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      Bayesian Integration and Non-Linear Feedback Control in a Full-Body Motor Task

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          Abstract

          A large number of experiments have asked to what degree human reaching movements can be understood as being close to optimal in a statistical sense. However, little is known about whether these principles are relevant for other classes of movements. Here we analyzed movement in a task that is similar to surfing or snowboarding. Human subjects stand on a force plate that measures their center of pressure. This center of pressure affects the acceleration of a cursor that is displayed in a noisy fashion (as a cloud of dots) on a projection screen while the subject is incentivized to keep the cursor close to a fixed position. We find that salient aspects of observed behavior are well-described by optimal control models where a Bayesian estimation model (Kalman filter) is combined with an optimal controller (either a Linear-Quadratic-Regulator or Bang-bang controller). We find evidence that subjects integrate information over time taking into account uncertainty. However, behavior in this continuous steering task appears to be a highly non-linear function of the visual feedback. While the nervous system appears to implement Bayes-like mechanisms for a full-body, dynamic task, it may additionally take into account the specific costs and constraints of the task.

          Author Summary

          There is a growing body of work demonstrating that humans are close to statistically optimal in both their perception of the world and their actions on it. That is, we seem to combine information from our sensors with the constraints and costs of moving to minimize our errors and effort. Most of the evidence for this type of behavior comes from tasks such as reaching in a small workspace or standing on a force plate passively viewing a stimulus. Although humans appear to be near-optimal for these tasks, it is not clear whether the theory holds for other tasks. Here we introduce a full-body, goal-directed task similar to surfing or snowboarding where subjects steer a cursor with their center of pressure. We find that subjects respond to sensory uncertainty near-optimally in this task, but their behavior is highly non-linear. This suggests that the computations performed by the nervous system may take into account a more complicated set of costs and constraints than previously supposed.

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          Most cited references18

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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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            Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action.

            We show that while a primate chooses between two reaching actions, its motor system first represents both options and later reflects selection between them. When two potential targets appeared, many (43%) task-related, directionally tuned cells in dorsal premotor cortex (PMd) discharged if one of the targets was near their preferred direction. At the population level, this generated two simultaneous sustained directional signals corresponding to the current reach options. After a subsequent nonspatial cue identified the correct target, the corresponding directional signal increased, and the signal for the rejected target was suppressed. The PMd population reliably predicted the monkey's response choice, including errors. This supports a planning model in which multiple reach options are initially specified and then gradually eliminated in a competition for overt execution, as more information accumulates.
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              • Article: not found

              Optimal feedback control and the neural basis of volitional motor control.

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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, USA )
                1553-734X
                1553-7358
                December 2009
                December 2009
                24 December 2009
                : 5
                : 12
                : e1000629
                Affiliations
                [1 ]Department of Physical Medicine and Rehabilitation, Northwestern University and Rehabilitation Institute of Chicago, Chicago, Illinois, United States of America
                [2 ]Department of Physiology, Northwestern University, Chicago, Illinois, United States of America
                [3 ]Department of Applied Mathematics, Northwestern University, Chicago, Illinois, United States of America
                University College London, United Kingdom
                Author notes

                Conceived and designed the experiments: IHS KW KPK. Performed the experiments: IHS HLF IV. Analyzed the data: IHS HLF KW. Wrote the paper: IHS HLF IV KW KPK.

                Article
                09-PLCB-RA-0939R3
                10.1371/journal.pcbi.1000629
                2789327
                20041205
                b005879f-bc77-4666-8a6f-eff7b68562f7
                Stevenson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 6 August 2009
                : 24 November 2009
                Page count
                Pages: 9
                Categories
                Research Article
                Computer Science/Systems and Control Theory
                Neuroscience/Motor Systems
                Neuroscience/Theoretical Neuroscience

                Quantitative & Systems biology
                Quantitative & Systems biology

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