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      Motor cortex activity across movement speeds is predicted by network-level strategies for generating muscle activity

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          Abstract

          Learned movements can be skillfully performed at different paces. What neural strategies produce this flexibility? Can they be predicted and understood by network modeling? We trained monkeys to perform a cycling task at different speeds, and trained artificial recurrent networks to generate the empirical muscle-activity patterns. Network solutions reflected the principle that smooth well-behaved dynamics require low trajectory tangling. Network solutions had a consistent form, which yielded quantitative and qualitative predictions. To evaluate predictions, we analyzed motor cortex activity recorded during the same task. Responses supported the hypothesis that the dominant neural signals reflect not muscle activity, but network-level strategies for generating muscle activity. Single-neuron responses were better accounted for by network activity than by muscle activity. Similarly, neural population trajectories shared their organization not with muscle trajectories, but with network solutions. Thus, cortical activity could be understood based on the need to generate muscle activity via dynamics that allow smooth, robust control over movement speed.

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          Most cited references57

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          How does the brain solve visual object recognition?

          Mounting evidence suggests that 'core object recognition,' the ability to rapidly recognize objects despite substantial appearance variation, is solved in the brain via a cascade of reflexive, largely feedforward computations that culminate in a powerful neuronal representation in the inferior temporal cortex. However, the algorithm that produces this solution remains poorly understood. Here we review evidence ranging from individual neurons and neuronal populations to behavior and computational models. We propose that understanding this algorithm will require using neuronal and psychophysical data to sift through many computational models, each based on building blocks of small, canonical subnetworks with a common functional goal. Copyright © 2012 Elsevier Inc. All rights reserved.
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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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              A solution for the best rotation to relate two sets of vectors

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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
                27 May 2022
                2022
                : 11
                : e67620
                Affiliations
                [1 ] Department of Electrical and Computer Engineering, University of Florida ( https://ror.org/02y3ad647) Gainesville United States
                [2 ] Zuckerman Mind Brain Behavior Institute, Columbia University ( https://ror.org/00hj8s172) New York United States
                [3 ] Grossman Center for the Statistics of Mind, Columbia University ( https://ror.org/00hj8s172) New York United States
                [4 ] Center for Theoretical Neuroscience, Columbia University ( https://ror.org/00hj8s172) New York United States
                [5 ] Department of Statistics, Columbia University ( https://ror.org/00hj8s172) New York United States
                [6 ] Department of Neuroscience, Columbia University ( https://ror.org/00hj8s172) New York United States
                [7 ] Kavli Institute for Brain Science, Columbia University ( https://ror.org/00hj8s172) New York United States
                Western University ( https://ror.org/02grkyz14) Canada
                University of Pennsylvania ( https://ror.org/00b30xv10) United States
                Western University ( https://ror.org/02grkyz14) Canada
                Western University ( https://ror.org/02grkyz14) Canada
                Author notes
                [†]

                These authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0003-4655-7050
                https://orcid.org/0000-0001-9123-6526
                Article
                67620
                10.7554/eLife.67620
                9197394
                35621264
                96a00f34-cab7-4dc8-b22a-c5f2ac84e170
                © 2022, Saxena, Russo et al

                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
                : 17 February 2021
                : 26 May 2022
                Funding
                Funded by: Grossman Center for the Statistics of Mind;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000879, Alfred P. Sloan Foundation;
                Award ID: FG-2015-65496
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000893, Simons Foundation;
                Award ID: 542963
                Award Recipient :
                Funded by: NIH;
                Award ID: 1U19NS104649
                Award Recipient :
                Funded by: NIH;
                Award ID: 5T32NS064929
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100001201, Kavli Foundation;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000893, Simons Foundation;
                Award ID: 325171
                Award Recipient :
                Funded by: Swiss National Science Foundation;
                Award ID: P2SKP2 178197
                Award Recipient :
                Funded by: Swiss National Science Foundation;
                Award ID: P400P2 186759
                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
                While performing learned movements at different speeds, motor cortex population activity can be understood based on the need to generate muscle activity via smooth, well-behaved dynamics.

                Life sciences
                motor cortex,speed,tangling,dynamical systems,neural networks,movement,rhesus macaque
                Life sciences
                motor cortex, speed, tangling, dynamical systems, neural networks, movement, rhesus macaque

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