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Optimizing interneuron circuits for compartment-specific feedback inhibition

Cortical circuits process information by rich recurrent interactions between excitatory neurons and inhibitory interneurons. One of the prime functions of interneurons is to stabilize the circuit by feedback inhibition, but the level of specificity on which inhibitory feedback operates is not fully...

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Detalles Bibliográficos
Autores principales: Keijser, Joram, Sprekeler, Henning
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9049365/
https://www.ncbi.nlm.nih.gov/pubmed/35482670
http://dx.doi.org/10.1371/journal.pcbi.1009933
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author Keijser, Joram
Sprekeler, Henning
author_facet Keijser, Joram
Sprekeler, Henning
author_sort Keijser, Joram
collection PubMed
description Cortical circuits process information by rich recurrent interactions between excitatory neurons and inhibitory interneurons. One of the prime functions of interneurons is to stabilize the circuit by feedback inhibition, but the level of specificity on which inhibitory feedback operates is not fully resolved. We hypothesized that inhibitory circuits could enable separate feedback control loops for different synaptic input streams, by means of specific feedback inhibition to different neuronal compartments. To investigate this hypothesis, we adopted an optimization approach. Leveraging recent advances in training spiking network models, we optimized the connectivity and short-term plasticity of interneuron circuits for compartment-specific feedback inhibition onto pyramidal neurons. Over the course of the optimization, the interneurons diversified into two classes that resembled parvalbumin (PV) and somatostatin (SST) expressing interneurons. Using simulations and mathematical analyses, we show that the resulting circuit can be understood as a neural decoder that inverts the nonlinear biophysical computations performed within the pyramidal cells. Our model provides a proof of concept for studying structure-function relations in cortical circuits by a combination of gradient-based optimization and biologically plausible phenomenological models.
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spelling pubmed-90493652022-04-29 Optimizing interneuron circuits for compartment-specific feedback inhibition Keijser, Joram Sprekeler, Henning PLoS Comput Biol Research Article Cortical circuits process information by rich recurrent interactions between excitatory neurons and inhibitory interneurons. One of the prime functions of interneurons is to stabilize the circuit by feedback inhibition, but the level of specificity on which inhibitory feedback operates is not fully resolved. We hypothesized that inhibitory circuits could enable separate feedback control loops for different synaptic input streams, by means of specific feedback inhibition to different neuronal compartments. To investigate this hypothesis, we adopted an optimization approach. Leveraging recent advances in training spiking network models, we optimized the connectivity and short-term plasticity of interneuron circuits for compartment-specific feedback inhibition onto pyramidal neurons. Over the course of the optimization, the interneurons diversified into two classes that resembled parvalbumin (PV) and somatostatin (SST) expressing interneurons. Using simulations and mathematical analyses, we show that the resulting circuit can be understood as a neural decoder that inverts the nonlinear biophysical computations performed within the pyramidal cells. Our model provides a proof of concept for studying structure-function relations in cortical circuits by a combination of gradient-based optimization and biologically plausible phenomenological models. Public Library of Science 2022-04-28 /pmc/articles/PMC9049365/ /pubmed/35482670 http://dx.doi.org/10.1371/journal.pcbi.1009933 Text en © 2022 Keijser, Sprekeler https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Keijser, Joram
Sprekeler, Henning
Optimizing interneuron circuits for compartment-specific feedback inhibition
title Optimizing interneuron circuits for compartment-specific feedback inhibition
title_full Optimizing interneuron circuits for compartment-specific feedback inhibition
title_fullStr Optimizing interneuron circuits for compartment-specific feedback inhibition
title_full_unstemmed Optimizing interneuron circuits for compartment-specific feedback inhibition
title_short Optimizing interneuron circuits for compartment-specific feedback inhibition
title_sort optimizing interneuron circuits for compartment-specific feedback inhibition
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9049365/
https://www.ncbi.nlm.nih.gov/pubmed/35482670
http://dx.doi.org/10.1371/journal.pcbi.1009933
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