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      Effective reinforcement learning following cerebellar damage requires a balance between exploration and motor noise

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          Abstract

          See Miall and Galea (doi: [Related article:]10.1093/awv343) for a scientific commentary on this article.

          Cerebellar lesions impair both coordination and motor learning. Therrien et al. show that affected individuals can learn using a reinforcement mechanism despite a deficit in error-based motor learning. They also identify a critical feature of cerebellar patients’ movements (motor noise), which determines the effectiveness of learning under reinforcement.

          Abstract

          See Miall and Galea (doi: [Related article:]10.1093/awv343) for a scientific commentary on this article.

          Cerebellar lesions impair both coordination and motor learning. Therrien et al. show that affected individuals can learn using a reinforcement mechanism despite a deficit in error-based motor learning. They also identify a critical feature of cerebellar patients’ movements (motor noise), which determines the effectiveness of learning under reinforcement.

          Abstract

          See Miall and Galea (doi: [Related article:]10.1093/awv343) for a scientific commentary on this article.

          Reinforcement and error-based processes are essential for motor learning, with the cerebellum thought to be required only for the error-based mechanism. Here we examined learning and retention of a reaching skill under both processes. Control subjects learned similarly from reinforcement and error-based feedback, but showed much better retention under reinforcement. To apply reinforcement to cerebellar patients, we developed a closed-loop reinforcement schedule in which task difficulty was controlled based on recent performance. This schedule produced substantial learning in cerebellar patients and controls. Cerebellar patients varied in their learning under reinforcement but fully retained what was learned. In contrast, they showed complete lack of retention in error-based learning. We developed a mechanistic model of the reinforcement task and found that learning depended on a balance between exploration variability and motor noise. While the cerebellar and control groups had similar exploration variability, the patients had greater motor noise and hence learned less. Our results suggest that cerebellar damage indirectly impairs reinforcement learning by increasing motor noise, but does not interfere with the reinforcement mechanism itself. Therefore, reinforcement can be used to learn and retain novel skills, but optimal reinforcement learning requires a balance between exploration variability and motor noise.

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          Most cited references21

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          Adaptive representation of dynamics during learning of a motor task.

          We investigated how the CNS learns to control movements in different dynamical conditions, and how this learned behavior is represented. In particular, we considered the task of making reaching movements in the presence of externally imposed forces from a mechanical environment. This environment was a force field produced by a robot manipulandum, and the subjects made reaching movements while holding the end-effector of this manipulandum. Since the force field significantly changed the dynamics of the task, subjects' initial movements in the force field were grossly distorted compared to their movements in free space. However, with practice, hand trajectories in the force field converged to a path very similar to that observed in free space. This indicated that for reaching movements, there was a kinematic plan independent of dynamical conditions. The recovery of performance within the changed mechanical environment is motor adaptation. In order to investigate the mechanism underlying this adaptation, we considered the response to the sudden removal of the field after a training phase. The resulting trajectories, named aftereffects, were approximately mirror images of those that were observed when the subjects were initially exposed to the field. This suggested that the motor controller was gradually composing a model of the force field, a model that the nervous system used to predict and compensate for the forces imposed by the environment. In order to explore the structure of the model, we investigated whether adaptation to a force field, as presented in a small region, led to aftereffects in other regions of the workspace. We found that indeed there were aftereffects in workspace regions where no exposure to the field had taken place; that is, there was transfer beyond the boundary of the training data. This observation rules out the hypothesis that the subject's model of the force field was constructed as a narrow association between visited states and experienced forces; that is, adaptation was not via composition of a look-up table. In contrast, subjects modeled the force field by a combination of computational elements whose output was broadly tuned across the motor state space. These elements formed a model that extrapolated to outside the training region in a coordinate system similar to that of the joints and muscles rather than end-point forces. This geometric property suggests that the elements of the adaptive process represent dynamics of a motor task in terms of the intrinsic coordinate system of the sensors and actuators.
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            Behavioral theories and the neurophysiology of reward.

            The functions of rewards are based primarily on their effects on behavior and are less directly governed by the physics and chemistry of input events as in sensory systems. Therefore, the investigation of neural mechanisms underlying reward functions requires behavioral theories that can conceptualize the different effects of rewards on behavior. The scientific investigation of behavioral processes by animal learning theory and economic utility theory has produced a theoretical framework that can help to elucidate the neural correlates for reward functions in learning, goal-directed approach behavior, and decision making under uncertainty. Individual neurons can be studied in the reward systems of the brain, including dopamine neurons, orbitofrontal cortex, and striatum. The neural activity can be related to basic theoretical terms of reward and uncertainty, such as contiguity, contingency, prediction error, magnitude, probability, expected value, and variance.
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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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                Author and article information

                Journal
                Brain
                Brain
                brainj
                brain
                Brain
                Oxford University Press
                0006-8950
                1460-2156
                January 2016
                01 December 2015
                01 December 2015
                : 139
                : 1
                : 101-114
                Affiliations
                1 Kennedy Krieger Institute, Center for Movement Studies, 707 N Broadway, Baltimore, MD, USA
                2 Johns Hopkins University School of Medicine, Department of Neuroscience, 725 N Wolfe St., Baltimore, MD, USA
                3 University of Cambridge, Department of Engineering, Trumpington St. Cambridge, UK CB2 1PZ, UK
                Author notes
                Correspondence to: Amy J. Bastian PhD, Kennedy Krieger Institute, 707 N Broadway, Baltimore, MD, USA 21205 E-mail: bastian@ 123456kennedykrieger.org

                *These authors contributed equally to this work.

                See Miall and Galea (doi: [Related article:]10.1093/awv343) for a scientific commentary on this article.

                Article
                awv329
                10.1093/brain/awv329
                4949390
                26626368
                a0381239-e132-4fbd-a5aa-63d79f50f9d6
                © The Author (2015). Published by Oxford University Press on behalf of the Guarantors of Brain.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 31 July 2015
                : 8 September 2015
                : 25 September 2015
                Page count
                Pages: 14
                Categories
                Original Articles
                1040

                Neurosciences
                reinforcement learning,adaptation,visuomotor rotation,ataxia,cerebellum
                Neurosciences
                reinforcement learning, adaptation, visuomotor rotation, ataxia, cerebellum

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