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      Distinct learning-induced changes in stimulus selectivity and interactions of GABAergic interneuron classes in visual cortex

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          Abstract

          <p id="P1">Learning increases the selectivity of cortical representations for behaviorally relevant stimuli, but how this occurs through changes in activity of different cell types remains unclear. We imaged simultaneously responses of pyramidal cells (PYR), and parvalbumin (PV), somatostatin (SOM), and vasoactive intestinal peptide (VIP) inhibitory interneurons in primary visual cortex while mice learned to discriminate two visual patterns. Learning increased the selectivity for both stimuli in subsets of PYR, PV and SOM cells but not VIP cells. Strikingly, PV neurons became as selective as PYR cells and less correlated with stimulus preference of the local network. A linear dynamical system model revealed that PYR to PV interactions reorganized such that stimulus selective PYR-PV subnetworks emerged during learning. In contrast, SOM cells became decorrelated from the local network and may gate selectivity changes. Thus, learning shapes the activity and interactions of multiple cell classes as the network becomes more selective for processing of behaviorally relevant stimuli. </p>

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          Most cited references36

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          Interneurons of the neocortical inhibitory system.

          Mammals adapt to a rapidly changing world because of the sophisticated cognitive functions that are supported by the neocortex. The neocortex, which forms almost 80% of the human brain, seems to have arisen from repeated duplication of a stereotypical microcircuit template with subtle specializations for different brain regions and species. The quest to unravel the blueprint of this template started more than a century ago and has revealed an immensely intricate design. The largest obstacle is the daunting variety of inhibitory interneurons that are found in the circuit. This review focuses on the organizing principles that govern the diversity of inhibitory interneurons and their circuits.
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            Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons.

            An understanding of the diversity of cortical GABAergic interneurons is critical to understand the function of the cerebral cortex. Recent data suggest that neurons expressing three markers, the Ca2+-binding protein parvalbumin (PV), the neuropeptide somatostatin (SST), and the ionotropic serotonin receptor 5HT3a (5HT3aR) account for nearly 100% of neocortical interneurons. Interneurons expressing each of these markers have a different embryological origin. Each group includes several types of interneurons that differ in morphological and electrophysiological properties and likely have different functions in the cortical circuit. The PV group accounts for ∼40% of GABAergic neurons and includes fast spiking basket cells and chandelier cells. The SST group, which represents ∼30% of GABAergic neurons, includes the Martinotti cells and a set of neurons that specifically target layerIV. The 5HT3aR group, which also accounts for ∼30% of the total interneuronal population, is heterogeneous and includes all of the neurons that express the neuropeptide VIP, as well as an equally numerous subgroup of neurons that do not express VIP and includes neurogliaform cells. The universal modulation of these neurons by serotonin and acetylcholine via ionotropic receptors suggests that they might be involved in shaping cortical circuits during specific brain states and behavioral contexts. Copyright © 2010 Wiley Periodicals, Inc.
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              Interneuron cell types are fit to function.

              Understanding brain circuits begins with an appreciation of their component parts - the cells. Although GABAergic interneurons are a minority population within the brain, they are crucial for the control of inhibition. Determining the diversity of these interneurons has been a central goal of neurobiologists, but this amazing cell type has so far defied a generalized classification system. Interneuron complexity within the telencephalon could be simplified by viewing them as elaborations of a much more finite group of developmentally specified cardinal classes that become further specialized as they mature. Our perspective emphasizes that the ultimate goal is to dispense with classification criteria and directly define interneuron types by function.
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                Author and article information

                Journal
                Nature Neuroscience
                Nat Neurosci
                Springer Nature
                1097-6256
                1546-1726
                May 21 2018
                Article
                10.1038/s41593-018-0143-z
                6390950
                29786081
                18b38334-a1fd-48da-aa0f-47f3d78b3a2b
                © 2018

                http://www.springer.com/tdm

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