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      Thalamo-cortical spiking model of incremental learning combining perception, context and NREM-sleep

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          Abstract

          The brain exhibits capabilities of fast incremental learning from few noisy examples, as well as the ability to associate similar memories in autonomously-created categories and to combine contextual hints with sensory perceptions. Together with sleep, these mechanisms are thought to be key components of many high-level cognitive functions. Yet, little is known about the underlying processes and the specific roles of different brain states. In this work, we exploited the combination of context and perception in a thalamo-cortical model based on a soft winner-take-all circuit of excitatory and inhibitory spiking neurons. After calibrating this model to express awake and deep-sleep states with features comparable with biological measures, we demonstrate the model capability of fast incremental learning from few examples, its resilience when proposed with noisy perceptions and contextual signals, and an improvement in visual classification after sleep due to induced synaptic homeostasis and association of similar memories.

          Author summary

          We created a thalamo-cortical spiking model (ThaCo) with the purpose of demonstrating a link among two phenomena that we believe to be essential for the brain capability of efficient incremental learning from few examples in noisy environments. Grounded in two experimental observations—the first about the effects of deep-sleep on pre- and post-sleep firing rate distributions, the second about the combination of perceptual and contextual information in pyramidal neurons—our model joins these two ingredients. ThaCo alternates phases of incremental learning, classification and deep-sleep. Memories of handwritten digit examples are learned through thalamo-cortical and cortico-cortical plastic synapses. In absence of noise, the combination of contextual information with perception enables fast incremental learning. Deep-sleep becomes crucial when noisy inputs are considered. We observed in ThaCo both homeostatic and associative processes: deep-sleep fights noise in perceptual and internal knowledge and it supports the categorical association of examples belonging to the same digit class, through reinforcement of class-specific cortico-cortical synapses. The distributions of pre-sleep and post-sleep firing rates during classification change in a manner similar to those of experimental observation. These changes promote energetic efficiency during recall of memories, better representation of individual memories and categories and higher classification performances.

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          Nearest neighbor pattern classification

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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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              Competitive Hebbian learning through spike-timing-dependent synaptic plasticity.

              Hebbian models of development and learning require both activity-dependent synaptic plasticity and a mechanism that induces competition between different synapses. One form of experimentally observed long-term synaptic plasticity, which we call spike-timing-dependent plasticity (STDP), depends on the relative timing of pre- and postsynaptic action potentials. In modeling studies, we find that this form of synaptic modification can automatically balance synaptic strengths to make postsynaptic firing irregular but more sensitive to presynaptic spike timing. It has been argued that neurons in vivo operate in such a balanced regime. Synapses modifiable by STDP compete for control of the timing of postsynaptic action potentials. Inputs that fire the postsynaptic neuron with short latency or that act in correlated groups are able to compete most successfully and develop strong synapses, while synapses of longer-latency or less-effective inputs are weakened.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draft
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: Methodology
                Role: InvestigationRole: Software
                Role: Formal analysisRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput Biol
                plos
                PLoS Computational Biology
                Public Library of Science (San Francisco, CA USA )
                1553-734X
                1553-7358
                June 2021
                28 June 2021
                : 17
                : 6
                : e1009045
                Affiliations
                [1 ] Dipartimento di Fisica, Università di Cagliari, Cagliari, Italy
                [2 ] Istituto Nazionale di Fisica Nucleare (INFN), Sezione di Cagliari, Cagliari, Italy
                [3 ] Ph.D. Program in Behavioural Neuroscience, “Sapienza” Università di Roma, Rome, Italy
                [4 ] Istituto Nazionale di Fisica Nucleare (INFN), Sezione di Roma, Rome, Italy
                [5 ] Dipartimento di Chimica e Farmacia, Università di Sassari, Sassari, Italy
                University of California San Diego, UNITED STATES
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0001-5144-6932
                https://orcid.org/0000-0003-3488-0088
                https://orcid.org/0000-0002-9958-2551
                https://orcid.org/0000-0003-0682-1232
                https://orcid.org/0000-0002-7378-2328
                https://orcid.org/0000-0001-7524-0285
                https://orcid.org/0000-0001-7079-5724
                https://orcid.org/0000-0003-1937-6086
                Article
                PCOMPBIOL-D-20-00684
                10.1371/journal.pcbi.1009045
                8270441
                34181642
                0376b742-b223-44a9-a904-f41a3ba2c3ba
                © 2021 Golosio et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 27 April 2020
                : 5 May 2021
                Page count
                Figures: 7, Tables: 1, Pages: 26
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100010661, Horizon 2020 Framework Programme;
                Award ID: 945539
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100010661, Horizon 2020 Framework Programme;
                Award ID: 785907
                Award Recipient :
                Funded by: INFN APE Parallel/Distributed Computing laboratory
                This work has been supported by the European Union Horizon 2020 Research and Innovation program under the FET Flagship Human Brain Project (grant agreement SGA3 n. 945539 and grant agreement SGA2 n. 785907; recipient Pier Stanislao Paolucci) and by the INFN APE Parallel/Distributed Computing laboratory. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
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                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
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                Biology and Life Sciences
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                Custom metadata
                vor-update-to-uncorrected-proof
                2021-07-09
                The model and data used to draw the results outlined in this manuscript are available at https://github.com/APE-group/ThaCo2.git and 10.5281/zenodo.4769175.

                Quantitative & Systems biology
                Quantitative & Systems biology

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