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      Long-term stability of cortical population dynamics underlying consistent behavior

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          Abstract

          Animals readily execute learned behaviors in a consistent manner over long periods of time, yet no equally stable neural correlate has been demonstrated. How does the cortex achieve this stable control? Using the sensorimotor system as a model of cortical processing, we investigated the hypothesis that the dynamics of neural latent activity, which capture the dominant co-variation patterns within the neural population, must be preserved across time. We recorded from populations of neurons in premotor, primary motor, and somatosensory cortices as monkeys performed a reaching task, for up to two years. Intriguingly, despite steady turnover in the recorded neurons, the low-dimensional latent dynamics remained stable. The stability allowed reliable decoding of behavioral features for the entire timespan, while fixed decoders based directly on the recorded neural activity degraded substantially. We posit that stable latent cortical dynamics within the manifold are the fundamental building blocks underlying consistent behavioral execution.

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          Most cited references53

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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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            High-performance neuroprosthetic control by an individual with tetraplegia.

            Paralysis or amputation of an arm results in the loss of the ability to orient the hand and grasp, manipulate, and carry objects, functions that are essential for activities of daily living. Brain-machine interfaces could provide a solution to restoring many of these lost functions. We therefore tested whether an individual with tetraplegia could rapidly achieve neurological control of a high-performance prosthetic limb using this type of an interface. We implanted two 96-channel intracortical microelectrodes in the motor cortex of a 52-year-old individual with tetraplegia. Brain-machine-interface training was done for 13 weeks with the goal of controlling an anthropomorphic prosthetic limb with seven degrees of freedom (three-dimensional translation, three-dimensional orientation, one-dimensional grasping). The participant's ability to control the prosthetic limb was assessed with clinical measures of upper limb function. This study is registered with ClinicalTrials.gov, NCT01364480. The participant was able to move the prosthetic limb freely in the three-dimensional workspace on the second day of training. After 13 weeks, robust seven-dimensional movements were performed routinely. Mean success rate on target-based reaching tasks was 91·6% (SD 4·4) versus median chance level 6·2% (95% CI 2·0-15·3). Improvements were seen in completion time (decreased from a mean of 148 s [SD 60] to 112 s [6]) and path efficiency (increased from 0·30 [0·04] to 0·38 [0·02]). The participant was also able to use the prosthetic limb to do skilful and coordinated reach and grasp movements that resulted in clinically significant gains in tests of upper limb function. No adverse events were reported. With continued development of neuroprosthetic limbs, individuals with long-term paralysis could recover the natural and intuitive command signals for hand placement, orientation, and reaching, allowing them to perform activities of daily living. Defense Advanced Research Projects Agency, National Institutes of Health, Department of Veterans Affairs, and UPMC Rehabilitation Institute. Copyright © 2013 Elsevier Ltd. All rights reserved.
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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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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature neuroscience
                1097-6256
                1546-1726
                24 November 2019
                06 January 2020
                February 2020
                06 July 2020
                : 23
                : 2
                : 260-270
                Affiliations
                [1. ]Neural and Cognitive Engineering Group, Center for Automation and Robotics, Spanish National Research Council, Arganda del Rey, Spain
                [2. ]Department of Physiology, Northwestern University, Chicago, Illinois, USA
                [3. ]Department of Fundamental Neuroscience, Faculty of Medicine, University of Geneva, Geneva, Switzerland
                [4. ]Department of Biomedical Engineering, Northwestern University, Chicago, Illinois, USA
                [5. ]Department of Physics and Astronomy, Northwestern University, Chicago, Illinois, USA
                [6. ]Department of Physical Medicine and Rehabilitation, Northwestern University, and Shirley Ryan Ability Lab, Chicago, Illinois, USA
                Author notes
                [⧫]

                Present address for Juan A. Gallego: Department of Bioengineering, Imperial College London, London, UK

                [†]

                These authors contributed equally.

                [‡]

                These authors jointly supervised this work.

                AUTHOR CONTRIBUTIONS

                J.A.G., M.G.P., S.A.S., and L.E.M. devised the project. M.G.P. and R.H.C. performed experiments and processed the data. J.A.G. and M.G.P. conducted the data analysis. J.A.G., M.G.P., R.H.C., S.A.S., and L.E.M. interpreted data and wrote the manuscript.

                [* ]Correspondence to: Juan A. Gallego ( gallego.juanalvaro@ 123456gmail.com ), Lee E. Miller ( lm@ 123456northwestern.edu )
                Article
                NIHMS1542655
                10.1038/s41593-019-0555-4
                7007364
                31907438
                2c500200-3051-4810-a180-1d0aa09c87b3

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                Neurosciences

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