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      Visually-updated hand state estimates modulate the proprioceptive reflex independently of motor task requirements

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          Abstract

          Fast signaling from vision and proprioception to muscle activation plays essential roles in quickly correcting movement. Though many studies have demonstrated modulation of the quick sensorimotor responses as depending on context in each modality, the contribution of multimodal information has not been established. Here, we examined whether state estimates contributing to stretch reflexes are represented solely by proprioceptive information or by multimodal information. Unlike previous studies, we newly found a significant stretch-reflex attenuation by the distortion and elimination of visual-feedback without any change in motor tasks. Furthermore, the stretch-reflex amplitude reduced with increasing elimination durations which would degrade state estimates. By contrast, even though a distortion was introduced in the target-motor-mapping, the stretch reflex was not simultaneously attenuated with visuomotor reflex. Our results therefore indicate that the observed stretch-reflex attenuation is specifically ascribed to uncertainty increase in estimating hand states, suggesting multimodal contributions to the generation of stretch reflexes.

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          Most cited references59

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          Bayesian integration in sensorimotor learning.

          When we learn a new motor skill, such as playing an approaching tennis ball, both our sensors and the task possess variability. Our sensors provide imperfect information about the ball's velocity, so we can only estimate it. Combining information from multiple modalities can reduce the error in this estimate. On a longer time scale, not all velocities are a priori equally probable, and over the course of a match there will be a probability distribution of velocities. According to bayesian theory, an optimal estimate results from combining information about the distribution of velocities-the prior-with evidence from sensory feedback. As uncertainty increases, when playing in fog or at dusk, the system should increasingly rely on prior knowledge. To use a bayesian strategy, the brain would need to represent the prior distribution and the level of uncertainty in the sensory feedback. Here we control the statistical variations of a new sensorimotor task and manipulate the uncertainty of the sensory feedback. We show that subjects internally represent both the statistical distribution of the task and their sensory uncertainty, combining them in a manner consistent with a performance-optimizing bayesian process. The central nervous system therefore employs probabilistic models during sensorimotor learning.
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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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              Optimal feedback control and the neural basis of volitional motor control.

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                Author and article information

                Contributors
                Role: Reviewing Editor
                Role: Senior Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                31 March 2020
                2020
                : 9
                : e52380
                Affiliations
                [1 ]NTT Communication Science Laboratories, Nippon Telegraph and Telephone Co. KanagawaJapan
                University of Ottawa Canada
                University of Pennsylvania United States
                University of Ottawa Canada
                University of Ottawa Canada
                Author information
                https://orcid.org/0000-0003-3541-2251
                Article
                52380
                10.7554/eLife.52380
                7108863
                32228855
                d93a2a9e-3567-4458-bafc-fdafefc6418d
                © 2020, Ito and Gomi

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 03 October 2019
                : 13 March 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: JP16H06566
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                Distortion and elimination of limb visual feedback affects low-level stretch reflex control, indicating the involvement of a high-level and multimodal representation of the limb state in orchestrating hierarchical sensorimotor control.

                Life sciences
                sensorimotor hierarchy,multimodal state representation,target reaching movement,visual feedback,limb state uncertainty,human

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