scholarly journals Flexible explicit but rigid implicit learning in a visuomotor adaptation task

2015 ◽  
Vol 113 (10) ◽  
pp. 3836-3849 ◽  
Author(s):  
Krista M. Bond ◽  
Jordan A. Taylor
Keyword(s):  
Implicit Learning ◽  
Computational Models ◽  
Visuomotor Adaptation ◽  
Task Demands ◽  
Similar Degree ◽  
Explicit Learning ◽  
Prediction Errors ◽  
Visuomotor Rotation ◽  
Indirect Measures ◽  
Task Conditions

There is mounting evidence for the idea that performance in a visuomotor rotation task can be supported by both implicit and explicit forms of learning. The implicit component of learning has been well characterized in previous experiments and is thought to arise from the adaptation of an internal model driven by sensorimotor prediction errors. However, the role of explicit learning is less clear, and previous investigations aimed at characterizing the explicit component have relied on indirect measures such as dual-task manipulations, posttests, and descriptive computational models. To address this problem, we developed a new method for directly assaying explicit learning by having participants verbally report their intended aiming direction on each trial. While our previous research employing this method has demonstrated the possibility of measuring explicit learning over the course of training, it was only tested over a limited scope of manipulations common to visuomotor rotation tasks. In the present study, we sought to better characterize explicit and implicit learning over a wider range of task conditions. We tested how explicit and implicit learning change as a function of the specific visual landmarks used to probe explicit learning, the number of training targets, and the size of the rotation. We found that explicit learning was remarkably flexible, responding appropriately to task demands. In contrast, implicit learning was strikingly rigid, with each task condition producing a similar degree of implicit learning. These results suggest that explicit learning is a fundamental component of motor learning and has been overlooked or conflated in previous visuomotor tasks.

scholarly journals Effect of coordinate frame compatibility on the transfer of implicit and explicit learning across limbs

2016 ◽  
Vol 116 (3) ◽  
pp. 1239-1249 ◽  
Author(s):  
Eugene Poh ◽  
Timothy J. Carroll ◽  
Jordan A. Taylor
Keyword(s):  
Implicit Learning ◽  
Neural Representation ◽  
Coordinate Frame ◽  
Explicit Learning ◽  
Verbal Reports ◽  
Visuomotor Rotation ◽  
Left And Right ◽  
Task Conditions ◽  
Opposite Limb ◽  
Implicit And Explicit

Insights into the neural representation of motor learning can be obtained by investigating how learning transfers to novel task conditions. We recently demonstrated that visuomotor rotation learning transferred strongly between left and right limbs when the task was performed in a sagittal workspace, which afforded a consistent remapping for the two limbs in both extrinsic and joint-based coordinates. In contrast, transfer was absent when performed in horizontal workspace, where the extrinsically defined perturbation required conflicting joint-based remapping for the left and right limbs. Because visuomotor learning is thought to be supported by both implicit and explicit forms of learning, however, it is unclear to what extent these distinct forms of learning contribute to interlimb transfer. In this study, we assessed the degree to which interlimb transfer, following visuomotor rotation training, reflects explicit vs. implicit learning by obtaining verbal reports of participants' aiming direction before each movement. We also determined the extent to which these distinct components of learning are constrained by the compatibility of coordinate systems by comparing transfer between groups of participants who reached to targets arranged in the horizontal and sagittal planes. Both sagittal and horizontal conditions displayed complete transfer of explicit learning to the untrained limb. In contrast, transfer of implicit learning was incomplete, but the sagittal condition showed greater transfer than the horizontal condition. These findings suggest that explicit strategies developed with one limb can be fully implemented in the opposite limb, whereas implicit transfer depends on the degree to which new sensorimotor maps are spatially compatible for the two limbs.

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

Brain ◽  
2019 ◽  
Vol 142 (3) ◽  
pp. 662-673 ◽  
Author(s):  
Aaron L Wong ◽  
Cherie L Marvel ◽  
Jordan A Taylor ◽  
John W Krakauer
Keyword(s):  
Prediction Error ◽  
Poor Performance ◽  
Visuomotor Adaptation ◽  
Cerebellar Degeneration ◽  
Prediction Errors ◽  
Cerebellar Disease ◽  
Learning Mechanisms ◽  
Visuomotor Rotation ◽  
Age Related ◽  
Sensory Prediction

Abstract 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.

scholarly journals A locomotor learning paradigm using distorted visual feedback elicits strategic learning

2018 ◽  
Vol 120 (4) ◽  
pp. 1923-1931 ◽  
Author(s):  
Margaret A. French ◽  
Susanne M. Morton ◽  
Charalambos C. Charalambous ◽  
Darcy S. Reisman
Keyword(s):  
Upper Extremity ◽  
Implicit Learning ◽  
Visual Feedback ◽  
Explicit Learning ◽  
Strategic Learning ◽  
Overground Walking ◽  
Visuomotor Rotation ◽  
Small Component ◽  
Walking Pattern ◽  
Do So

Distorted visual feedback (DVF) during locomotion has been suggested to result in the development of a new walking pattern in healthy individuals through implicit learning processes. Recent work in upper extremity visuomotor rotation paradigms suggest that these paradigms involve implicit and explicit learning. Additionally, in upper extremity visuomotor paradigms, the verbal cues provided appear to impact how a behavior is learned and when this learned behavior is used. Here, in two experiments in neurologically intact individuals, we tested how verbal instruction impacts learning a new locomotor pattern on a treadmill through DVF, the transfer of that pattern to overground walking, and what types of learning occur (i.e., implicit vs. explicit learning). In experiment 1, we found that the instructions provided impacted the amount learned through DVF, but not the size of the aftereffects or the amount of the pattern transferred to overground walking. Additionally, the aftereffects observed were significantly different from the baseline walking pattern, but smaller than the behavior changes observed during learning, which is uncharacteristic of implicit sensorimotor adaptation. Thus, experiment 2 aimed to determine the cause of these discrepancies. In this experiment, when VF was not provided, individuals continued using the learned walking pattern when instructed to do so and returned toward their baseline pattern when instructed to do so. Based on these results, we conclude that DVF during locomotion results in a large portion of explicit learning and a small portion of implicit learning. NEW & NOTEWORTHY The results of this study suggest that distorted visual feedback during locomotor learning involves the development of an explicit strategy with only a small component of implicit learning. This is important because previous studies using distorted visual feedback have suggested that locomotor learning relies primarily on implicit learning. This paradigm, therefore, provides a new way to examine a different form of learning in locomotion.

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

2018 ◽  
Author(s):  
Aaron L. Wong ◽  
Cherie L. Marvel ◽  
Jordan A. Taylor ◽  
John W. Krakauer
Keyword(s):  
Spinocerebellar Ataxia ◽  
Prediction Error ◽  
Visuomotor Adaptation ◽  
Cerebellar Degeneration ◽  
Prediction Errors ◽  
Healthy Controls ◽  
Learning Mechanisms ◽  
Visuomotor Rotation ◽  
Age Related ◽  
Sensory Prediction

ABSTRACTSystematic 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 controls that this promotes a switch to strategic re-aiming based on target errors. We then showed that with vision of the hand, patients with spinocerebellar ataxia 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, and retain it for at least one year. Both patients and older controls, however, exhibited impaired overall adaptation performance compared to younger healthy controls (age, 18-33), likely due to age-related reductions in spatial and working memory. Moreover, patients failed to generalize, i.e., they were unable to adopt analogous aiming strategies in response to novel rotations, nor could they further improve their performance without vision of the hand. 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 degeneration. 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 spinocerebellar ataxia in visuomotor adaptation tasks.

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

2019 ◽  
Vol 121 (5) ◽  
pp. 1953-1966 ◽  
Author(s):  
Eugene Poh ◽  
Jordan A. Taylor
Keyword(s):  
Implicit Learning ◽  
Reference Frame ◽  
Reference Frames ◽  
Visuomotor Adaptation ◽  
Visuomotor Rotation ◽  
Mixed Representation ◽  
Multiple Processes ◽  
Implicit Motor ◽  
The Individual ◽  
The Brain

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.

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

2019 ◽  
Vol 122 (3) ◽  
pp. 1050-1059 ◽  
Author(s):  
David M. Huberdeau ◽  
John W. Krakauer ◽  
Adrian M. Haith
Keyword(s):  
Qualitative Change ◽  
Visuomotor Adaptation ◽  
Skill Learning ◽  
Memory Representation ◽  
Prediction Errors ◽  
Visuomotor Rotation ◽  
Repeated Practice ◽  
Target Locations ◽  
Sensory Prediction ◽  
Automatic Action

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.

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

2021 ◽  
Author(s):  
Elinor Tzvi ◽  
Sebastian Loens ◽  
Opher Donchin
Keyword(s):  
Premotor Cortex ◽  
Motor Program ◽  
Visuomotor Adaptation ◽  
Prediction Errors ◽  
Visuomotor Rotation ◽  
Non Invasive ◽  
Behavioral Studies ◽  
Sensory Prediction ◽  
The Brain

AbstractThe 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 .

Differential motor learning via reward and punishment

2019 ◽  
Vol 73 (2) ◽  
pp. 249-259 ◽  
Author(s):  
Yanlong Song ◽  
Siyuan Lu ◽  
Ann L Smiley-Oyen
Keyword(s):  
Loss Aversion ◽  
Visual Target ◽  
Visuomotor Adaptation ◽  
Explicit Learning ◽  
Prediction Errors ◽  
Model Free ◽  
Explicit Processes ◽  
Multiple Processes ◽  
Sensory Prediction ◽  
Reward And Punishment

Visuomotor adaptation involves multiple processes such as explicit learning, implicit learning from sensory prediction errors, and model-free mechanisms like use-dependent plasticity. Recent findings show that reward and punishment differently affect visuomotor adaptation. This study examined whether punishment and reward had distinct effects on explicit learning. When participants practised adapting to a large, abrupt visual rotation during reaching for a virtual visual target, visual feedback of the cursor was not provided. Only performance-based scalar reward or punishment feedback (money gained or lost) was used, thereby emphasising explicit processes during adaptation. The results revealed that punishment, compared with reward, induced faster adaptation and greater variability of reaching in the initial phase of adaptation. We interpret these findings as reflecting enhanced explicit learning, likely due to loss aversion.

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

2017 ◽  
Author(s):  
Peter A. Butcher ◽  
Richard B. Ivry ◽  
Sheng-Han Kuo ◽  
David Rydz ◽  
John W. Krakauer ◽  
...  
Keyword(s):  
Implicit Learning ◽  
Prediction Error ◽  
Internal Model ◽  
Sensorimotor Adaptation ◽  
Prediction Errors ◽  
Cerebellar Dysfunction ◽  
Visuomotor Rotation ◽  
Cerebellar Damage ◽  
Internal Forward Model ◽  
Sensory Prediction

AbstractIndividuals 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 don’t individuals with cerebellar damage 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, prior to executing a movement on each trial, the participants verbally reported their intended aiming location. Compared to healthy controls, participants with spinocerebellar ataxia (SCA) displayed impairments in both implicit learning and aiming. This was observed when the visuomotor rotation was introduced abruptly (Exp. 1) or gradually (Exp. 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 (Exp. 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 and noteworthyIndividuals 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.

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

2018 ◽  
Author(s):  
Eugene Poh ◽  
Jordan A. Taylor
Keyword(s):  
Implicit Learning ◽  
Reference Frame ◽  
Reference Frames ◽  
Visuomotor Adaptation ◽  
Visuomotor Rotation ◽  
Mixed Representation ◽  
Postural Changes ◽  
Multiple Processes ◽  
Implicit Motor ◽  
The Individual

AbstractStudies on generalization of learned visuomotor perturbations has 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 is the result of multiple processes, such as explicit re-aiming 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 if 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 to isolate explicit and implicit learning, and tested generalization across different limb postures to dissociate the extrinsic and intrinsic representations. We found that explicit generalization occurred predominantly in an extrinsic reference frame but the amplitude was reduced with postural changes, whereas implicit generalization was phase-shifted according to a mixed reference frame representation and amplitude was maintained. 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 shape the generalization pattern observed at novel limb postures.New and noteworthyGeneralization 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.

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