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Optimal responsiveness and information flow in networks of heterogeneous neurons

Cerebral cortex is characterized by a strong neuron-to-neuron heterogeneity, but it is unclear what consequences this may have for cortical computations, while most computational models consider networks of identical units. Here, we study network models of spiking neurons endowed with heterogeneity,...

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Detalles Bibliográficos
Autores principales: Di Volo, Matteo, Destexhe, Alain
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8413388/
https://www.ncbi.nlm.nih.gov/pubmed/34475456
http://dx.doi.org/10.1038/s41598-021-96745-2
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author Di Volo, Matteo
Destexhe, Alain
author_facet Di Volo, Matteo
Destexhe, Alain
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description Cerebral cortex is characterized by a strong neuron-to-neuron heterogeneity, but it is unclear what consequences this may have for cortical computations, while most computational models consider networks of identical units. Here, we study network models of spiking neurons endowed with heterogeneity, that we treat independently for excitatory and inhibitory neurons. We find that heterogeneous networks are generally more responsive, with an optimal responsiveness occurring for levels of heterogeneity found experimentally in different published datasets, for both excitatory and inhibitory neurons. To investigate the underlying mechanisms, we introduce a mean-field model of heterogeneous networks. This mean-field model captures optimal responsiveness and suggests that it is related to the stability of the spontaneous asynchronous state. The mean-field model also predicts that new dynamical states can emerge from heterogeneity, a prediction which is confirmed by network simulations. Finally we show that heterogeneous networks maximise the information flow in large-scale networks, through recurrent connections. We conclude that neuronal heterogeneity confers different responsiveness to neural networks, which should be taken into account to investigate their information processing capabilities.
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spelling pubmed-84133882021-09-07 Optimal responsiveness and information flow in networks of heterogeneous neurons Di Volo, Matteo Destexhe, Alain Sci Rep Article Cerebral cortex is characterized by a strong neuron-to-neuron heterogeneity, but it is unclear what consequences this may have for cortical computations, while most computational models consider networks of identical units. Here, we study network models of spiking neurons endowed with heterogeneity, that we treat independently for excitatory and inhibitory neurons. We find that heterogeneous networks are generally more responsive, with an optimal responsiveness occurring for levels of heterogeneity found experimentally in different published datasets, for both excitatory and inhibitory neurons. To investigate the underlying mechanisms, we introduce a mean-field model of heterogeneous networks. This mean-field model captures optimal responsiveness and suggests that it is related to the stability of the spontaneous asynchronous state. The mean-field model also predicts that new dynamical states can emerge from heterogeneity, a prediction which is confirmed by network simulations. Finally we show that heterogeneous networks maximise the information flow in large-scale networks, through recurrent connections. We conclude that neuronal heterogeneity confers different responsiveness to neural networks, which should be taken into account to investigate their information processing capabilities. Nature Publishing Group UK 2021-09-02 /pmc/articles/PMC8413388/ /pubmed/34475456 http://dx.doi.org/10.1038/s41598-021-96745-2 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 Article
Di Volo, Matteo
Destexhe, Alain
Optimal responsiveness and information flow in networks of heterogeneous neurons
title Optimal responsiveness and information flow in networks of heterogeneous neurons
title_full Optimal responsiveness and information flow in networks of heterogeneous neurons
title_fullStr Optimal responsiveness and information flow in networks of heterogeneous neurons
title_full_unstemmed Optimal responsiveness and information flow in networks of heterogeneous neurons
title_short Optimal responsiveness and information flow in networks of heterogeneous neurons
title_sort optimal responsiveness and information flow in networks of heterogeneous neurons
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8413388/
https://www.ncbi.nlm.nih.gov/pubmed/34475456
http://dx.doi.org/10.1038/s41598-021-96745-2
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