Theta-gamma coupling emerges from spatially heterogeneous cholinergic neuromodulation.

Theta and gamma rhythms and their cross-frequency coupling play critical roles in perception, attention, learning, and memory. Available data suggest that forebrain acetylcholine (ACh) signaling promotes theta-gamma coupling, although the mechanism has not been identified. Recent evidence suggests t...

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Autores principales:	Yihao Yang, Howard Gritton, Martin Sarter, Sara J Aton, Victoria Booth, Michal Zochowski
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/4234b9b80a7c465081980f2e87aacbd7
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spelling	oai:doaj.org-article:4234b9b80a7c465081980f2e87aacbd72021-12-02T19:57:21ZTheta-gamma coupling emerges from spatially heterogeneous cholinergic neuromodulation.1553-734X1553-735810.1371/journal.pcbi.1009235https://doaj.org/article/4234b9b80a7c465081980f2e87aacbd72021-07-01T00:00:00Zhttps://doi.org/10.1371/journal.pcbi.1009235https://doaj.org/toc/1553-734Xhttps://doaj.org/toc/1553-7358Theta and gamma rhythms and their cross-frequency coupling play critical roles in perception, attention, learning, and memory. Available data suggest that forebrain acetylcholine (ACh) signaling promotes theta-gamma coupling, although the mechanism has not been identified. Recent evidence suggests that cholinergic signaling is both temporally and spatially constrained, in contrast to the traditional notion of slow, spatially homogeneous, and diffuse neuromodulation. Here, we find that spatially constrained cholinergic stimulation can generate theta-modulated gamma rhythms. Using biophysically-based excitatory-inhibitory (E-I) neural network models, we simulate the effects of ACh on neural excitability by varying the conductance of a muscarinic receptor-regulated K+ current. In E-I networks with local excitatory connectivity and global inhibitory connectivity, we demonstrate that theta-gamma-coupled firing patterns emerge in ACh modulated network regions. Stable gamma-modulated firing arises within regions with high ACh signaling, while theta or mixed theta-gamma activity occurs at the peripheries of these regions. High gamma activity also alternates between different high-ACh regions, at theta frequency. Our results are the first to indicate a causal role for spatially heterogenous ACh signaling in the emergence of localized theta-gamma rhythmicity. Our findings also provide novel insights into mechanisms by which ACh signaling supports the brain region-specific attentional processing of sensory information.Yihao YangHoward GrittonMartin SarterSara J AtonVictoria BoothMichal ZochowskiPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Computational Biology, Vol 17, Iss 7, p e1009235 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Yihao Yang Howard Gritton Martin Sarter Sara J Aton Victoria Booth Michal Zochowski Theta-gamma coupling emerges from spatially heterogeneous cholinergic neuromodulation.
description	Theta and gamma rhythms and their cross-frequency coupling play critical roles in perception, attention, learning, and memory. Available data suggest that forebrain acetylcholine (ACh) signaling promotes theta-gamma coupling, although the mechanism has not been identified. Recent evidence suggests that cholinergic signaling is both temporally and spatially constrained, in contrast to the traditional notion of slow, spatially homogeneous, and diffuse neuromodulation. Here, we find that spatially constrained cholinergic stimulation can generate theta-modulated gamma rhythms. Using biophysically-based excitatory-inhibitory (E-I) neural network models, we simulate the effects of ACh on neural excitability by varying the conductance of a muscarinic receptor-regulated K+ current. In E-I networks with local excitatory connectivity and global inhibitory connectivity, we demonstrate that theta-gamma-coupled firing patterns emerge in ACh modulated network regions. Stable gamma-modulated firing arises within regions with high ACh signaling, while theta or mixed theta-gamma activity occurs at the peripheries of these regions. High gamma activity also alternates between different high-ACh regions, at theta frequency. Our results are the first to indicate a causal role for spatially heterogenous ACh signaling in the emergence of localized theta-gamma rhythmicity. Our findings also provide novel insights into mechanisms by which ACh signaling supports the brain region-specific attentional processing of sensory information.
format	article
author	Yihao Yang Howard Gritton Martin Sarter Sara J Aton Victoria Booth Michal Zochowski
author_facet	Yihao Yang Howard Gritton Martin Sarter Sara J Aton Victoria Booth Michal Zochowski
author_sort	Yihao Yang
title	Theta-gamma coupling emerges from spatially heterogeneous cholinergic neuromodulation.
title_short	Theta-gamma coupling emerges from spatially heterogeneous cholinergic neuromodulation.
title_full	Theta-gamma coupling emerges from spatially heterogeneous cholinergic neuromodulation.
title_fullStr	Theta-gamma coupling emerges from spatially heterogeneous cholinergic neuromodulation.
title_full_unstemmed	Theta-gamma coupling emerges from spatially heterogeneous cholinergic neuromodulation.
title_sort	theta-gamma coupling emerges from spatially heterogeneous cholinergic neuromodulation.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/4234b9b80a7c465081980f2e87aacbd7
work_keys_str_mv	AT yihaoyang thetagammacouplingemergesfromspatiallyheterogeneouscholinergicneuromodulation AT howardgritton thetagammacouplingemergesfromspatiallyheterogeneouscholinergicneuromodulation AT martinsarter thetagammacouplingemergesfromspatiallyheterogeneouscholinergicneuromodulation AT sarajaton thetagammacouplingemergesfromspatiallyheterogeneouscholinergicneuromodulation AT victoriabooth thetagammacouplingemergesfromspatiallyheterogeneouscholinergicneuromodulation AT michalzochowski thetagammacouplingemergesfromspatiallyheterogeneouscholinergicneuromodulation
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Theta-gamma coupling emerges from spatially heterogeneous cholinergic neuromodulation.

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