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      Stable task information from an unstable neural population

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          Abstract

          Over days and weeks, neural activity representing an animal’s position and movement in sensorimotor cortex has been found to continually reconfigure or ‘drift’ during repeated trials of learned tasks, with no obvious change in behavior. This challenges classical theories, which assume stable engrams underlie stable behavior. However, it is not known whether this drift occurs systematically, allowing downstream circuits to extract consistent information. Analyzing long-term calcium imaging recordings from posterior parietal cortex in mice ( Mus musculus), we show that drift is systematically constrained far above chance, facilitating a linear weighted readout of behavioral variables. However, a significant component of drift continually degrades a fixed readout, implying that drift is not confined to a null coding space. We calculate the amount of plasticity required to compensate drift independently of any learning rule, and find that this is within physiologically achievable bounds. We demonstrate that a simple, biologically plausible local learning rule can achieve these bounds, accurately decoding behavior over many days.

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          Most cited references36

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          On the implementation of an interior-point filter line-search algorithm for large-scale nonlinear programming

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            Long-term dynamics of CA1 hippocampal place codes

            Via Ca2+-imaging in freely behaving mice that repeatedly explored a familiar environment, we tracked thousands of CA1 pyramidal cells' place fields over weeks. Place coding was dynamic, for each day the ensemble representation of this environment involved a unique subset of cells. Yet, cells within the ∼15–25% overlap between any two of these subsets retained the same place fields, which sufficed to preserve an accurate spatial representation across weeks.
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              Choice-specific sequences in parietal cortex during a virtual-navigation decision task

              The posterior parietal cortex (PPC) plays an important role in many cognitive behaviors; however, the neural circuit dynamics underlying PPC function are not well understood. Here we optically imaged the spatial and temporal activity patterns of neuronal populations in mice performing a PPC-dependent task that combined a perceptual decision and memory-guided navigation in a virtual environment. Individual neurons had transient activation staggered relative to one another in time, forming a sequence of neuronal activation spanning the entire length of a task trial. Distinct sequences of neurons were triggered on trials with opposite behavioral choices and defined divergent, choice-specific trajectories through a state space of neuronal population activity. Cells participating in the different sequences and at distinct time points in the task were anatomically intermixed over microcircuit length scales (< 100 micrometers). During working memory decision tasks the PPC may therefore perform computations through sequence-based circuit dynamics, rather than long-lived stable states, implemented using anatomically intermingled microcircuits.
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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
                14 July 2020
                2020
                : 9
                : e51121
                Affiliations
                [1 ]Department of Engineering, University of Cambridge CambridgeUnited Kingdom
                [2 ]Department of Electrical Engineering, Stanford University StanfordUnited States
                [3 ]Department of Neurobiology, Harvard Medical School BostonUnited States
                University of Chicago United States
                Emory University United States
                University of Chicago United States
                Author information
                https://orcid.org/0000-0002-4196-774X
                https://orcid.org/0000-0002-1029-0158
                Article
                51121
                10.7554/eLife.51121
                7392606
                32660692
                6a236f50-fae7-4fdf-8899-327206883b5b
                © 2020, Rule 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
                : 15 August 2019
                : 17 June 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000854, Human Frontier Science Program;
                Award ID: RGY0069
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100010663, H2020 European Research Council;
                Award ID: FLEXNEURO 716643
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: NS089521
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: MH107620
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: NS108410
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Short Report
                Computational and Systems Biology
                Neuroscience
                Custom metadata
                Analysis and modelling of sensorimotor neural activity shows how ongoing plasticity and appropriately tuned weights can cope with substantial ongoing changes in the neural code.

                Life sciences
                spatial navigation,learning and memory,neural coding,computational neuroscience,plasticity,systems modeling,mouse

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