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      The Dynamical Regime of Sensory Cortex: Stable Dynamics around a Single Stimulus-Tuned Attractor Account for Patterns of Noise Variability

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          Summary

          Correlated variability in cortical activity is ubiquitously quenched following stimulus onset, in a stimulus-dependent manner. These modulations have been attributed to circuit dynamics involving either multiple stable states (“attractors”) or chaotic activity. Here we show that a qualitatively different dynamical regime, involving fluctuations about a single, stimulus-driven attractor in a loosely balanced excitatory-inhibitory network (the stochastic “stabilized supralinear network”), best explains these modulations. Given the supralinear input/output functions of cortical neurons, increased stimulus drive strengthens effective network connectivity. This shifts the balance from interactions that amplify variability to suppressive inhibitory feedback, quenching correlated variability around more strongly driven steady states. Comparing to previously published and original data analyses, we show that this mechanism, unlike previous proposals, uniquely accounts for the spatial patterns and fast temporal dynamics of variability suppression. Specifying the cortical operating regime is key to understanding the computations underlying perception.

          Highlights

          • A simple network model explains stimulus-tuning of cortical variability suppression

          • Inhibition stabilizes recurrently interacting neurons with supralinear I/O functions

          • Stimuli strengthen inhibitory stabilization around a stable state, quenching variability

          • Single-trial V1 data are compatible with this model and rules out competing proposals

          Abstract

          Stimuli suppress cortical correlated variability. Hennequin et al. show that a cortical operating regime of inhibitory stabilization around a single stable state—the “stabilized supralinear network”—explains this suppression’s tuning and timing, while alternative proposed regimes do not.

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          Most cited references71

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          Normalization as a canonical neural computation.

          There is increasing evidence that the brain relies on a set of canonical neural computations, repeating them across brain regions and modalities to apply similar operations to different problems. A promising candidate for such a computation is normalization, in which the responses of neurons are divided by a common factor that typically includes the summed activity of a pool of neurons. Normalization was developed to explain responses in the primary visual cortex and is now thought to operate throughout the visual system, and in many other sensory modalities and brain regions. Normalization may underlie operations such as the representation of odours, the modulatory effects of visual attention, the encoding of value and the integration of multisensory information. Its presence in such a diversity of neural systems in multiple species, from invertebrates to mammals, suggests that it serves as a canonical neural computation.
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            Generating coherent patterns of activity from chaotic neural networks.

            Neural circuits display complex activity patterns both spontaneously and when responding to a stimulus or generating a motor output. How are these two forms of activity related? We develop a procedure called FORCE learning for modifying synaptic strengths either external to or within a model neural network to change chaotic spontaneous activity into a wide variety of desired activity patterns. FORCE learning works even though the networks we train are spontaneously chaotic and we leave feedback loops intact and unclamped during learning. Using this approach, we construct networks that produce a wide variety of complex output patterns, input-output transformations that require memory, multiple outputs that can be switched by control inputs, and motor patterns matching human motion capture data. Our results reproduce data on premovement activity in motor and premotor cortex, and suggest that synaptic plasticity may be a more rapid and powerful modulator of network activity than generally appreciated.
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              Attention improves performance primarily by reducing interneuronal correlations

              Visual attention can dramatically improve behavioural performance by allowing observers to focus on the important information in a complex scene. Attention also typically increases the firing rates of cortical sensory neurons. Rate increases improve the signal-to-noise ratio of individual neurons, and this improvement has been assumed to underlie attention-related improvements in behaviour. We recorded dozens of neurons simultaneously in visual area V4 and found that changes in single neurons accounted for only a small fraction of the improvement in the sensitivity of the population. Instead, over 80% of the attentional improvement in the population signal was caused by decreases in the correlations between the trial-to-trial fluctuations in the responses of pairs of neurons. These results suggest that the representation of sensory information in populations of neurons and the way attention affects the sensitivity of the population may only be understood by considering the interactions between neurons.
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                Author and article information

                Contributors
                Journal
                Neuron
                Neuron
                Neuron
                Cell Press
                0896-6273
                1097-4199
                16 May 2018
                16 May 2018
                : 98
                : 4
                : 846-860.e5
                Affiliations
                [1 ]Computational and Biological Learning Lab, Department of Engineering, University of Cambridge, Cambridge CB2 1PZ, UK
                [2 ]Center for Theoretical Neuroscience, College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
                [3 ]Department of Neuroscience, Swartz Program in Theoretical Neuroscience, Kavli Institute for Brain Science, College of Physicians and Surgeons, Columbia University, New York, NY 10032, USA
                [4 ]Centre de Neurophysique, Physiologie, et Pathologie, CNRS, 75270 Paris Cedex 06, France
                [5 ]Institute of Neuroscience, Department of Biology and Mathematics, University of Oregon, Eugene, OR 97403, USA
                [6 ]Department of Neurology, Massachusetts General Hospital and Brigham and Women’s Hospital, Harvard Medical School, Boston, MA 02115, USA
                [7 ]Department of Cognitive Science, Central European University, 1051 Budapest, Hungary
                Author notes
                []Corresponding author g.hennequin@ 123456eng.cam.ac.uk
                [8]

                Senior author

                [9]

                These authors contributed equally

                [10]

                Lead Contact

                Article
                S0896-6273(18)30325-8
                10.1016/j.neuron.2018.04.017
                5971207
                29772203
                f14ba9ab-2c9e-4a00-9019-9fb682d548fc
                © 2018 The Author(s)

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 2 August 2016
                : 14 February 2018
                : 12 April 2018
                Categories
                Article

                Neurosciences
                cortical variability,circuit dynamics,noise correlations,variability quenching,v1,mt,theoretical neuroscience

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