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Acetylcholine facilitates localized synaptic potentiation and location specific feature binding

Forebrain acetylcholine (ACh) signaling has been shown to drive attention and learning. Recent experimental evidence of spatially and temporally constrained cholinergic signaling has sparked interest to investigate how it facilitates stimulus-induced learning. We use biophysical excitatory-inhibitor...

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Autores principales: Yang, Yihao, Booth, Victoria, Zochowski, Michal
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10684311/
https://www.ncbi.nlm.nih.gov/pubmed/38033788
http://dx.doi.org/10.3389/fncir.2023.1239096
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author Yang, Yihao
Booth, Victoria
Zochowski, Michal
author_facet Yang, Yihao
Booth, Victoria
Zochowski, Michal
author_sort Yang, Yihao
collection PubMed
description Forebrain acetylcholine (ACh) signaling has been shown to drive attention and learning. Recent experimental evidence of spatially and temporally constrained cholinergic signaling has sparked interest to investigate how it facilitates stimulus-induced learning. We use biophysical excitatory-inhibitory (E-I) multi-module neural network models to show that external stimuli and ACh signaling can mediate spatially constrained synaptic potentiation patterns. The effects of ACh on neural excitability are simulated by varying the conductance of a muscarinic receptor-regulated hyperpolarizing slow K+ current (m-current). Each network module consists of an E-I network with local excitatory connectivity and global inhibitory connectivity. The modules are interconnected with plastic excitatory synaptic connections, that change via a spike-timing-dependent plasticity (STDP) rule. Our results indicate that spatially constrained ACh release influences the information flow represented by network dynamics resulting in selective reorganization of inter-module interactions. Moreover the information flow depends on the level of synchrony in the network. For highly synchronous networks, the more excitable module leads firing in the less excitable one resulting in strengthening of the outgoing connections from the former and weakening of its incoming synapses. For networks with more noisy firing patterns, activity in high ACh regions is prone to induce feedback firing of synchronous volleys and thus strengthening of the incoming synapses to the more excitable region and weakening of outgoing synapses. Overall, these results suggest that spatially and directionally specific plasticity patterns, as are presumed necessary for feature binding, can be mediated by spatially constrained ACh release.
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spelling pubmed-106843112023-11-30 Acetylcholine facilitates localized synaptic potentiation and location specific feature binding Yang, Yihao Booth, Victoria Zochowski, Michal Front Neural Circuits Neuroscience Forebrain acetylcholine (ACh) signaling has been shown to drive attention and learning. Recent experimental evidence of spatially and temporally constrained cholinergic signaling has sparked interest to investigate how it facilitates stimulus-induced learning. We use biophysical excitatory-inhibitory (E-I) multi-module neural network models to show that external stimuli and ACh signaling can mediate spatially constrained synaptic potentiation patterns. The effects of ACh on neural excitability are simulated by varying the conductance of a muscarinic receptor-regulated hyperpolarizing slow K+ current (m-current). Each network module consists of an E-I network with local excitatory connectivity and global inhibitory connectivity. The modules are interconnected with plastic excitatory synaptic connections, that change via a spike-timing-dependent plasticity (STDP) rule. Our results indicate that spatially constrained ACh release influences the information flow represented by network dynamics resulting in selective reorganization of inter-module interactions. Moreover the information flow depends on the level of synchrony in the network. For highly synchronous networks, the more excitable module leads firing in the less excitable one resulting in strengthening of the outgoing connections from the former and weakening of its incoming synapses. For networks with more noisy firing patterns, activity in high ACh regions is prone to induce feedback firing of synchronous volleys and thus strengthening of the incoming synapses to the more excitable region and weakening of outgoing synapses. Overall, these results suggest that spatially and directionally specific plasticity patterns, as are presumed necessary for feature binding, can be mediated by spatially constrained ACh release. Frontiers Media S.A. 2023-11-10 /pmc/articles/PMC10684311/ /pubmed/38033788 http://dx.doi.org/10.3389/fncir.2023.1239096 Text en Copyright © 2023 Yang, Booth and Zochowski. 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
Yang, Yihao
Booth, Victoria
Zochowski, Michal
Acetylcholine facilitates localized synaptic potentiation and location specific feature binding
title Acetylcholine facilitates localized synaptic potentiation and location specific feature binding
title_full Acetylcholine facilitates localized synaptic potentiation and location specific feature binding
title_fullStr Acetylcholine facilitates localized synaptic potentiation and location specific feature binding
title_full_unstemmed Acetylcholine facilitates localized synaptic potentiation and location specific feature binding
title_short Acetylcholine facilitates localized synaptic potentiation and location specific feature binding
title_sort acetylcholine facilitates localized synaptic potentiation and location specific feature binding
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10684311/
https://www.ncbi.nlm.nih.gov/pubmed/38033788
http://dx.doi.org/10.3389/fncir.2023.1239096
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