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      Sleep-like slow oscillations improve visual classification through synaptic homeostasis and memory association in a thalamo-cortical model

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          Abstract

          The occurrence of sleep passed through the evolutionary sieve and is widespread in animal species. Sleep is known to be beneficial to cognitive and mnemonic tasks, while chronic sleep deprivation is detrimental. Despite the importance of the phenomenon, a complete understanding of its functions and underlying mechanisms is still lacking. In this paper, we show interesting effects of deep-sleep-like slow oscillation activity on a simplified thalamo-cortical model which is trained to encode, retrieve and classify images of handwritten digits. During slow oscillations, spike-timing-dependent-plasticity (STDP) produces a differential homeostatic process. It is characterized by both a specific unsupervised enhancement of connections among groups of neurons associated to instances of the same class (digit) and a simultaneous down-regulation of stronger synapses created by the training. This hierarchical organization of post-sleep internal representations favours higher performances in retrieval and classification tasks. The mechanism is based on the interaction between top-down cortico-thalamic predictions and bottom-up thalamo-cortical projections during deep-sleep-like slow oscillations. Indeed, when learned patterns are replayed during sleep, cortico-thalamo-cortical connections favour the activation of other neurons coding for similar thalamic inputs, promoting their association. Such mechanism hints at possible applications to artificial learning systems.

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          Most cited references24

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          Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration.

          Sleep is universal, tightly regulated, and its loss impairs cognition. But why does the brain need to disconnect from the environment for hours every day? The synaptic homeostasis hypothesis (SHY) proposes that sleep is the price the brain pays for plasticity. During a waking episode, learning statistical regularities about the current environment requires strengthening connections throughout the brain. This increases cellular needs for energy and supplies, decreases signal-to-noise ratios, and saturates learning. During sleep, spontaneous activity renormalizes net synaptic strength and restores cellular homeostasis. Activity-dependent down-selection of synapses can also explain the benefits of sleep on memory acquisition, consolidation, and integration. This happens through the offline, comprehensive sampling of statistical regularities incorporated in neuronal circuits over a lifetime. This Perspective considers the rationale and evidence for SHY and points to open issues related to sleep and plasticity. Copyright © 2014 Elsevier Inc. All rights reserved.
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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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              Awake hippocampal sharp-wave ripples support spatial memory.

              The hippocampus is critical for spatial learning and memory. Hippocampal neurons in awake animals exhibit place field activity that encodes current location, as well as sharp-wave ripple (SWR) activity during which representations based on past experiences are often replayed. The relationship between these patterns of activity and the memory functions of the hippocampus is poorly understood. We interrupted awake SWRs in animals learning a spatial alternation task. We observed a specific learning and performance deficit that persisted throughout training. This deficit was associated with awake SWR activity, as SWR interruption left place field activity and post-experience SWR reactivation intact. These results provide a link between awake SWRs and hippocampal memory processes, which suggests that awake replay of memory-related information during SWRs supports learning and memory-guided decision-making.
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                Author and article information

                Contributors
                cristiano.capone@roma1.infn.it
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                20 June 2019
                20 June 2019
                2019
                : 9
                : 8990
                Affiliations
                [1 ]GRID grid.470218.8, INFN Sezione di Roma, ; Rome, Italy
                [2 ]GRID grid.7841.a, PhD Program in Behavioural Neuroscience, “Sapienza” University of Rome, ; Rome, Italy
                [3 ]ISNI 0000 0004 1755 3242, GRID grid.7763.5, Dipartimento di Fisica, Università di Cagliari, ; Cagliari, Italy
                [4 ]GRID grid.470195.e, INFN Sezione di Cagliari, ; Cagliari, Italy
                Author information
                http://orcid.org/0000-0001-5144-6932
                http://orcid.org/0000-0003-1937-6086
                Article
                45525
                10.1038/s41598-019-45525-0
                6586839
                31222151
                ff6fb2aa-3c0d-473e-a49d-fa0c55144b17
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 24 January 2019
                : 3 June 2019
                Categories
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                Custom metadata
                © The Author(s) 2019

                Uncategorized
                consolidation,network models,sleep,learning algorithms
                Uncategorized
                consolidation, network models, sleep, learning algorithms

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