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      Contribution of explicit processes to reinforcement-based motor learning

      1 , 1 , 1
      Journal of Neurophysiology
      American Physiological Society

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          Abstract

          <p class="first" id="d713367e154">Despite increasing interest in the role of reward in motor learning, the underlying mechanisms remain ill defined. In particular, the contribution of explicit processes to reward-based motor learning is unclear. To address this, we examined subjects’ ( <i>n</i> = 30) ability to learn to compensate for a gradually introduced 25° visuomotor rotation with only reward-based feedback (binary success/failure). Only two-thirds of subjects ( <i>n</i> = 20) were successful at the maximum angle. The remaining subjects initially followed the rotation but after a variable number of trials began to reach at an insufficiently large angle and subsequently returned to near-baseline performance ( <i>n</i> = 10). Furthermore, those who were successful accomplished this via a large explicit component, evidenced by a reduction in reach angle when they were asked to remove any strategy they employed. However, both groups displayed a small degree of remaining retention even after the removal of this explicit component. All subjects made greater and more variable changes in reach angle after incorrect (unrewarded) trials. However, subjects who failed to learn showed decreased sensitivity to errors, even in the initial period in which they followed the rotation, a pattern previously found in parkinsonian patients. In a second experiment, the addition of a secondary mental rotation task completely abolished learning ( <i>n</i> = 10), while a control group replicated the results of the first experiment ( <i>n</i> = 10). These results emphasize a pivotal role of explicit processes during reinforcement-based motor learning, and the susceptibility of this form of learning to disruption has important implications for its potential therapeutic benefits. </p><p id="d713367e171"> <b>NEW &amp; NOTEWORTHY</b> We demonstrate that learning a visuomotor rotation with only reward-based feedback is principally accomplished via the development of a large explicit component. Furthermore, this form of learning is susceptible to disruption with a secondary task. The results suggest that future experiments utilizing reward-based feedback should aim to dissect the roles of implicit and explicit reinforcement learning systems. Therapeutic motor learning approaches based on reward should be aware of the sensitivity to disruption. </p>

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          Most cited references30

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          Temporal structure of motor variability is dynamically regulated and predicts motor learning ability.

          Individual differences in motor learning ability are widely acknowledged, yet little is known about the factors that underlie them. Here we explore whether movement-to-movement variability in motor output, a ubiquitous if often unwanted characteristic of motor performance, predicts motor learning ability. Surprisingly, we found that higher levels of task-relevant motor variability predicted faster learning both across individuals and across tasks in two different paradigms, one relying on reward-based learning to shape specific arm movement trajectories and the other relying on error-based learning to adapt movements in novel physical environments. We proceeded to show that training can reshape the temporal structure of motor variability, aligning it with the trained task to improve learning. These results provide experimental support for the importance of action exploration, a key idea from reinforcement learning theory, showing that motor variability facilitates motor learning in humans and that our nervous systems actively regulate it to improve learning.
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            Prelude to and resolution of an error: EEG phase synchrony reveals cognitive control dynamics during action monitoring.

            Error-related activity in the medial prefrontal cortex (mPFC) is thought to work in conjunction with lateral prefrontal cortex (lPFC) as a part of an action-monitoring network, where errors signal the need for increased cognitive control. The neural mechanism by which this mPFC-lPFC interaction occurs remains unknown. We hypothesized that transient synchronous oscillations in the theta range reflect a mechanism by which these structures interact. To test this hypothesis, we extracted oscillatory phase and power from current-source-density-transformed electroencephalographic data recorded during a Flanker task. Theta power in the mPFC was diminished on the trial preceding an error and increased immediately after an error, consistent with predictions of an action-monitoring system. These power dynamics appeared to take place over a response-related background of oscillatory theta phase coherence. Theta phase synchronization between FCz (mPFC) and F5/6 (lPFC) sites was robustly increased during error trials. The degree of mPFC-lPFC oscillatory synchronization predicted the degree of mPFC power on error trials, and both of these dynamics predicted the degree of posterror reaction time slowing. Oscillatory dynamics in the theta band may in part underlie a mechanism of communication between networks involved in action monitoring and cognitive control.
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              Contributions of spatial working memory to visuomotor learning.

              Previous studies of motor learning have described the importance of cognitive processes during the early stages of learning; however, the precise nature of these processes and their neural correlates remains unclear. The present study investigated whether spatial working memory (SWM) contributes to visuomotor adaptation depending on the stage of learning. We tested the hypothesis that SWM would contribute early in the adaptation process by measuring (i) the correlation between SWM tasks and the rate of adaptation, and (ii) the overlap between the neural substrates of a SWM mental rotation task and visuomotor adaptation. Participants completed a battery of neuropsychological tests, a visuomotor adaptation task, and an SWM task involving mental rotation, with the latter two tasks performed in a 3.0-T MRI scanner. Performance on a neuropsychological test of SWM (two-dimensional mental rotation) correlated with the rate of early, but not late, visuomotor adaptation. During the early, but not late, adaptation period, participants showed overlapping brain activation with the SWM mental rotation task, in right dorsolateral prefrontal cortex and the bilateral inferior parietal lobules. These findings suggest that the early, but not late, phase of visuomotor adaptation engages SWM processes.
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                Author and article information

                Journal
                Journal of Neurophysiology
                Journal of Neurophysiology
                American Physiological Society
                0022-3077
                1522-1598
                June 2018
                June 2018
                : 119
                : 6
                : 2241-2255
                Affiliations
                [1 ]School of Psychology, University of Birmingham, Birmingham, United Kingdom
                Article
                10.1152/jn.00901.2017
                6032115
                29537918
                ad721774-cf99-4d18-b917-b694d286aedd
                © 2018
                History

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