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      Cortical population activity within a preserved neural manifold underlies multiple motor behaviors

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          Abstract

          Populations of cortical neurons flexibly perform different functions; for the primary motor cortex (M1) this means a rich repertoire of motor behaviors. We investigate the flexibility of M1 movement control by analyzing neural population activity during a variety of skilled wrist and reach-to-grasp tasks. We compare across tasks the neural modes that capture dominant neural covariance patterns during each task. While each task requires different patterns of muscle and single unit activity, we find unexpected similarities at the neural population level: the structure and activity of the neural modes is largely preserved across tasks. Furthermore, we find two sets of neural modes with task-independent activity that capture, respectively, generic temporal features of the set of tasks and a task-independent mapping onto muscle activity. This system of flexibly combined, well-preserved neural modes may underlie the ability of M1 to learn and generate a wide-ranging behavioral repertoire.

          Abstract

          Motor cortical neurons enable performance of a wide range of movements. Here, the authors report that dominant population activity patterns, the neural modes, are largely preserved across various tasks, with many displaying consistent temporal dynamics and reliably mapping onto muscle activity.

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          Most cited references74

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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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            Dimensionality reduction for large-scale neural recordings.

            Most sensory, cognitive and motor functions depend on the interactions of many neurons. In recent years, there has been rapid development and increasing use of technologies for recording from large numbers of neurons, either sequentially or simultaneously. A key question is what scientific insight can be gained by studying a population of recorded neurons beyond studying each neuron individually. Here, we examine three important motivations for population studies: single-trial hypotheses requiring statistical power, hypotheses of population response structure and exploratory analyses of large data sets. Many recent studies have adopted dimensionality reduction to analyze these populations and to find features that are not apparent at the level of individual neurons. We describe the dimensionality reduction methods commonly applied to population activity and offer practical advice about selecting methods and interpreting their outputs. This review is intended for experimental and computational researchers who seek to understand the role dimensionality reduction has had and can have in systems neuroscience, and who seek to apply these methods to their own data.
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              On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex.

              The activity of single cells in the motor cortex was recorded while monkeys made arm movements in eight directions (at 45 degrees intervals) in a two-dimensional apparatus. These movements started from the same point and were of the same amplitude. The activity of 606 cells related to proximal arm movements was examined in the task; 323 of the 606 cells were active in that task and were studied in detail. The frequency of discharge of 241 of the 323 cells (74.6%) varied in an orderly fashion with the direction of movement. Discharge was most intense with movements in a preferred direction and was reduced gradually when movements were made in directions farther and farther away from the preferred one. This resulted in a bell-shaped directional tuning curve. These relations were observed for cell discharge during the reaction time, the movement time, and the period that preceded the earliest changes in the electromyographic activity (approximately 80 msec before movement onset). In about 75% of the 241 directionally tuned cells, the frequency of discharge, D, was a sinusoidal function of the direction of movement, theta: D = b0 + b1 sin theta + b2cos theta, or, in terms of the preferred direction, theta 0: D = b0 + c1cos (theta - theta0), where b0, b1, b2, and c1 are regression coefficients. Preferred directions differed for different cells so that the tuning curves partially overlapped. The orderly variation of cell discharge with the direction of movement and the fact that cells related to only one of the eight directions of movement tested were rarely observed indicate that movements in a particular direction are not subserved by motor cortical cells uniquely related to that movement. It is suggested, instead, that a movement trajectory in a desired direction might be generated by the cooperation of cells with overlapping tuning curves. The nature of this hypothetical population code for movement direction remains to be elucidated.
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                Author and article information

                Contributors
                gallego.juanalvaro@gmail.com
                lm@northwestern.edu
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                12 October 2018
                12 October 2018
                2018
                : 9
                : 4233
                Affiliations
                [1 ]ISNI 0000 0001 2299 3507, GRID grid.16753.36, Department of Physiology, Feinberg School of Medicine, , Northwestern University, ; 303 E. Chicago Avenue, Chicago, IL 60611 USA
                [2 ]Neural and Cognitive Engineering Group, Centre for Automation and Robotics CSIC-UPM, Ctra. Campo Real km 0.2 - La Poveda, 28500 Arganda del Rey, Spain
                [3 ]ISNI 0000 0001 2299 3507, GRID grid.16753.36, Department of Biomedical Engineering, , Northwestern University, ; 2145 Sheridan Road, Evanston, IL 60208 USA
                [4 ]ISNI 0000 0000 9064 4811, GRID grid.63984.30, Département de Psychiatrie et Neurosciences, Université Laval, , CERVO Research Center, ; 2601 Ch. de la Canardière, Québec, QC G1J 2G3 Canada
                [5 ]ISNI 0000 0001 2299 3507, GRID grid.16753.36, Department of Physics and Astronomy, , Northwestern University, ; Evanston, IL 60208 USA
                [6 ]ISNI 0000 0001 2299 3507, GRID grid.16753.36, Department of Physical Medicine and Rehabilitation, , Northwestern University, ; Chicago, IL 60611 USA
                Author information
                http://orcid.org/0000-0003-2146-0703
                http://orcid.org/0000-0001-9800-2386
                http://orcid.org/0000-0002-5048-6884
                http://orcid.org/0000-0001-8675-7140
                Article
                6560
                10.1038/s41467-018-06560-z
                6185944
                30315158
                635175c5-3fb4-4bb5-9745-81ba2d604d22
                © The Author(s) 2018

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 16 September 2017
                : 12 September 2018
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100004963, EC | Seventh Framework Programme (European Union Seventh Framework Programme);
                Award ID: FP7-PEOPLE-2013-IOF-627384
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100000065, U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS);
                Award ID: F31-NS092356
                Award ID: NS053603
                Award ID: NS053603
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100006937, U.S. Department of Health & Human Services | NIH | NICHD | National Center for Medical Rehabilitation Research (NCMRR);
                Award ID: T32-HD07418
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100006435, Center for Selective C-H Functionalization, National Science Foundation;
                Award ID: DGE-1324585
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100000156, Fonds de Recherche du Québec - Santé (Fonds de la recherche en sante du Quebec);
                Award ID: 22343
                Award Recipient :
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