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      Motor planning flexibly optimizes performance under uncertainty about task goals

      a , 1 , 1

      Nature Communications

      Nature Publishing Group

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          Abstract

          In an environment full of potential goals, how does the brain determine which movement to execute? Existing theories posit that the motor system prepares for all potential goals by generating several motor plans in parallel. One major line of evidence for such theories is that presenting two competing goals often results in a movement intermediate between them. These intermediate movements are thought to reflect an unintentional averaging of the competing plans. However, normative theories suggest instead that intermediate movements might actually be deliberate, generated because they improve task performance over a random guessing strategy. To test this hypothesis, we vary the benefit of making an intermediate movement by changing movement speed. We find that participants generate intermediate movements only at (slower) speeds where they measurably improve performance. Our findings support the normative view that the motor system selects only a single, flexible motor plan, optimized for uncertain goals.

          Abstract

          It is thought that, when goals are uncertain, actions are generated by averaging multiple possible movement plans. Here the authors show that movement planning under uncertainty instead varies flexibly depending on the speed of the movement in order to maximize success.

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          Most cited references 40

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          Neural population dynamics during reaching

          Most theories of motor cortex have assumed that neural activity represents movement parameters. This view derives from an analogous approach to primary visual cortex, where neural activity represents patterns of light. Yet it is unclear how well that analogy holds. Single-neuron responses in motor cortex appear strikingly complex, and there is marked disagreement regarding which movement parameters are represented. A better analogy might be with other motor systems, where a common principle is rhythmic neural activity. We found that motor cortex responses during reaching contain a brief but strong oscillatory component, something quite unexpected for a non-periodic behavior. Oscillation amplitude and phase followed naturally from the preparatory state, suggesting a mechanistic role for preparatory neural activity. These results demonstrate unexpected yet surprisingly simple structure in the population response. That underlying structure explains many of the confusing features of individual-neuron responses.
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            Cortical mechanisms of action selection: the affordance competition hypothesis.

             Paul Cisek (2007)
            At every moment, the natural world presents animals with two fundamental pragmatic problems: selection between actions that are currently possible and specification of the parameters or metrics of those actions. It is commonly suggested that the brain addresses these by first constructing representations of the world on which to build knowledge and make a decision, and then by computing and executing an action plan. However, neurophysiological data argue against this serial viewpoint. In contrast, it is proposed here that the brain processes sensory information to specify, in parallel, several potential actions that are currently available. These potential actions compete against each other for further processing, while information is collected to bias this competition until a single response is selected. The hypothesis suggests that the dorsal visual system specifies actions which compete against each other within the fronto-parietal cortex, while a variety of biasing influences are provided by prefrontal regions and the basal ganglia. A computational model is described, which illustrates how this competition may take place in the cerebral cortex. Simulations of the model capture qualitative features of neurophysiological data and reproduce various behavioural phenomena.
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              Evidence for a distributed hierarchy of action representation in the brain.

              Complex human behavior is organized around temporally distal outcomes. Behavioral studies based on tasks such as normal prehension, multi-step object use and imitation establish the existence of relative hierarchies of motor control. The retrieval errors in apraxia also support the notion of a hierarchical model for representing action in the brain. In this review, three functional brain imaging studies of action observation using the method of repetition suppression are used to identify a putative neural architecture that supports action understanding at the level of kinematics, object centered goals and ultimately, motor outcomes. These results, based on observation, may match a similar functional-anatomic hierarchy for action planning and execution. If this is true, then the findings support a functional-anatomic model that is distributed across a set of interconnected brain areas that are differentially recruited for different aspects of goal-oriented behavior, rather than a homogeneous mirror neuron system for organizing and understanding all behavior.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                03 March 2017
                2017
                : 8
                Affiliations
                [1 ]Department of Neurology, Johns Hopkins University School of Medicine , Baltimore, Maryland 21287, USA
                Author notes
                Article
                ncomms14624
                10.1038/ncomms14624
                5337982
                28256513
                Copyright © 2017, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

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