scholarly journals Sensory prediction errors, not performance errors, update memories in visuomotor adaptation

2018 ◽  
Author(s):  
Kangwoo Lee ◽  
Youngmin Oh ◽  
Jun Izawa ◽  
Nicolas Schweighofer
Keyword(s):  
Visuomotor Adaptation ◽  
Motor Memory ◽  
Prediction Errors ◽  
Visuomotor Rotation ◽  
Main Target ◽  
Memory Decay ◽  
Performance Errors ◽  
Sensory Predictions ◽  
Sensory Prediction

AbstractSensory prediction errors are thought to update memories in motor 1 adaptation, but the role of performance errors is largely unknown. To dissociate these errors, we manipulated visual feedback during fast shooting movements under visuomotor rotation. Participants were instructed to strategically correct for performance errors by shooting to a neighboring target in one of four conditions: following the movement onset, the main target, the neighboring target, both targets, or none of the targets disappeared. Participants in all conditions experienced a drift away from the main target following the strategy. In conditions where the main target was shown, participants often tried to minimize performance errors caused by the drift by generating corrective movements. However, despite differences in performance during adaptation between conditions, memory decay in a delayed washout block was indistinguishable between conditions. Our results thus suggest that, in visuomotor adaptation, sensory predictions errors, but not performance errors, update the slow, temporally stable, component of motor memory.

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 .

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 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 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 Task errors contribute to implicit remapping in sensorimotor adaptation

2018 ◽  
Author(s):  
Li-Ann Leow ◽  
Welber Marinovic ◽  
Aymar de Rugy ◽  
Timothy J Carroll
Keyword(s):  
Sensory Feedback ◽  
Hand Position ◽  
Sensorimotor Adaptation ◽  
Prediction Errors ◽  
Reward Prediction ◽  
Strategic Processes ◽  
The Relationship ◽  
Sensory Prediction ◽  
Or Task

AbstractPerturbations of sensory feedback evoke sensory prediction errors (discrepancies between predicted and actual sensory outcomes of movements), and reward prediction errors (discrepancies between predicted rewards and actual rewards). Sensory prediction errors result in obligatory remapping of the relationship between motor commands and predicted sensory outcomes. The role of reward prediction errors in sensorimotor adaptation is less clear. When moving towards a target, we expect to obtain the reward of hitting the target, and so we experience a reward prediction error if the perturbation causes us to miss it. These discrepancies between desired task outcomes and actual task outcomes, or “task errors”, are thought to drive the use of strategic processes to restore success, although their role is not fully understood. Here, we investigated the role of task errors in sensorimotor adaptation: during target-reaching, we either removed task errors by moving the target mid-movement to align with cursor feedback of hand position, or enforced task error by moving the target away from the cursor feedback of hand position. Removing task errors not only reduced the rate and extent of adaptation during exposure to the perturbation, but also reduced the amount of post-adaptation implicit remapping. Hence, task errors contribute to implicit remapping resulting from sensory prediction errors. This suggests that the system which implicitly acquires new sensorimotor maps via exposure to sensory prediction errors is also sensitive to reward prediction errors.

scholarly journals Reduced transfer of visuomotor adaptation is associated with aberrant sense of agency in Schizophrenia

2018 ◽  
Author(s):  
Sonia Bansal ◽  
Karthik G Murthy ◽  
Justin Fitzgerald ◽  
Barbara L. Schwartz ◽  
Wilsaan M. Joiner
Keyword(s):  
Negative Symptoms ◽  
Motor Behavior ◽  
Visuomotor Adaptation ◽  
Sense Of Agency ◽  
Common Source ◽  
Prediction Errors ◽  
Movement Trajectories ◽  
Action Awareness ◽  
Before And After ◽  
Sensory Prediction

ABSTRACTOne deficit associated with schizophrenia (SZ) is the reduced ability to distinguish sensations resulting from self-caused actions from those due to external sources. This reduced sense of agency (SoA, awareness of ownership over self-generated actions) is hypothesized to result from a diminished utilization of internal monitoring signals of self-movement (i.e., efferent copy) which subsequently impairs forming and utilizing sensory prediction errors (differences between the predicted and actual sensory consequences resulting from movement). Here, we investigated the connections between clinical SZ symptoms and motor adaptation, a process that uses sensory prediction errors to update motor output. Schizophrenia patients (SZP, N=30) and non-psychiatric healthy control subjects (HC, N=31) adapted to altered movement visual feedback, and then applied the motor recalibration to untested contexts (i.e., the spatial generalization to untrained targets). Although adaptation was similar for SZP and controls, the extent of generalization was significantly less for SZP; movement trajectories made by patients to the furthest untrained target (135°) before and after adaptation were largely indistinguishable. Interestingly, deficits in the generalization were correlated to positive symptoms of psychosis (e.g., hallucinations), but not negative symptoms. Generalization was also associated with subjective measures of SoA across both SZP and HC, emphasizing the major role action awareness plays in motor behavior, and suggesting that tendencies to misattribute agency, even in HC, manifest in abnormal motor performance. We discuss the possible link of these findings to cerebellar circuit abnormalities that may be a common source for deficits in the utilization of sensory prediction errors and aberrant SoA.

scholarly journals Formation of a long-term memory for visuomotor adaptation following only a few trials of practice

2015 ◽  
Vol 114 (2) ◽  
pp. 969-977 ◽  
Author(s):  
David M. Huberdeau ◽  
Adrian M. Haith ◽  
John W. Krakauer
Keyword(s):  
Human Subjects ◽  
Motor Adaptation ◽  
Visuomotor Adaptation ◽  
Reaching Movements ◽  
Motor Memory ◽  
Long Term Memory ◽  
Visuomotor Rotation ◽  
Initial Exposure ◽  
Term Memory

The term savings refers to faster motor adaptation upon reexposure to a previously experienced perturbation, a phenomenon thought to reflect the existence of a long-term motor memory. It is commonly assumed that sustained practice during the first perturbation exposure is necessary to create this memory. Here we sought to test this assumption by determining the minimum amount of experience necessary during initial adaptation to a visuomotor rotation to bring about savings the following day. Four groups of human subjects experienced 2, 5, 10, or 40 trials of a counterclockwise 30° cursor rotation during reaching movements on one day and were retested the following day to assay for savings. Groups that experienced five trials or more of adaptation on day 1 showed clear savings on day 2. Subjects in all groups learned significantly more from the first rotation trial on day 2 than on day 1, but this learning rate advantage was maintained only in groups that had reached asymptote during the initial exposure. Additional experiments revealed that savings occurred when the magnitude, but not the direction, of the rotation differed across exposures, and when a 5-min break, rather than an overnight one, separated the first and second exposure. The overall pattern of savings we observe across conditions can be explained as rapid retrieval of the state of learning attained during the first exposure rather than as modulation of sensitivity to error. We conclude that a long-term memory for compensating for a perturbation can be rapidly acquired and rapidly retrieved.

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 The relationship between reinforcement and explicit strategies during visuomotor adaptation

2017 ◽  
Author(s):  
Olivier Codol ◽  
Peter J Holland ◽  
Joseph M Galea
Keyword(s):  
Prediction Error ◽  
Visuomotor Adaptation ◽  
Strategy Use ◽  
Asymptotic Performance ◽  
Preparation Time ◽  
Learning Success ◽  
Error Learning ◽  
The Relationship ◽  
Sensory Prediction

AbstractThe motor system’s ability to adapt to changes in the environment is essential for maintaining accurate movements. During such adaptation several distinct systems are recruited: cerebellar sensory-prediction error learning, success-based reinforcement, and explicit strategy-use. Although much work has focused on the relationship between cerebellar learning and strategy-use, there is little research regarding how reinforcement and strategy-use interact. To address this, participants first learnt a 20° visuomotor displacement. After reaching asymptotic performance, binary, hit-or-miss feedback (BF) was introduced either with or without visual feedback, the latter promoting reinforcement. Subsequently, retention was assessed using no-feedback trials, with half of the participants in each group being instructed to stop using any strategy. Although BF led to an increase in retention of the visuomotor displacement, instructing participants to remove their strategy nullified this effect, suggesting strategy-use is critical to BF-based reinforcement. In a second experiment, we prevented the expression or development of a strategy during BF performance, by either constraining participants to a short preparation time (expression) or by introducing the displacement gradually (development). As both strongly impaired BF performance, it suggests reinforcement requires both the development and expression of a strategy. These results emphasise a pivotal role of strategy-use during reinforcement-based motor learning.

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