scholarly journals Residual errors in visuomotor adaptation persist despite extended motor preparation periods

2021 ◽  
Author(s):  
Matthew Weightman ◽  
John-Stuart Brittain ◽  
R.Chris Miall ◽  
Ned Jenkinson

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.

Author(s):  
Lisa Langsdorf ◽  
Jana Maresch ◽  
Mathias Hegele ◽  
Samuel D. McDougle ◽  
Raphael Schween

AbstractOne persistent curiosity in visuomotor adaptation tasks is that participants often do not reach maximal performance. This incomplete asymptote has been explained as a consequence of obligatory computations within the implicit adaptation system, such as an equilibrium between learning and forgetting. A body of recent work has shown that in standard adaptation tasks, cognitive strategies operate alongside implicit learning. We reasoned that incomplete learning in adaptation tasks may primarily reflect a speed-accuracy tradeoff on time-consuming motor planning. Across three experiments, we find evidence supporting this hypothesis, showing that hastened motor planning may primarily lead to under-compensation. When an obligatory waiting period was administered before movement start, participants were able to fully counteract imposed perturbations (Experiment 1). Inserting the same delay between trials – rather than during movement planning – did not induce full compensation, suggesting that the motor planning interval influences the learning asymptote (Experiment 2). In the last experiment (Experiment 3), we asked participants to continuously report their movement intent. We show that emphasizing explicit re-aiming strategies (and concomitantly increasing planning time) also lead to complete asymptotic learning. Findings from all experiments support the hypothesis that incomplete adaptation is, in part, the result of an intrinsic speed-accuracy tradeoff, perhaps related to cognitive strategies that require parametric attentional reorienting from the visual target to the goal.


Author(s):  
Lisa Langsdorf ◽  
Jana Maresch ◽  
Mathias Hegele ◽  
Samuel D. McDougle ◽  
Raphael Schween

AbstractOne persistent curiosity in visuomotor adaptation tasks is that participants often do not reach maximal performance. This incomplete asymptote has been explained as a consequence of obligatory computations within the implicit adaptation system, such as an equilibrium between learning and forgetting. A body of recent work has shown that in standard adaptation tasks, cognitive strategies operate alongside implicit learning. We reasoned that incomplete learning in adaptation tasks may primarily reflect a speed-accuracy trade-off on time-consuming motor planning. Across three experiments, we find evidence supporting this hypothesis, showing that hastened motor planning may primarily lead to under-compensation. When an obligatory waiting period was administered before movement start, participants were able to fully counteract imposed perturbations (experiment 1). Inserting the same delay between trials - rather than during movement planning - did not induce full compensation, suggesting that the motor planning interval predicts the learning asymptote (experiment 2). In the last experiment, we asked participants to continuously report their movement intent. We show that emphasizing explicit re-aiming strategies (and concomitantly increasing planning time) also lead to complete asymptotic learning. Findings from all experiments support the hypothesis that incomplete adaptation is, in part, the result of an intrinsic speed-accuracy trade-off, perhaps related to cognitive strategies that require parametric attentional reorienting from the visual target to the goal.


2009 ◽  
Vol 102 (5) ◽  
pp. 2790-2799 ◽  
Author(s):  
Jinsung Wang ◽  
Robert L. Sainburg

A long history of behavioral and physiological research has suggested that bilateral coordination invokes unique neural processes that are not involved in unilateral movements. This hypothesis predicts that motor learning should show limited transfer between unilateral and bilateral conditions, which is consistent with a recent finding that indicated partial, but not complete, transfer of learning between the two conditions. However, during learning of new motor skills, transformations must also be made between visual and proprioceptive coordinate systems, a process that may occur upstream to the processes that differentiate bilateral from unilateral movements. We now investigate whether visuomotor adaptations are shared between unilateral and bilateral movement conditions. Our results indicate substantial transfer from bilateral to subsequent unilateral conditions for both arms. Interestingly, whereas the nondominant arm never showed complete adaptation to visual rotation under bilateral conditions, this interference, or lack of improvement, in bilateral performance did not disturb the visuomotor adaptation process or transfer, as reflected by superb unilateral performances immediately following the bilateral conditions. These findings unambiguously indicate that visuomotor adaptation can extensively generalize between bilateral and unilateral conditions, thus suggesting a substantial overlap in the neural processes underlying visuomotor transformations between the two movement conditions. Our findings provide support for a two-stage model of motor planning, in which the visuomotor transformation process precedes the processes that convert the visuomotor plan into effector-specific commands that incorporate bilateral synergies and that result in the forces that determine motion.


2021 ◽  
Author(s):  
Milou J.L. van Helvert ◽  
Leonie Oostwoud Wijdenes ◽  
Linda Geerligs ◽  
W. Pieter Medendorp

AbstractWhile beta-band activity during motor planning is known to be modulated by uncertainty about where to act, less is known about its modulations to uncertainty about how to act. To investigate this issue, we recorded oscillatory brain activity with EEG while human participants (n = 17) performed a hand choice reaching task. The reaching hand was either predetermined or of participants’ choice, and the target was close to one of the two hands or at about equal distance from both. To measure neural activity in a motion-artifact-free time window, the location of the upcoming target was cued 1000-1500 ms before the presentation of the target, whereby the cue was valid in 50% of trials. As evidence for motor planning during the cueing phase, behavioral observations showed that the cue affected later hand choice. Furthermore, reaction times were longer in the choice than in the predetermined trials, supporting the notion of a competitive process for hand selection. Modulations of beta-band power over central cortical regions, but not alpha-band or theta-band power, were in line with these observations. During the cueing period, reaches in predetermined trials were preceded by larger decreases in beta-band power than reaches in choice trials. Cue direction did not affect reaction times or beta-band power, which may be due to the cue being invalid in 50% of trials, retaining effector uncertainty during motor planning. Our findings suggest that effector uncertainty, similar to target uncertainty, selectively modulates beta-band power during motor planning.New & NoteworthyWhile reach-related beta-band power in central cortical areas is known to modulate with the number of potential targets, here we show, using a cueing paradigm, that the power in this frequency band, but not in the alpha or theta-band, is also modulated by the uncertainty of which hand to use. This finding supports the notion that multiple possible effector-specific actions can be specified in parallel up to the level of motor preparation.


2009 ◽  
Vol 101 (5) ◽  
pp. 2263-2269 ◽  
Author(s):  
Aymar de Rugy ◽  
Mark R. Hinder ◽  
Daniel G. Woolley ◽  
Richard G. Carson

Reaching to visual targets engages the nervous system in a series of transformations between sensory information and motor commands. That which remains to be determined is the extent to which the processes that mediate sensorimotor adaptation to novel environments engage neural circuits that represent the required movement in joint-based or muscle-based coordinate systems. We sought to establish the contribution of these alternative representations to the process of visuomotor adaptation. To do so we applied a visuomotor rotation during a center-out isometric torque production task that involved flexion/extension and supination/pronation at the elbow-joint complex. In separate sessions, distinct half-quadrant rotations (i.e., 45°) were applied such that adaptation could be achieved either by only rescaling the individual joint torques (i.e., the visual target and torque target remained in the same quadrant) or by additionally requiring torque reversal at a contributing joint (i.e., the visual target and torque target were in different quadrants). Analysis of the time course of directional errors revealed that the degree of adaptation was lower (by ∼20%) when reversals in the direction of joint torques were required. It has been established previously that in this task space, a transition between supination and pronation requires the engagement of a different set of muscle synergists, whereas in a transition between flexion and extension no such change is required. The additional observation that the initial level of adaptation was lower and the subsequent aftereffects were smaller, for trials that involved a pronation–supination transition than for those that involved a flexion–extension transition, supports the conclusion that the process of adaptation engaged, at least in part, neural circuits that represent the required motor output in a muscle-based coordinate system.


Brain ◽  
2019 ◽  
Vol 142 (3) ◽  
pp. 662-673 ◽  
Author(s):  
Aaron L Wong ◽  
Cherie L Marvel ◽  
Jordan A Taylor ◽  
John W Krakauer

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.


2011 ◽  
Vol 106 (6) ◽  
pp. 3157-3172 ◽  
Author(s):  
Jordan A. Taylor ◽  
Greg J. Wojaczynski ◽  
Richard B. Ivry

Studies of intermanual transfer have been used to probe representations formed during skill acquisition. We employ a new method that provides a continuous assay of intermanual transfer, intermixing right- and left-hand trials while limiting visual feedback to right-hand movements. We manipulated the degree of awareness of the visuomotor rotation, introducing a 22.5° perturbation in either an abrupt single step or gradually in ∼1° increments every 10 trials. Intermanual transfer was observed with the direction of left-hand movements shifting in the opposite direction of the rotation over the course of training. The transfer on left-hand trials was less than that observed in the right hand. Moreover, the magnitude of transfer was larger in our mixed-limb design compared with the standard blocked design in which transfer is only probed at the end of training. Transfer was similar in the abrupt and gradual groups, suggesting that awareness of the perturbation has little effect on intermanual transfer. In a final experiment, participants were provided with a strategy to offset an abrupt rotation, a method that has been shown to increase error over the course of training due to the operation of sensorimotor adaptation. This deterioration was also observed on left-hand probe trials, providing further support that awareness has little effect on intermanual transfer. These results indicate that intermanual transfer is not dependent on the implementation of cognitively assisted strategies that participants might adopt when they become aware that the visuomotor mapping has been perturbed. Rather, the results indicate that the information available to processes involved in adaptation entails some degree of effector independence.


Neuroreport ◽  
2019 ◽  
Vol 30 (12) ◽  
pp. 856-862
Author(s):  
Makoto Suzuki ◽  
Takako Suzuki ◽  
Satoshi Tanaka ◽  
Kazuhiro Sugawara ◽  
Toyohiro Hamaguchi

2008 ◽  
Vol 100 (5) ◽  
pp. 2537-2548 ◽  
Author(s):  
Eric Zarahn ◽  
Gregory D. Weston ◽  
Johnny Liang ◽  
Pietro Mazzoni ◽  
John W. Krakauer

Adaptation of the motor system to sensorimotor perturbations is a type of learning relevant for tool use and coping with an ever-changing body. Memory for motor adaptation can take the form of savings: an increase in the apparent rate constant of readaptation compared with that of initial adaptation. The assessment of savings is simplified if the sensory errors a subject experiences at the beginning of initial adaptation and the beginning of readaptation are the same. This can be accomplished by introducing either 1) a sufficiently small number of counterperturbation trials (counterperturbation paradigm [ CP]) or 2) a sufficiently large number of zero-perturbation trials (washout paradigm [ WO]) between initial adaptation and readaptation. A two-rate, linear time-invariant state-space model (SSMLTI,2) was recently shown to theoretically produce savings for CP. However, we reasoned from superposition that this model would be unable to explain savings for WO. Using the same task (planar reaching) and type of perturbation (visuomotor rotation), we found comparable savings for both CP and WO paradigms. Although SSMLTI,2 explained some degree of savings for CP it failed completely for WO. We conclude that for visuomotor rotation, savings in general is not simply a consequence of LTI dynamics. Instead savings for visuomotor rotation involves metalearning, which we show can be modeled as changes in system parameters across the phases of an adaptation experiment.


2009 ◽  
Vol 65 ◽  
pp. S104
Author(s):  
Yu Shimizu ◽  
Hiroshi Imamizu ◽  
Masaaki Sato ◽  
Mitsuo Kawato

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