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      Reward Association Enhances Stimulus-Specific Representations in Primary Visual Cortex

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          Summary

          The potential for neuronal representations of external stimuli to be modified by previous experience is critical for efficient sensory processing and improved behavioral outcomes. To investigate how repeated exposure to a visual stimulus affects its representation in mouse primary visual cortex (V1), we performed two-photon calcium imaging of layer 2/3 neurons and assessed responses before, during, and after the presentation of a repetitive stimulus over 5 consecutive days. We found a stimulus-specific enhancement of the neuronal representation of the repetitively presented stimulus when it was associated with a reward. This was observed both after mice actively learned a rewarded task and when the reward was randomly received. Stimulus-specific enhanced representation resulted both from neurons gaining selectivity and from increased response reliability in previously selective neurons. In the absence of reward, there was either no change in stimulus representation or a decreased representation when the stimulus was viewed at a fixed temporal frequency. Pairing a second stimulus with a reward led to a similar enhanced representation and increased discriminability between the equally rewarded stimuli. Single-neuron responses showed that separate subpopulations discriminated between the two rewarded stimuli depending on whether the stimuli were displayed in a virtual environment or viewed on a single screen. We suggest that reward-associated responses enable the generalization of enhanced stimulus representation across these V1 subpopulations. We propose that this dynamic regulation of visual processing based on the behavioral relevance of sensory input ultimately enhances and stabilizes the representation of task-relevant features while suppressing responses to non-relevant stimuli.

          Highlights

          • Reward association drives the enhanced representation of repetitive visual stimuli

          • Increased discriminability between two equally rewarded stimuli with learning

          • Enhanced responses to rewarded stimuli generalize across subpopulations and contexts

          • Dynamic regulation of V1 responses based on behavioral relevance of visual input

          Abstract

          Henschke et al. show that reward association enhances the representation of repetitive visual stimuli in mouse primary visual cortex. Two equally rewarded stimuli led to similar enhanced representation and increased discriminability with learning. Responses to rewarded stimuli generalize across V1 subpopulations and viewing contexts.

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          Most cited references61

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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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            Top-down influences on visual processing.

            Re-entrant or feedback pathways between cortical areas carry rich and varied information about behavioural context, including attention, expectation, perceptual tasks, working memory and motor commands. Neurons receiving such inputs effectively function as adaptive processors that are able to assume different functional states according to the task being executed. Recent data suggest that the selection of particular inputs, representing different components of an association field, enable neurons to take on different functional roles. In this Review, we discuss the various top-down influences exerted on the visual cortical pathways and highlight the dynamic nature of the receptive field, which allows neurons to carry information that is relevant to the current perceptual demands.
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              A cortical circuit for gain control by behavioral state.

              The brain's response to sensory input is strikingly modulated by behavioral state. Notably, the visual response of mouse primary visual cortex (V1) is enhanced by locomotion, a tractable and accessible example of a time-locked change in cortical state. The neural circuits that transmit behavioral state to sensory cortex to produce this modulation are unknown. In vivo calcium imaging of behaving animals revealed that locomotion activates vasoactive intestinal peptide (VIP)-positive neurons in mouse V1 independent of visual stimulation and largely through nicotinic inputs from basal forebrain. Optogenetic activation of VIP neurons increased V1 visual responses in stationary awake mice, artificially mimicking the effect of locomotion, and photolytic damage of VIP neurons abolished the enhancement of V1 responses by locomotion. These findings establish a cortical circuit for the enhancement of visual response by locomotion and provide a potential common circuit for the modulation of sensory processing by behavioral state. Copyright © 2014 Elsevier Inc. All rights reserved.
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                Author and article information

                Contributors
                Journal
                Curr Biol
                Curr. Biol
                Current Biology
                Cell Press
                0960-9822
                1879-0445
                18 May 2020
                18 May 2020
                : 30
                : 10
                : 1866-1880.e5
                Affiliations
                [1 ]Center for Behavioral Brain Sciences, Institute of Cognitive Neurology and Dementia Research, Otto-von-Guericke University Magdeburg, Leipziger Str. 44, Magdeburg 39120, Germany
                [2 ]German Center for Neurodegenerative Diseases, Leipziger Str. 44, Magdeburg 39120, Germany
                [3 ]Centre for Discovery Brain Sciences, Edinburgh Medical School: Biomedical Sciences, University of Edinburgh, 15 George Square, Edinburgh, EH8 9XD, UK
                [4 ]Simons Initiative for the Developing Brain, University of Edinburgh, 15 George Square, Edinburgh EH8 9XD, UK
                Author notes
                []Corresponding author janelle.pakan@ 123456med.ovgu.de
                [∗∗ ]Corresponding author n.rochefort@ 123456ed.ac.uk
                [5]

                These authors contributed equally

                [6]

                Lead Contact

                Article
                S0960-9822(20)30356-0
                10.1016/j.cub.2020.03.018
                7237886
                32243857
                580dd711-7dab-4c0f-b67d-500d46da91ed
                © 2020 The Author(s)

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

                History
                : 16 July 2019
                : 7 February 2020
                : 9 March 2020
                Categories
                Article

                Life sciences
                visual cortex,reward,reinforcement learning,orientation selectivity,plasiticy,awake mouse,layer 2/3,locomotion,visuomotor,stimulus discrimination

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