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Heterogeneous mechanisms for synchronization of networks of resonant neurons under different E/I balance regimes

Rhythmic synchronization of neuronal firing patterns is a widely present phenomenon in the brain—one that seems to be essential for many cognitive processes. A variety of mechanisms contribute to generation and synchronization of network oscillations, ranging from intrinsic cellular excitability to...

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Autores principales: Wu, Jiaxing, Aton, Sara J., Booth, Victoria, Zochowski, Michal
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10013004/
https://www.ncbi.nlm.nih.gov/pubmed/36926113
http://dx.doi.org/10.3389/fnetp.2022.975951
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author Wu, Jiaxing
Aton, Sara J.
Booth, Victoria
Zochowski, Michal
author_facet Wu, Jiaxing
Aton, Sara J.
Booth, Victoria
Zochowski, Michal
author_sort Wu, Jiaxing
collection PubMed
description Rhythmic synchronization of neuronal firing patterns is a widely present phenomenon in the brain—one that seems to be essential for many cognitive processes. A variety of mechanisms contribute to generation and synchronization of network oscillations, ranging from intrinsic cellular excitability to network mediated effects. However, it is unclear how these mechanisms interact together. Here, using computational modeling of excitatory-inhibitory neural networks, we show that different synchronization mechanisms dominate network dynamics at different levels of excitation and inhibition (i.e. E/I levels) as synaptic strength is systematically varied. Our results show that with low synaptic strength networks are sensitive to external oscillatory drive as a synchronizing mechanism—a hallmark of resonance. In contrast, in a strongly-connected regime, synchronization is driven by network effects via the direct interaction between excitation and inhibition, and spontaneous oscillations and cross-frequency coupling emerge. Unexpectedly, we find that while excitation dominates network synchrony at low excitatory coupling strengths, inhibition dominates at high excitatory coupling strengths. Together, our results provide novel insights into the oscillatory modulation of firing patterns in different excitation/inhibition regimes.
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spelling pubmed-100130042023-03-15 Heterogeneous mechanisms for synchronization of networks of resonant neurons under different E/I balance regimes Wu, Jiaxing Aton, Sara J. Booth, Victoria Zochowski, Michal Front Netw Physiol Network Physiology Rhythmic synchronization of neuronal firing patterns is a widely present phenomenon in the brain—one that seems to be essential for many cognitive processes. A variety of mechanisms contribute to generation and synchronization of network oscillations, ranging from intrinsic cellular excitability to network mediated effects. However, it is unclear how these mechanisms interact together. Here, using computational modeling of excitatory-inhibitory neural networks, we show that different synchronization mechanisms dominate network dynamics at different levels of excitation and inhibition (i.e. E/I levels) as synaptic strength is systematically varied. Our results show that with low synaptic strength networks are sensitive to external oscillatory drive as a synchronizing mechanism—a hallmark of resonance. In contrast, in a strongly-connected regime, synchronization is driven by network effects via the direct interaction between excitation and inhibition, and spontaneous oscillations and cross-frequency coupling emerge. Unexpectedly, we find that while excitation dominates network synchrony at low excitatory coupling strengths, inhibition dominates at high excitatory coupling strengths. Together, our results provide novel insights into the oscillatory modulation of firing patterns in different excitation/inhibition regimes. Frontiers Media S.A. 2022-09-30 /pmc/articles/PMC10013004/ /pubmed/36926113 http://dx.doi.org/10.3389/fnetp.2022.975951 Text en Copyright © 2022 Wu, Aton, Booth and Zochowski. 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 Network Physiology
Wu, Jiaxing
Aton, Sara J.
Booth, Victoria
Zochowski, Michal
Heterogeneous mechanisms for synchronization of networks of resonant neurons under different E/I balance regimes
title Heterogeneous mechanisms for synchronization of networks of resonant neurons under different E/I balance regimes
title_full Heterogeneous mechanisms for synchronization of networks of resonant neurons under different E/I balance regimes
title_fullStr Heterogeneous mechanisms for synchronization of networks of resonant neurons under different E/I balance regimes
title_full_unstemmed Heterogeneous mechanisms for synchronization of networks of resonant neurons under different E/I balance regimes
title_short Heterogeneous mechanisms for synchronization of networks of resonant neurons under different E/I balance regimes
title_sort heterogeneous mechanisms for synchronization of networks of resonant neurons under different e/i balance regimes
topic Network Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10013004/
https://www.ncbi.nlm.nih.gov/pubmed/36926113
http://dx.doi.org/10.3389/fnetp.2022.975951
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