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Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks

Neurons in vitro connect to each other and form neural networks that display emergent electrophysiological activity. This activity begins as spontaneous uncorrelated firing in the early phase of development, and as functional excitatory and inhibitory synapses mature, the activity typically emerges...

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Autores principales: Weir, Janelle Shari, Christiansen, Nicholas, Sandvig, Axel, Sandvig, Ioanna
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9978115/
https://www.ncbi.nlm.nih.gov/pubmed/36874945
http://dx.doi.org/10.3389/fncir.2023.1020487
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author Weir, Janelle Shari
Christiansen, Nicholas
Sandvig, Axel
Sandvig, Ioanna
author_facet Weir, Janelle Shari
Christiansen, Nicholas
Sandvig, Axel
Sandvig, Ioanna
author_sort Weir, Janelle Shari
collection PubMed
description Neurons in vitro connect to each other and form neural networks that display emergent electrophysiological activity. This activity begins as spontaneous uncorrelated firing in the early phase of development, and as functional excitatory and inhibitory synapses mature, the activity typically emerges as spontaneous network bursts. Network bursts are events of coordinated global activation among many neurons interspersed with periods of silencing and are important for synaptic plasticity, neural information processing, and network computation. While bursting is the consequence of balanced excitatory-inhibitory (E/I) interactions, the functional mechanisms underlying their evolution from physiological to potentially pathophysiological states, such as decreasing or increasing in synchrony, are still poorly understood. Synaptic activity, especially that related to maturity of E/I synaptic transmission, is known to strongly influence these processes. In this study, we used selective chemogenetic inhibition to target and disrupt excitatory synaptic transmission in in vitro neural networks to study functional response and recovery of spontaneous network bursts over time. We found that over time, inhibition resulted in increases in both network burstiness and synchrony. Our results indicate that the disruption in excitatory synaptic transmission during early network development likely affected inhibitory synaptic maturity which resulted in an overall decrease in network inhibition at later stages. These findings lend support to the importance of E/I balance in maintaining physiological bursting dynamics and, conceivably, information processing capacity in neural networks.
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spelling pubmed-99781152023-03-03 Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks Weir, Janelle Shari Christiansen, Nicholas Sandvig, Axel Sandvig, Ioanna Front Neural Circuits Neural Circuits Neurons in vitro connect to each other and form neural networks that display emergent electrophysiological activity. This activity begins as spontaneous uncorrelated firing in the early phase of development, and as functional excitatory and inhibitory synapses mature, the activity typically emerges as spontaneous network bursts. Network bursts are events of coordinated global activation among many neurons interspersed with periods of silencing and are important for synaptic plasticity, neural information processing, and network computation. While bursting is the consequence of balanced excitatory-inhibitory (E/I) interactions, the functional mechanisms underlying their evolution from physiological to potentially pathophysiological states, such as decreasing or increasing in synchrony, are still poorly understood. Synaptic activity, especially that related to maturity of E/I synaptic transmission, is known to strongly influence these processes. In this study, we used selective chemogenetic inhibition to target and disrupt excitatory synaptic transmission in in vitro neural networks to study functional response and recovery of spontaneous network bursts over time. We found that over time, inhibition resulted in increases in both network burstiness and synchrony. Our results indicate that the disruption in excitatory synaptic transmission during early network development likely affected inhibitory synaptic maturity which resulted in an overall decrease in network inhibition at later stages. These findings lend support to the importance of E/I balance in maintaining physiological bursting dynamics and, conceivably, information processing capacity in neural networks. Frontiers Media S.A. 2023-02-16 /pmc/articles/PMC9978115/ /pubmed/36874945 http://dx.doi.org/10.3389/fncir.2023.1020487 Text en Copyright © 2023 Weir, Christiansen, Sandvig and Sandvig. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neural Circuits
Weir, Janelle Shari
Christiansen, Nicholas
Sandvig, Axel
Sandvig, Ioanna
Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks
title Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks
title_full Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks
title_fullStr Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks
title_full_unstemmed Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks
title_short Selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks
title_sort selective inhibition of excitatory synaptic transmission alters the emergent bursting dynamics of in vitro neural networks
topic Neural Circuits
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9978115/
https://www.ncbi.nlm.nih.gov/pubmed/36874945
http://dx.doi.org/10.3389/fncir.2023.1020487
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