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      Balanced networks under spike-time dependent plasticity

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          Abstract

          The dynamics of local cortical networks are irregular, but correlated. Dynamic excitatory–inhibitory balance is a plausible mechanism that generates such irregular activity, but it remains unclear how balance is achieved and maintained in plastic neural networks. In particular, it is not fully understood how plasticity induced changes in the network affect balance, and in turn, how correlated, balanced activity impacts learning. How do the dynamics of balanced networks change under different plasticity rules? How does correlated spiking activity in recurrent networks change the evolution of weights, their eventual magnitude, and structure across the network? To address these questions, we develop a theory of spike–timing dependent plasticity in balanced networks. We show that balance can be attained and maintained under plasticity–induced weight changes. We find that correlations in the input mildly affect the evolution of synaptic weights. Under certain plasticity rules, we find an emergence of correlations between firing rates and synaptic weights. Under these rules, synaptic weights converge to a stable manifold in weight space with their final configuration dependent on the initial state of the network. Lastly, we show that our framework can also describe the dynamics of plastic balanced networks when subsets of neurons receive targeted optogenetic input.

          Author Summary

          Animals are able to learn complex tasks through changes in individual synapses between cells. Such changes lead to the coevolution of neural activity patterns and the structure of neural connectivity, but the consequences of these interactions are not fully understood. We consider plasticity in model neural networks which achieve an average balance between the excitatory and inhibitory synaptic inputs to different cells, and display cortical–like, irregular activity. We extend the theory of balanced networks to account for synaptic plasticity and show which rules can maintain balance, and which will drive the network into a different state. This theory of plasticity can provide insights into the relationship between stimuli, network dynamics, and synaptic circuitry.

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          Most cited references107

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          Neocortical excitation/inhibition balance in information processing and social dysfunction.

          Severe behavioural deficits in psychiatric diseases such as autism and schizophrenia have been hypothesized to arise from elevations in the cellular balance of excitation and inhibition (E/I balance) within neural microcircuitry. This hypothesis could unify diverse streams of pathophysiological and genetic evidence, but has not been susceptible to direct testing. Here we design and use several novel optogenetic tools to causally investigate the cellular E/I balance hypothesis in freely moving mammals, and explore the associated circuit physiology. Elevation, but not reduction, of cellular E/I balance within the mouse medial prefrontal cortex was found to elicit a profound impairment in cellular information processing, associated with specific behavioural impairments and increased high-frequency power in the 30-80 Hz range, which have both been observed in clinical conditions in humans. Consistent with the E/I balance hypothesis, compensatory elevation of inhibitory cell excitability partially rescued social deficits caused by E/I balance elevation. These results provide support for the elevated cellular E/I balance hypothesis of severe neuropsychiatric disease-related symptoms.
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            Millisecond-timescale, genetically targeted optical control of neural activity.

            Temporally precise, noninvasive control of activity in well-defined neuronal populations is a long-sought goal of systems neuroscience. We adapted for this purpose the naturally occurring algal protein Channelrhodopsin-2, a rapidly gated light-sensitive cation channel, by using lentiviral gene delivery in combination with high-speed optical switching to photostimulate mammalian neurons. We demonstrate reliable, millisecond-timescale control of neuronal spiking, as well as control of excitatory and inhibitory synaptic transmission. This technology allows the use of light to alter neural processing at the level of single spikes and synaptic events, yielding a widely applicable tool for neuroscientists and biomedical engineers.
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              The self-organizing map

              T Kohonen (1990)
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: SoftwareRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, CA USA )
                1553-734X
                1553-7358
                May 2021
                12 May 2021
                : 17
                : 5
                : e1008958
                Affiliations
                [1 ] Department of Mathematics, University of Houston, Houston, Texas, United States of America
                [2 ] Department of Applied and Computational Mathematics and Statistics, University of Notre Dame, Notre Dame, Indiana, United States of America
                [3 ] Interdisciplinary Center for Network Science and Applications, University of Notre Dame, Notre Dame, Indiana, United States of America
                [4 ] Department of Biology and Biochemistry, University of Houston, Houston, Texas, United States of America
                Max-Planck-Institut fur Brain Research, GERMANY
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                https://orcid.org/0000-0003-4862-4771
                https://orcid.org/0000-0003-2105-9282
                https://orcid.org/0000-0002-1975-3913
                Article
                PCOMPBIOL-D-20-00683
                10.1371/journal.pcbi.1008958
                8143429
                33979336
                8b19ce43-9e9f-49ce-b025-e48baacf1f01
                © 2021 Akil 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
                : 25 April 2020
                : 12 April 2021
                Page count
                Figures: 4, Tables: 1, Pages: 23
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: 1R01MH115557
                Award Recipient :
                Funded by: National Science Foundation
                Award ID: DMS-1654268
                Award Recipient :
                Funded by: National Science Foundation (US)
                Award ID: DBI-1707400
                Award Recipient :
                Funded by: National Science Foundation (US)
                Award ID: DBI-1707400
                Award Recipient :
                Funded by: National Science Foundation (US)
                Award ID: DBI-1707400
                Award Recipient :
                Funding was provided by grants NIH-1R01MH115557 (KJ), NSF DMS-1654268 (RR) and DBI-1707400 465 (AA, RR, and KJ). National Institutes of Health - https://www.nih.gov National Science Foundation - https://nsf.gov. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Neurons
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Neurons
                Biology and Life Sciences
                Physiology
                Electrophysiology
                Membrane Potential
                Action Potentials
                Biology and Life Sciences
                Physiology
                Electrophysiology
                Neurophysiology
                Action Potentials
                Biology and Life Sciences
                Neuroscience
                Neurophysiology
                Action Potentials
                Biology and Life Sciences
                Neuroscience
                Cellular Neuroscience
                Synaptic Plasticity
                Biology and Life Sciences
                Neuroscience
                Developmental Neuroscience
                Synaptic Plasticity
                Computer and Information Sciences
                Neural Networks
                Biology and Life Sciences
                Neuroscience
                Neural Networks
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                Neuroscience
                Cellular Neuroscience
                Neuronal Plasticity
                Biology and Life Sciences
                Anatomy
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                Synapses
                Medicine and Health Sciences
                Anatomy
                Nervous System
                Synapses
                Biology and Life Sciences
                Physiology
                Electrophysiology
                Neurophysiology
                Synapses
                Biology and Life Sciences
                Neuroscience
                Neurophysiology
                Synapses
                Biology and Life Sciences
                Physiology
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                Homeostasis
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
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                Custom metadata
                vor-update-to-uncorrected-proof
                2021-05-24
                There is no data per se, but all code is available at https://github.com/alanakil/PlasticBalancedNetsPackage.

                Quantitative & Systems biology
                Quantitative & Systems biology

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