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State transitions through inhibitory interneurons in a cortical network model

Inhibitory interneurons shape the spiking characteristics and computational properties of cortical networks. Interneuron subtypes can precisely regulate cortical function but the roles of interneuron subtypes for promoting different regimes of cortical activity remains unclear. Therefore, we investi...

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Detalles Bibliográficos
Autores principales: Bryson, Alexander, Berkovic, Samuel F., Petrou, Steven, Grayden, David B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8550371/
https://www.ncbi.nlm.nih.gov/pubmed/34653178
http://dx.doi.org/10.1371/journal.pcbi.1009521
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author Bryson, Alexander
Berkovic, Samuel F.
Petrou, Steven
Grayden, David B.
author_facet Bryson, Alexander
Berkovic, Samuel F.
Petrou, Steven
Grayden, David B.
author_sort Bryson, Alexander
collection PubMed
description Inhibitory interneurons shape the spiking characteristics and computational properties of cortical networks. Interneuron subtypes can precisely regulate cortical function but the roles of interneuron subtypes for promoting different regimes of cortical activity remains unclear. Therefore, we investigated the impact of fast spiking and non-fast spiking interneuron subtypes on cortical activity using a network model with connectivity and synaptic properties constrained by experimental data. We found that network properties were more sensitive to modulation of the fast spiking population, with reductions of fast spiking excitability generating strong spike correlations and network oscillations. Paradoxically, reduced fast spiking excitability produced a reduction of global excitation-inhibition balance and features of an inhibition stabilised network, in which firing rates were driven by the activity of excitatory neurons within the network. Further analysis revealed that the synaptic interactions and biophysical features associated with fast spiking interneurons, in particular their rapid intrinsic response properties and short synaptic latency, enabled this state transition by enhancing gain within the excitatory population. Therefore, fast spiking interneurons may be uniquely positioned to control the strength of recurrent excitatory connectivity and the transition to an inhibition stabilised regime. Overall, our results suggest that interneuron subtypes can exert selective control over excitatory gain allowing for differential modulation of global network state.
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spelling pubmed-85503712021-10-28 State transitions through inhibitory interneurons in a cortical network model Bryson, Alexander Berkovic, Samuel F. Petrou, Steven Grayden, David B. PLoS Comput Biol Research Article Inhibitory interneurons shape the spiking characteristics and computational properties of cortical networks. Interneuron subtypes can precisely regulate cortical function but the roles of interneuron subtypes for promoting different regimes of cortical activity remains unclear. Therefore, we investigated the impact of fast spiking and non-fast spiking interneuron subtypes on cortical activity using a network model with connectivity and synaptic properties constrained by experimental data. We found that network properties were more sensitive to modulation of the fast spiking population, with reductions of fast spiking excitability generating strong spike correlations and network oscillations. Paradoxically, reduced fast spiking excitability produced a reduction of global excitation-inhibition balance and features of an inhibition stabilised network, in which firing rates were driven by the activity of excitatory neurons within the network. Further analysis revealed that the synaptic interactions and biophysical features associated with fast spiking interneurons, in particular their rapid intrinsic response properties and short synaptic latency, enabled this state transition by enhancing gain within the excitatory population. Therefore, fast spiking interneurons may be uniquely positioned to control the strength of recurrent excitatory connectivity and the transition to an inhibition stabilised regime. Overall, our results suggest that interneuron subtypes can exert selective control over excitatory gain allowing for differential modulation of global network state. Public Library of Science 2021-10-15 /pmc/articles/PMC8550371/ /pubmed/34653178 http://dx.doi.org/10.1371/journal.pcbi.1009521 Text en © 2021 Bryson et al 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
Bryson, Alexander
Berkovic, Samuel F.
Petrou, Steven
Grayden, David B.
State transitions through inhibitory interneurons in a cortical network model
title State transitions through inhibitory interneurons in a cortical network model
title_full State transitions through inhibitory interneurons in a cortical network model
title_fullStr State transitions through inhibitory interneurons in a cortical network model
title_full_unstemmed State transitions through inhibitory interneurons in a cortical network model
title_short State transitions through inhibitory interneurons in a cortical network model
title_sort state transitions through inhibitory interneurons in a cortical network model
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8550371/
https://www.ncbi.nlm.nih.gov/pubmed/34653178
http://dx.doi.org/10.1371/journal.pcbi.1009521
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