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      Reorganization between preparatory and movement population responses in motor cortex

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          Abstract

          Neural populations can change the computation they perform on very short timescales. Although such flexibility is common, the underlying computational strategies at the population level remain unknown. To address this gap, we examined population responses in motor cortex during reach preparation and movement. We found that there exist exclusive and orthogonal population-level subspaces dedicated to preparatory and movement computations. This orthogonality yielded a reorganization in response correlations: the set of neurons with shared response properties changed completely between preparation and movement. Thus, the same neural population acts, at different times, as two separate circuits with very different properties. This finding is not predicted by existing motor cortical models, which predict overlapping preparation-related and movement-related subspaces. Despite orthogonality, responses in the preparatory subspace were lawfully related to subsequent responses in the movement subspace. These results reveal a population-level strategy for performing separate but linked computations.

          Abstract

          Single neuron responses are highly complex and dynamic yet they are able to flexibly represent behaviour through their collective activity. Here the authors demonstrate that population activity patterns of motor cortex neurons are orthogonal during successive task epochs that are linked through a simple linear function.

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          Most cited references61

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          Real-time computing without stable states: a new framework for neural computation based on perturbations.

          A key challenge for neural modeling is to explain how a continuous stream of multimodal input from a rapidly changing environment can be processed by stereotypical recurrent circuits of integrate-and-fire neurons in real time. We propose a new computational model for real-time computing on time-varying input that provides an alternative to paradigms based on Turing machines or attractor neural networks. It does not require a task-dependent construction of neural circuits. Instead, it is based on principles of high-dimensional dynamical systems in combination with statistical learning theory and can be implemented on generic evolved or found recurrent circuitry. It is shown that the inherent transient dynamics of the high-dimensional dynamical system formed by a sufficiently large and heterogeneous neural circuit may serve as universal analog fading memory. Readout neurons can learn to extract in real time from the current state of such recurrent neural circuit information about current and past inputs that may be needed for diverse tasks. Stable internal states are not required for giving a stable output, since transient internal states can be transformed by readout neurons into stable target outputs due to the high dimensionality of the dynamical system. Our approach is based on a rigorous computational model, the liquid state machine, that, unlike Turing machines, does not require sequential transitions between well-defined discrete internal states. It is supported, as the Turing machine is, by rigorous mathematical results that predict universal computational power under idealized conditions, but for the biologically more realistic scenario of real-time processing of time-varying inputs. Our approach provides new perspectives for the interpretation of neural coding, the design of experiments and data analysis in neurophysiology, and the solution of problems in robotics and neurotechnology.
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            The importance of mixed selectivity in complex cognitive tasks.

            Single-neuron activity in the prefrontal cortex (PFC) is tuned to mixtures of multiple task-related aspects. Such mixed selectivity is highly heterogeneous, seemingly disordered and therefore difficult to interpret. We analysed the neural activity recorded in monkeys during an object sequence memory task to identify a role of mixed selectivity in subserving the cognitive functions ascribed to the PFC. We show that mixed selectivity neurons encode distributed information about all task-relevant aspects. Each aspect can be decoded from the population of neurons even when single-cell selectivity to that aspect is eliminated. Moreover, mixed selectivity offers a significant computational advantage over specialized responses in terms of the repertoire of input-output functions implementable by readout neurons. This advantage originates from the highly diverse nonlinear selectivity to mixtures of task-relevant variables, a signature of high-dimensional neural representations. Crucially, this dimensionality is predictive of animal behaviour as it collapses in error trials. Our findings recommend a shift of focus for future studies from neurons that have easily interpretable response tuning to the widely observed, but rarely analysed, mixed selectivity neurons.
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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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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                27 October 2016
                2016
                : 7
                : 13239
                Affiliations
                [1 ]Center for Theoretical Neuroscience, Columbia University , New York, New York 10032, USA
                [2 ]Department of Neuroscience, Columbia University Medical Center , New York, New York 10032, USA
                [3 ]Cold Spring Harbor Laboratory , Cold Spring Harbor, New York 11724, USA
                [4 ]Grossman Center for the Statistics of Mind, Columbia University , 1255 Amsterdam Avenue, New York, New York 10027, USA
                [5 ]David Mahoney Center for Brain and Behavior Research, Columbia University Medical Center , New York, New York 10032, USA
                [6 ]Kavli Institute for Brain Science, Columbia University Medical Center , New York, New York 10032, USA
                [7 ]Department of Statistics, Columbia University , 1255 Amsterdam Avenue, Room 1005 SSW, MC 4690, New York, New York 10027, USA
                Author notes
                [*]

                These authors contributed equally to this work

                Article
                ncomms13239
                10.1038/ncomms13239
                5095296
                27807345
                aa3be64e-fac8-42db-b254-55a21792bf08
                Copyright © 2016, 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/

                History
                : 27 June 2016
                : 14 September 2016
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