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Effect of steady-state response versus excitatory/inhibitory balance on spiking synchronization in neural networks with log-normal synaptic weight distribution

Synchronization of neural activity, especially at the gamma band, contributes to perceptual functions. In several psychiatric disorders, deficits of perceptual functions are reflected in synchronization abnormalities. Plausible cause of this impairment is an alteration in the balance between excitat...

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Autores principales: Nobukawa, Sou, Wagatsuma, Nobuhiko, Ikeda, Takashi, Hasegawa, Chiaki, Kikuchi, Mitsuru, Takahashi, Tetsuya
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Netherlands 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9279535/
https://www.ncbi.nlm.nih.gov/pubmed/35847535
http://dx.doi.org/10.1007/s11571-021-09757-z
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author Nobukawa, Sou
Wagatsuma, Nobuhiko
Ikeda, Takashi
Hasegawa, Chiaki
Kikuchi, Mitsuru
Takahashi, Tetsuya
author_facet Nobukawa, Sou
Wagatsuma, Nobuhiko
Ikeda, Takashi
Hasegawa, Chiaki
Kikuchi, Mitsuru
Takahashi, Tetsuya
author_sort Nobukawa, Sou
collection PubMed
description Synchronization of neural activity, especially at the gamma band, contributes to perceptual functions. In several psychiatric disorders, deficits of perceptual functions are reflected in synchronization abnormalities. Plausible cause of this impairment is an alteration in the balance between excitation and inhibition (E/I balance); a disruption in the E/I balance leads to abnormal neural interactions reminiscent of pathological states. Moreover, the local lateral excitatory-excitatory synaptic connections in the cortex exhibit excitatory postsynaptic potentials (EPSPs) that follow a log-normal amplitude distribution. This long-tailed distribution is considered an important factor for the emergence of spatiotemporal neural activity. In this context, we hypothesized that manipulating the EPSP distribution under abnormal E/I balance conditions would provide insights into psychiatric disorders characterized by deficits in perceptual functions, potentially revealing the mechanisms underlying pathological neural behaviors. In this study, we evaluated the synchronization of neural activity with external periodic stimuli in spiking neural networks in cases of both E/I balance and imbalance with or without a long-tailed EPSP amplitude distribution. The results showed that external stimuli of a high frequency lead to a decrease in the degree of synchronization with an increasing ratio of excitatory to inhibitory neurons in the presence, but not in the absence, of high-amplitude EPSPs. This monotonic reduction can be interpreted as an autonomous, strong-EPSP-dependent spiking activity selectively interfering with the responses to external stimuli. This observation is consistent with pathological findings. Thus, our modeling approach has potential to improve the understanding of the steady-state response in both healthy and pathological states.
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spelling pubmed-92795352022-07-15 Effect of steady-state response versus excitatory/inhibitory balance on spiking synchronization in neural networks with log-normal synaptic weight distribution Nobukawa, Sou Wagatsuma, Nobuhiko Ikeda, Takashi Hasegawa, Chiaki Kikuchi, Mitsuru Takahashi, Tetsuya Cogn Neurodyn Research Article Synchronization of neural activity, especially at the gamma band, contributes to perceptual functions. In several psychiatric disorders, deficits of perceptual functions are reflected in synchronization abnormalities. Plausible cause of this impairment is an alteration in the balance between excitation and inhibition (E/I balance); a disruption in the E/I balance leads to abnormal neural interactions reminiscent of pathological states. Moreover, the local lateral excitatory-excitatory synaptic connections in the cortex exhibit excitatory postsynaptic potentials (EPSPs) that follow a log-normal amplitude distribution. This long-tailed distribution is considered an important factor for the emergence of spatiotemporal neural activity. In this context, we hypothesized that manipulating the EPSP distribution under abnormal E/I balance conditions would provide insights into psychiatric disorders characterized by deficits in perceptual functions, potentially revealing the mechanisms underlying pathological neural behaviors. In this study, we evaluated the synchronization of neural activity with external periodic stimuli in spiking neural networks in cases of both E/I balance and imbalance with or without a long-tailed EPSP amplitude distribution. The results showed that external stimuli of a high frequency lead to a decrease in the degree of synchronization with an increasing ratio of excitatory to inhibitory neurons in the presence, but not in the absence, of high-amplitude EPSPs. This monotonic reduction can be interpreted as an autonomous, strong-EPSP-dependent spiking activity selectively interfering with the responses to external stimuli. This observation is consistent with pathological findings. Thus, our modeling approach has potential to improve the understanding of the steady-state response in both healthy and pathological states. Springer Netherlands 2021-12-03 2022-08 /pmc/articles/PMC9279535/ /pubmed/35847535 http://dx.doi.org/10.1007/s11571-021-09757-z Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Nobukawa, Sou
Wagatsuma, Nobuhiko
Ikeda, Takashi
Hasegawa, Chiaki
Kikuchi, Mitsuru
Takahashi, Tetsuya
Effect of steady-state response versus excitatory/inhibitory balance on spiking synchronization in neural networks with log-normal synaptic weight distribution
title Effect of steady-state response versus excitatory/inhibitory balance on spiking synchronization in neural networks with log-normal synaptic weight distribution
title_full Effect of steady-state response versus excitatory/inhibitory balance on spiking synchronization in neural networks with log-normal synaptic weight distribution
title_fullStr Effect of steady-state response versus excitatory/inhibitory balance on spiking synchronization in neural networks with log-normal synaptic weight distribution
title_full_unstemmed Effect of steady-state response versus excitatory/inhibitory balance on spiking synchronization in neural networks with log-normal synaptic weight distribution
title_short Effect of steady-state response versus excitatory/inhibitory balance on spiking synchronization in neural networks with log-normal synaptic weight distribution
title_sort effect of steady-state response versus excitatory/inhibitory balance on spiking synchronization in neural networks with log-normal synaptic weight distribution
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9279535/
https://www.ncbi.nlm.nih.gov/pubmed/35847535
http://dx.doi.org/10.1007/s11571-021-09757-z
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