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      Learning Enhances Sensory and Multiple Non-sensory Representations in Primary Visual Cortex

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          Summary

          We determined how learning modifies neural representations in primary visual cortex (V1) during acquisition of a visually guided behavioral task. We imaged the activity of the same layer 2/3 neuronal populations as mice learned to discriminate two visual patterns while running through a virtual corridor, where one pattern was rewarded. Improvements in behavioral performance were closely associated with increasingly distinguishable population-level representations of task-relevant stimuli, as a result of stabilization of existing and recruitment of new neurons selective for these stimuli. These effects correlated with the appearance of multiple task-dependent signals during learning: those that increased neuronal selectivity across the population when expert animals engaged in the task, and those reflecting anticipation or behavioral choices specifically in neuronal subsets preferring the rewarded stimulus. Therefore, learning engages diverse mechanisms that modify sensory and non-sensory representations in V1 to adjust its processing to task requirements and the behavioral relevance of visual stimuli.

          Highlights

          • V1 neurons increasingly discriminate task-relevant stimuli with learning

          • Chronic imaging reveals single cell changes underlying this population effect

          • Learning-related changes are reduced when animals ignore task-relevant stimuli

          • Anticipatory and behavioral choice-related signals emerge in reward-predicting cells

          Abstract

          By tracking the same visual cortex neurons across days, Poort et al. demonstrate how learning a visual task leads to increasingly distinguishable representations of relevant stimuli. These changes parallel the emergence of diverse non-sensory signals in specific neuronal subsets.

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          Most cited references31

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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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            Imaging large-scale neural activity with cellular resolution in awake, mobile mice.

            We report a technique for two-photon fluorescence imaging with cellular resolution in awake, behaving mice with minimal motion artifact. The apparatus combines an upright, table-mounted two-photon microscope with a spherical treadmill consisting of a large, air-supported Styrofoam ball. Mice, with implanted cranial windows, are head restrained under the objective while their limbs rest on the ball's upper surface. Following adaptation to head restraint, mice maneuver on the spherical treadmill as their heads remain motionless. Image sequences demonstrate that running-associated brain motion is limited to approximately 2-5 microm. In addition, motion is predominantly in the focal plane, with little out-of-plane motion, making the application of a custom-designed Hidden-Markov-Model-based motion correction algorithm useful for postprocessing. Behaviorally correlated calcium transients from large neuronal and astrocytic populations were routinely measured, with an estimated motion-induced false positive error rate of <5%.
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              Selective attention. Long-range and local circuits for top-down modulation of visual cortex processing.

              Top-down modulation of sensory processing allows the animal to select inputs most relevant to current tasks. We found that the cingulate (Cg) region of the mouse frontal cortex powerfully influences sensory processing in the primary visual cortex (V1) through long-range projections that activate local γ-aminobutyric acid-ergic (GABAergic) circuits. Optogenetic activation of Cg neurons enhanced V1 neuron responses and improved visual discrimination. Focal activation of Cg axons in V1 caused a response increase at the activation site but a decrease at nearby locations (center-surround modulation). Whereas somatostatin-positive GABAergic interneurons contributed preferentially to surround suppression, vasoactive intestinal peptide-positive interneurons were crucial for center facilitation. Long-range corticocortical projections thus act through local microcircuits to exert spatially specific top-down modulation of sensory processing. Copyright © 2014, American Association for the Advancement of Science.
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                Author and article information

                Contributors
                Journal
                Neuron
                Neuron
                Neuron
                Cell Press
                0896-6273
                1097-4199
                17 June 2015
                17 June 2015
                : 86
                : 6
                : 1478-1490
                Affiliations
                [1 ]Biozentrum, University of Basel, Klingelbergstrasse 50/70, 4056 Basel, Switzerland
                [2 ]University College London, 21 University Street, London WC1E 6DE, UK
                [3 ]Gatsby Computational Neuroscience Unit, University College London, 17 Queen Square, London WC1N 3AR, UK
                [4 ]Friedrich Miescher Institute for Biomedical Research, Maulbeerstrasse 66, 4058 Basel, Switzerland
                Author notes
                []Corresponding author sonja.hofer@ 123456unibas.ch
                [5]

                Co-first author

                Article
                S0896-6273(15)00476-6
                10.1016/j.neuron.2015.05.037
                4503798
                26051421
                bc218fd1-7c5f-4f9d-89b6-23752e649499
                © 2015 The Authors

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

                History
                : 8 December 2014
                : 7 March 2015
                : 29 April 2015
                Categories
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                Neurosciences
                Neurosciences

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