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Asynchronous and Coherent Dynamics in Balanced Excitatory-Inhibitory Spiking Networks

Dynamic excitatory-inhibitory (E-I) balance is a paradigmatic mechanism invoked to explain the irregular low firing activity observed in the cortex. However, we will show that the E-I balance can be at the origin of other regimes observable in the brain. The analysis is performed by combining extens...

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Autores principales: Bi, Hongjie, di Volo, Matteo, Torcini, Alessandro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8702645/
https://www.ncbi.nlm.nih.gov/pubmed/34955768
http://dx.doi.org/10.3389/fnsys.2021.752261
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author Bi, Hongjie
di Volo, Matteo
Torcini, Alessandro
author_facet Bi, Hongjie
di Volo, Matteo
Torcini, Alessandro
author_sort Bi, Hongjie
collection PubMed
description Dynamic excitatory-inhibitory (E-I) balance is a paradigmatic mechanism invoked to explain the irregular low firing activity observed in the cortex. However, we will show that the E-I balance can be at the origin of other regimes observable in the brain. The analysis is performed by combining extensive simulations of sparse E-I networks composed of N spiking neurons with analytical investigations of low dimensional neural mass models. The bifurcation diagrams, derived for the neural mass model, allow us to classify the possible asynchronous and coherent behaviors emerging in balanced E-I networks with structural heterogeneity for any finite in-degree K. Analytic mean-field (MF) results show that both supra and sub-threshold balanced asynchronous regimes are observable in our system in the limit N >> K >> 1. Due to the heterogeneity, the asynchronous states are characterized at the microscopic level by the splitting of the neurons in to three groups: silent, fluctuation, and mean driven. These features are consistent with experimental observations reported for heterogeneous neural circuits. The coherent rhythms observed in our system can range from periodic and quasi-periodic collective oscillations (COs) to coherent chaos. These rhythms are characterized by regular or irregular temporal fluctuations joined to spatial coherence somehow similar to coherent fluctuations observed in the cortex over multiple spatial scales. The COs can emerge due to two different mechanisms. A first mechanism analogous to the pyramidal-interneuron gamma (PING), usually invoked for the emergence of γ-oscillations. The second mechanism is intimately related to the presence of current fluctuations, which sustain COs characterized by an essentially simultaneous bursting of the two populations. We observe period-doubling cascades involving the PING-like COs finally leading to the appearance of coherent chaos. Fluctuation driven COs are usually observable in our system as quasi-periodic collective motions characterized by two incommensurate frequencies. However, for sufficiently strong current fluctuations these collective rhythms can lock. This represents a novel mechanism of frequency locking in neural populations promoted by intrinsic fluctuations. COs are observable for any finite in-degree K, however, their existence in the limit N >> K >> 1 appears as uncertain.
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spelling pubmed-87026452021-12-25 Asynchronous and Coherent Dynamics in Balanced Excitatory-Inhibitory Spiking Networks Bi, Hongjie di Volo, Matteo Torcini, Alessandro Front Syst Neurosci Neuroscience Dynamic excitatory-inhibitory (E-I) balance is a paradigmatic mechanism invoked to explain the irregular low firing activity observed in the cortex. However, we will show that the E-I balance can be at the origin of other regimes observable in the brain. The analysis is performed by combining extensive simulations of sparse E-I networks composed of N spiking neurons with analytical investigations of low dimensional neural mass models. The bifurcation diagrams, derived for the neural mass model, allow us to classify the possible asynchronous and coherent behaviors emerging in balanced E-I networks with structural heterogeneity for any finite in-degree K. Analytic mean-field (MF) results show that both supra and sub-threshold balanced asynchronous regimes are observable in our system in the limit N >> K >> 1. Due to the heterogeneity, the asynchronous states are characterized at the microscopic level by the splitting of the neurons in to three groups: silent, fluctuation, and mean driven. These features are consistent with experimental observations reported for heterogeneous neural circuits. The coherent rhythms observed in our system can range from periodic and quasi-periodic collective oscillations (COs) to coherent chaos. These rhythms are characterized by regular or irregular temporal fluctuations joined to spatial coherence somehow similar to coherent fluctuations observed in the cortex over multiple spatial scales. The COs can emerge due to two different mechanisms. A first mechanism analogous to the pyramidal-interneuron gamma (PING), usually invoked for the emergence of γ-oscillations. The second mechanism is intimately related to the presence of current fluctuations, which sustain COs characterized by an essentially simultaneous bursting of the two populations. We observe period-doubling cascades involving the PING-like COs finally leading to the appearance of coherent chaos. Fluctuation driven COs are usually observable in our system as quasi-periodic collective motions characterized by two incommensurate frequencies. However, for sufficiently strong current fluctuations these collective rhythms can lock. This represents a novel mechanism of frequency locking in neural populations promoted by intrinsic fluctuations. COs are observable for any finite in-degree K, however, their existence in the limit N >> K >> 1 appears as uncertain. Frontiers Media S.A. 2021-12-10 /pmc/articles/PMC8702645/ /pubmed/34955768 http://dx.doi.org/10.3389/fnsys.2021.752261 Text en Copyright © 2021 Bi, di Volo and Torcini. 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 Neuroscience
Bi, Hongjie
di Volo, Matteo
Torcini, Alessandro
Asynchronous and Coherent Dynamics in Balanced Excitatory-Inhibitory Spiking Networks
title Asynchronous and Coherent Dynamics in Balanced Excitatory-Inhibitory Spiking Networks
title_full Asynchronous and Coherent Dynamics in Balanced Excitatory-Inhibitory Spiking Networks
title_fullStr Asynchronous and Coherent Dynamics in Balanced Excitatory-Inhibitory Spiking Networks
title_full_unstemmed Asynchronous and Coherent Dynamics in Balanced Excitatory-Inhibitory Spiking Networks
title_short Asynchronous and Coherent Dynamics in Balanced Excitatory-Inhibitory Spiking Networks
title_sort asynchronous and coherent dynamics in balanced excitatory-inhibitory spiking networks
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8702645/
https://www.ncbi.nlm.nih.gov/pubmed/34955768
http://dx.doi.org/10.3389/fnsys.2021.752261
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