus potentially serving as a cue to enable dual adaptation. Disentangling these possibilities is critical to understanding how humans acquire and maintain motor memories for different skills and tools. We therefore investigated generalization of explicit and implicit adaptation to untrained movement directions after participants practiced two opposing cursor rotations, which were associated with the visual display being presented in the left or right half of the screen. Whereas participants learned to compensate for opposing rotations by explicit strategies specific to this visual workspace cue, aftereffects were not cue sensitive. Instead, aftereffects displayed bimodal generalization patterns that appeared to reflect locally limited learning of both transformations. By varying target arrangements and instructions, we show that these patterns are consistent with implicit adaptation that generalizes locally around movement plans associated with opposing visuomotor transformations. Our findings show that strategies can shape implicit adaptation in a complex manner. NEW & NOTEWORTHY Visuomotor dual adaptation experiments have identified contextual cues that enable learning of separate visuomotor mappings, but the underlying representations of learning are unclear. We report that visual workspace separation as a contextual cue enables the compensation of opposing cursor rotations by a combination of explicit and implicit processes: Learners developed context-dependent explicit aiming strategies, whereas an implicit visuomotor map represented dual adaptation independent from arbitrary context cues by local adaptation around the explicit movement plan.

Relative sensitivity of explicit reaiming and implicit motor adaptation.

It has become increasingly clear that learning in visuomotor rotation tasks, which induce an angular mismatch between movements of the hand and visual feedback, largely results from the combined effort of two distinct processes: implicit motor adaptation and explicit reaiming. However, it remains unclear how these two processes work together to produce trial-by-trial learning. Previous work has found that implicit motor adaptation operates automatically, regardless of task relevance, and saturates for large errors. In contrast, little is known about the automaticity of explicit reaiming and its sensitivity to error magnitude. Here we sought to characterize the automaticity and sensitivity function of these two processes to determine how they work together to facilitate performance in a visuomotor rotation task. We found that implicit adaptation scales relative to the visual error but only for small perturbations-replicating prior work. In contrast, explicit reaiming scales linearly for all tested perturbation sizes. Furthermore, the consistency of the perturbation appears to diminish both implicit adaptation and explicit reaiming, but to different degrees. Whereas implicit adaptation always displayed a response to the error, explicit reaiming was only engaged when errors displayed a minimal degree of consistency. This comports with the idea that implicit adaptation is obligatory and less flexible, whereas explicit reaiming is volitional and flexible. NEW & NOTEWORTHY This paper provides the first psychometric sensitivity function for explicit reaiming. Additionally, we show that the sensitivities of both implicit adaptation and explicit reaiming are influenced by consistency of errors. The pattern of results across two experiments further supports the idea that implicit adaptation is largely inflexible, whereas explicit reaiming is flexible and can be suppressed when unnecessary.

Characteristics of Implicit Sensorimotor Adaptation Revealed by Task-irrelevant Clamped Feedback.

Sensorimotor adaptation occurs when there is a discrepancy between the expected and actual sensory consequences of a movement. This learning can be precisely measured, but its source has been hard to pin down because standard adaptation tasks introduce two potential learning signals: task performance errors and sensory prediction errors. Here we employed a new method that induces sensory prediction errors without task performance errors. This method combines the use of clamped visual feedback that is angularly offset from the target and independent of the direction of motion, along with instructions to ignore this feedback while reaching to targets. Despite these instructions, participants unknowingly showed robust adaptation of their movements. This adaptation was similar to that observed with standard methods, showing sign dependence, local generalization, and cerebellar dependency. Surprisingly, adaptation rate and magnitude were invariant across a large range of offsets. Collectively, our results challenge current models of adaptation and demonstrate that behavior observed in many studies of adaptation reflect the composite effects of task performance and sensory prediction errors.

Implications of plan-based generalization in sensorimotor adaptation.

Generalization is a fundamental aspect of behavior, allowing for the transfer of knowledge from one context to another. The details of this transfer are thought to reveal how the brain represents what it learns. Generalization has been a central focus in studies of sensorimotor adaptation, and its pattern has been well characterized: Learning of new dynamic and kinematic transformations in one region of space tapers off in a Gaussian-like fashion to neighboring untrained regions, echoing tuned population codes in the brain. In contrast to common allusions to generalization in cognitive science, generalization in visually guided reaching is usually framed as a passive consequence of neural tuning functions rather than a cognitive feature of learning. While previous research has presumed that maximum generalization occurs at the instructed task goal or the actual movement direction, recent work suggests that maximum generalization may occur at the location of an explicitly accessible movement plan. Here we provide further support for plan-based generalization, formalize this theory in an updated model of adaptation, and test several unexpected implications of the model. First, we employ a generalization paradigm to parameterize the generalization function and ascertain its maximum point. We then apply the derived generalization function to our model and successfully simulate and fit the time course of implicit adaptation across three behavioral experiments. We find that dynamics predicted by plan-based generalization are borne out in the data, are contrary to what traditional models predict, and lead to surprising implications for the behavioral, computational, and neural characteristics of sensorimotor adaptation.NEW & NOTEWORTHY The pattern of generalization is thought to reveal how the motor system represents learned actions. Recent work has made the intriguing suggestion that maximum generalization in sensorimotor adaptation tasks occurs at the location of the learned movement plan. Here we support this interpretation, develop a novel model of motor adaptation that incorporates plan-based generalization, and use the model to successfully predict surprising dynamics in the time course of adaptation across several conditions.

Individual differences in implicit motor learning: task specificity in sensorimotor adaptation and sequence learning.

In standard taxonomies, motor skills are typically treated as representative of implicit or procedural memory. We examined two emblematic tasks of implicit motor learning, sensorimotor adaptation and sequence learning, asking whether individual differences in learning are correlated between these tasks, as well as how individual differences within each task are related to different performance variables. As a prerequisite, it was essential to establish the reliability of learning measures for each task. Participants were tested twice on a visuomotor adaptation task and on a sequence learning task, either the serial reaction time task or the alternating reaction time task. Learning was evident in all tasks at the group level and reliable at the individual level in visuomotor adaptation and the alternating reaction time task but not in the serial reaction time task. Performance variability was predictive of learning in both domains, yet the relationship was in the opposite direction for adaptation and sequence learning. For the former, faster learning was associated with lower variability, consistent with models of sensorimotor adaptation in which learning rates are sensitive to noise. For the latter, greater learning was associated with higher variability and slower reaction times, factors that may facilitate the spread of activation required to form predictive, sequential associations. Interestingly, learning measures of the different tasks were not correlated. Together, these results oppose a shared process for implicit learning in sensorimotor adaptation and sequence learning and provide insight into the factors that account for individual differences in learning within each task domain. NEW & NOTEWORTHY: We investigated individual differences in the ability to implicitly learn motor skills. As a prerequisite, we assessed whether individual differences were reliable across test sessions. We found that two commonly used tasks of implicit learning, visuomotor adaptation and the alternating serial reaction time task, exhibited good test-retest reliability in measures of learning and performance. However, the learning measures did not correlate between the two tasks, arguing against a shared process for implicit motor learning.

The cerebellum does more than sensory prediction error-based learning in sensorimotor adaptation tasks.

Individuals with damage to the cerebellum perform poorly in sensorimotor adaptation paradigms. This deficit has been attributed to impairment in sensory prediction error-based updating of an internal forward model, a form of implicit learning. These individuals can, however, successfully counter a perturbation when instructed with an explicit aiming strategy. This successful use of an instructed aiming strategy presents a paradox: In adaptation tasks, why do individuals with cerebellar damage not come up with an aiming solution on their own to compensate for their implicit learning deficit? To explore this question, we employed a variant of a visuomotor rotation task in which, before executing a movement on each trial, the participants verbally reported their intended aiming location. Compared with healthy control participants, participants with spinocerebellar ataxia displayed impairments in both implicit learning and aiming. This was observed when the visuomotor rotation was introduced abruptly (experiment 1) or gradually (experiment 2). This dual deficit does not appear to be related to the increased movement variance associated with ataxia: Healthy undergraduates showed little change in implicit learning or aiming when their movement feedback was artificially manipulated to produce similar levels of variability (experiment 3). Taken together the results indicate that a consequence of cerebellar dysfunction is not only impaired sensory prediction error-based learning but also a difficulty in developing and/or maintaining an aiming solution in response to a visuomotor perturbation. We suggest that this dual deficit can be explained by the cerebellum forming part of a network that learns and maintains action-outcome associations across trials.NEW & NOTEWORTHY Individuals with cerebellar pathology are impaired in sensorimotor adaptation. This deficit has been attributed to an impairment in error-based learning, specifically, from a deficit in using sensory prediction errors to update an internal model. Here we show that these individuals also have difficulty in discovering an aiming solution to overcome their adaptation deficit, suggesting a new role for the cerebellum in sensorimotor adaptation tasks.