The inhibitory control of traveling waves in cortical networks.

Propagating waves of activity can be evoked and can occur spontaneously in vivo and in vitro in cerebral cortex. These waves are thought to be instrumental in the propagation of information across cortical regions and as a means to modulate the sensitivity of neurons to subsequent stimuli. In normal...

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Main Authors: Grishma Palkar, Jian-Young Wu, Bard Ermentrout
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2023-09-01
Series:PLoS Computational Biology
Online Access:https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1010697&type=printable
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author Grishma Palkar
Jian-Young Wu
Bard Ermentrout
author_facet Grishma Palkar
Jian-Young Wu
Bard Ermentrout
author_sort Grishma Palkar
collection DOAJ
description Propagating waves of activity can be evoked and can occur spontaneously in vivo and in vitro in cerebral cortex. These waves are thought to be instrumental in the propagation of information across cortical regions and as a means to modulate the sensitivity of neurons to subsequent stimuli. In normal tissue, the waves are sparse and tightly controlled by inhibition and other negative feedback processes. However, alterations of this balance between excitation and inhibition can lead to pathological behavior such as seizure-type dynamics (with low inhibition) or failure to propagate (with high inhibition). We develop a spiking one-dimensional network of neurons to explore the reliability and control of evoked waves and compare this to a cortical slice preparation where the excitability can be pharmacologically manipulated. We show that the waves enhance sensitivity of the cortical network to stimuli in specific spatial and temporal ways. To gain further insight into the mechanisms of propagation and transitions to pathological behavior, we derive a mean-field model for the synaptic activity. We analyze the mean-field model and a piece-wise constant approximation of it and study the stability of the propagating waves as spatial and temporal properties of the inhibition are altered. We show that that the transition to seizure-like activity is gradual but that the loss of propagation is abrupt and can occur via either the loss of existence of the wave or through a loss of stability leading to complex patterns of propagation.
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spelling doaj.art-379ebbb70f614ba0b3bc97eef26cee262023-09-26T05:30:47ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582023-09-01199e101069710.1371/journal.pcbi.1010697The inhibitory control of traveling waves in cortical networks.Grishma PalkarJian-Young WuBard ErmentroutPropagating waves of activity can be evoked and can occur spontaneously in vivo and in vitro in cerebral cortex. These waves are thought to be instrumental in the propagation of information across cortical regions and as a means to modulate the sensitivity of neurons to subsequent stimuli. In normal tissue, the waves are sparse and tightly controlled by inhibition and other negative feedback processes. However, alterations of this balance between excitation and inhibition can lead to pathological behavior such as seizure-type dynamics (with low inhibition) or failure to propagate (with high inhibition). We develop a spiking one-dimensional network of neurons to explore the reliability and control of evoked waves and compare this to a cortical slice preparation where the excitability can be pharmacologically manipulated. We show that the waves enhance sensitivity of the cortical network to stimuli in specific spatial and temporal ways. To gain further insight into the mechanisms of propagation and transitions to pathological behavior, we derive a mean-field model for the synaptic activity. We analyze the mean-field model and a piece-wise constant approximation of it and study the stability of the propagating waves as spatial and temporal properties of the inhibition are altered. We show that that the transition to seizure-like activity is gradual but that the loss of propagation is abrupt and can occur via either the loss of existence of the wave or through a loss of stability leading to complex patterns of propagation.https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1010697&type=printable
spellingShingle Grishma Palkar
Jian-Young Wu
Bard Ermentrout
The inhibitory control of traveling waves in cortical networks.
PLoS Computational Biology
title The inhibitory control of traveling waves in cortical networks.
title_full The inhibitory control of traveling waves in cortical networks.
title_fullStr The inhibitory control of traveling waves in cortical networks.
title_full_unstemmed The inhibitory control of traveling waves in cortical networks.
title_short The inhibitory control of traveling waves in cortical networks.
title_sort inhibitory control of traveling waves in cortical networks
url https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1010697&type=printable
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