Individual Differences in Sensorimotor Adaptation Are Conserved Over Time and Across Force-Field Tasks

Sensorimotor adaptation enables the nervous system to modify actions for different conditions and environments. Many studies have investigated factors that influence adaptation at the group level. There is growing recognition that individuals vary in their ability to adapt motor skills and that a better understanding of individual differences in adaptation may inform how motor skills are taught and rehabilitated. Here we examined individual differences in the adaptation of upper-limb reaching movements. We quantified the extent to which participants adapted their movements to a velocity-dependent force field during an initial session, at 24 h, and again 1-week later. Participants (n = 28) displayed savings, which was expressed as greater initial adaptation when re-exposed to the force field. Individual differences in adaptation across various stages of the experiment displayed weak-strong reliability, such that individuals who adapted to a greater extent in the initial session tended to do so when re-exposed to the force field. Our second experiment investigated if individual differences in adaptation are also present when participants adapt to different force fields or a force field and visuomotor rotation. Separate groups of participants adapted to position- and velocity-dependent force fields (Experiment 2a; n = 20) or a velocity-dependent force field and visuomotor rotation in a single session (Experiment 2b; n = 20). Participants who adapted to a greater extent to velocity-dependent forces tended to show a greater extent of adaptation when exposed to position-dependent forces. In contrast, correlations were weak between various stages of adaptation to the force-field and visuomotor rotation. Collectively, our study reveals individual differences in adaptation that are reliable across repeated exposure to the same force field and present when adapting to different force fields.

Sensitivity to error during visuomotor adaptation is similarly modulated by abrupt, gradual and random perturbation schedules

It has been suggested that sensorimotor adaptation involves at least two processes (i.e., fast and slow) that differ in retention and error sensitivity. Previous work has shown that repeated exposure to an abrupt force field perturbation results in greater error sensitivity for both the fast and slow processes. While this implies that the faster relearning is associated with increased error sensitivity, it remains unclear what aspects of prior experience modulate error sensitivity. In the present study, we manipulated the initial training using different perturbation schedules, thought to differentially affect fast and slow learning processes based on error magnitude, and then observed what effect prior learning had on subsequent adaptation. During initial training of a visuomotor rotation task, we exposed three groups of participants to either an abrupt, a gradual, or a random perturbation schedule. During a testing session, all three groups were subsequently exposed to an abrupt perturbation schedule. Comparing the two sessions of the control group who experienced repetition of the same perturbation, we found an increased error sensitivity for both processes. We found that the error sensitivity was increased for both the fast and slow processes, with no reliable changes in the retention, for both the gradual and structural learning groups when compared to the first session of the control group. We discuss the findings in the context of how fast and slow learning processes respond to a history of errors.

Sensorimotor knowledge from task-irrelevant feedback contributes to motor learning

Exposure to task-irrelevant feedback leads to perceptual learning, but its effect on motor learning has been understudied. Here we asked human participants to reach a visual target with a hand-controlled cursor while observing another cursor moving independently in a different direction. While the task-irrelevant feedback did not change the main task's performance, it elicited robust savings in subsequent adaptation to classical visuomotor rotation perturbation. We demonstrated that the saving effect resulted from a faster formation of strategic learning through a series of experiments, not from gains in the implicit learning process. Furthermore, the saving effect was robust against drastic changes in stimulus features (i.e., rotation size or direction) or task types (i.e., for motor adaptation and skill learning). However, the effect was absent when the task-irrelevant feedback did not carry the visuomotor relationship embedded in visuomotor rotation. Thus, though previous research on perceptual learning has related task-irrelevant feedback to changes in early sensory processes, our findings support its role in acquiring abstract sensorimotor knowledge during motor learning. Motor learning studies have traditionally focused on task-relevant feedback, but our study extends the scope of feedback processes and sheds new light on the dichotomy of explicit and implicit learning in motor adaptation as well as motor structure learning.

Residual errors in visuomotor adaptation persist despite extended motor preparation periods

A consistent finding in sensorimotor adaptation is a persistent undershoot of full compensation, such that performance asymptotes with residual errors greater than seen at baseline. This behaviour has been attributed to limiting factors within the implicit adaptation system, which reaches a sub-optimal equilibrium between trial-by-trial learning and forgetting. However, recent research has suggested that allowing longer motor planning periods prior to movement eliminates these residual errors. The additional planning time allows required cognitive processes to be completed before movement onset, thus increasing accuracy. Here we looked to extend these findings by investigating the relationship between increased motor preparation time and the size of imposed visuomotor rotation (30°, 45° or 60°), with regards to the final asymptotic level of adaptation. We found that restricting preparation time to 0.35 seconds impaired adaptation for moderate and larger rotations, resulting in larger residual errors compared to groups with additional preparation time. However, we found that even extended preparation time failed to eliminate persistent errors, regardless of magnitude of cursor rotation. Thus, the asymptote of adaptation was significantly less than the degree of imposed rotation, for all experimental groups. Additionally, there was a positive relationship between asymptotic error and implicit retention. These data suggest that a prolonged motor preparation period is insufficient to reliably achieve complete adaptation and therefore our results provide support for the proposal that the balance between error-based learning and forgetting (i.e., incomplete retention) contributes to asymptotic adaptation levels.

Sensitivity to Error During Visuomotor Adaptation is Similarly Modulated by Abrupt, Gradual and Random Perturbation Schedules

It has been suggested that sensorimotor adaptation involves at least two processes (i.e., fast and slow) that differ in retention and error sensitivity. Previous work has shown that repeated exposure to an abrupt force field perturbation results in greater error sensitivity for both the fast and slow processes. While this implies that the faster relearning is associated with increased error sensitivity, it remains unclear what aspects of prior experience modulate error sensitivity. In the present study, we manipulated the initial training using different perturbation schedules, thought to differentially affect fast and slow learning processes based on error magnitude, and then observed what effect prior learning had on subsequent adaptation. During initial training of a visuomotor rotation task, we exposed three groups of participants to either an abrupt, a gradual, or a random perturbation schedule. During a testing session, all three groups were subsequently exposed to an abrupt perturbation schedule. Comparing the two sessions of the control group who experienced repetition of the same perturbation, we found an increased error sensitivity for both processes. We found that the error sensitivity was increased for both the fast and slow processes, with no reliable changes in the retention, for both the gradual and structural learning groups when compared to the first session of the control group. We discuss the findings in the context of how fast and slow learning processes respond to a history of errors.

Validating model-based Bayesian integration using prior–cost metamers

There are two competing views on how humans make decisions under uncertainty. Bayesian decision theory posits that humans optimize their behavior by establishing and integrating internal models of past sensory experiences (priors) and decision outcomes (cost functions). An alternative hypothesis posits that decisions are optimized through trial and error without explicit internal models for priors and cost functions. To distinguish between these possibilities, we introduce a paradigm that probes the sensitivity of humans to transitions between prior–cost pairs that demand the same optimal policy (metamers) but distinct internal models. We demonstrate the utility of our approach in two experiments that were classically explained by Bayesian theory. Our approach validates the Bayesian learning strategy in an interval timing task but not in a visuomotor rotation task. More generally, our work provides a domain-general approach for testing the circumstances under which humans explicitly implement model-based Bayesian computations.

Mini-review: The Role of the Cerebellum in Visuomotor Adaptation

The incredible capability of the brain to quickly alter performance in response to ever-changing environment is rooted in the process of adaptation. The core aspect of adaptation is to fit an existing motor program to altered conditions. Adaptation to a visuomotor rotation or an external force has been well established as tools to study the mechanisms underlying sensorimotor adaptation. In this mini-review, we summarize recent findings from the field of visuomotor adaptation. We focus on the idea that the cerebellum plays a central role in the process of visuomotor adaptation and that interactions with cortical structures, in particular, the premotor cortex and the parietal cortex, may be crucial for this process. To this end, we cover a range of methodologies used in the literature that link cerebellar functions and visuomotor adaptation; behavioral studies in cerebellar lesion patients, neuroimaging and non-invasive stimulation approaches. The mini-review is organized as follows: first, we provide evidence that sensory prediction errors (SPE) in visuomotor adaptation rely on the cerebellum based on behavioral studies in cerebellar patients. Second, we summarize structural and functional imaging studies that provide insight into spatial localization as well as visuomotor adaptation dynamics in the cerebellum. Third, we discuss premotor — cerebellar interactions and how these may underlie visuomotor adaptation. And finally, we provide evidence from transcranial direct current and magnetic stimulation studies that link cerebellar activity, beyond correlational relationships, to visuomotor adaptation .

A conversion from slow to fast memory in response to passive motion

When the same perturbation is experienced consecutively, learning is accelerated on the second attempt. This savings is a central property of sensorimotor adaptation. Current models suggest that these improvements in learning are due to changes in the brain’s sensitivity to error. Here, we tested whether these increases in error sensitivity could be facilitated by passive movement experiences. In each experimental group, the robot moved the arm passively in the direction that solved the upcoming rotation, but no visual feedback was provided. Then, following a break in time, participants adapted to a visuomotor rotation. Prior passive movements substantially improved motor learning, increasing total compensation in each group by approximately 30%. Similar to savings, a state-space model suggested that this improvement in learning was due to an increase in error sensitivity, but not memory retention. Thus, passive memories appeared to increase the motor learning system’s sensitivity to error. However, some features in the observed behavior were not captured by this model, nor by similar empirical models, which assumed that learning was due a single exponential process. When we considered the possibility that learning was supported by parallel fast and slow adaptive processes, a striking pattern emerged; whereas initial improvements in learning were driven by a slower adaptive state, increases in error sensitivity gradually transferred to a faster learning system with the passage of time.