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Hippocampal sharp wave-ripples and the associated sequence replay emerge from structured synaptic interactions in a network model of area CA3

Hippocampal place cells are activated sequentially as an animal explores its environment. These activity sequences are internally recreated (‘replayed’), either in the same or reversed order, during bursts of activity (sharp wave-ripples [SWRs]) that occur in sleep and awake rest. SWR-associated rep...

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Autores principales: Ecker, András, Bagi, Bence, Vértes, Eszter, Steinbach-Németh, Orsolya, Karlócai, Mária R, Papp, Orsolya I, Miklós, István, Hájos, Norbert, Freund, Tamás F, Gulyás, Attila I, Káli, Szabolcs
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8865846/
https://www.ncbi.nlm.nih.gov/pubmed/35040779
http://dx.doi.org/10.7554/eLife.71850
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author Ecker, András
Bagi, Bence
Vértes, Eszter
Steinbach-Németh, Orsolya
Karlócai, Mária R
Papp, Orsolya I
Miklós, István
Hájos, Norbert
Freund, Tamás F
Gulyás, Attila I
Káli, Szabolcs
author_facet Ecker, András
Bagi, Bence
Vértes, Eszter
Steinbach-Németh, Orsolya
Karlócai, Mária R
Papp, Orsolya I
Miklós, István
Hájos, Norbert
Freund, Tamás F
Gulyás, Attila I
Káli, Szabolcs
author_sort Ecker, András
collection PubMed
description Hippocampal place cells are activated sequentially as an animal explores its environment. These activity sequences are internally recreated (‘replayed’), either in the same or reversed order, during bursts of activity (sharp wave-ripples [SWRs]) that occur in sleep and awake rest. SWR-associated replay is thought to be critical for the creation and maintenance of long-term memory. In order to identify the cellular and network mechanisms of SWRs and replay, we constructed and simulated a data-driven model of area CA3 of the hippocampus. Our results show that the chain-like structure of recurrent excitatory interactions established during learning not only determines the content of replay, but is essential for the generation of the SWRs as well. We find that bidirectional replay requires the interplay of the experimentally confirmed, temporally symmetric plasticity rule, and cellular adaptation. Our model provides a unifying framework for diverse phenomena involving hippocampal plasticity, representations, and dynamics, and suggests that the structured neural codes induced by learning may have greater influence over cortical network states than previously appreciated.
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spelling pubmed-88658462022-02-24 Hippocampal sharp wave-ripples and the associated sequence replay emerge from structured synaptic interactions in a network model of area CA3 Ecker, András Bagi, Bence Vértes, Eszter Steinbach-Németh, Orsolya Karlócai, Mária R Papp, Orsolya I Miklós, István Hájos, Norbert Freund, Tamás F Gulyás, Attila I Káli, Szabolcs eLife Computational and Systems Biology Hippocampal place cells are activated sequentially as an animal explores its environment. These activity sequences are internally recreated (‘replayed’), either in the same or reversed order, during bursts of activity (sharp wave-ripples [SWRs]) that occur in sleep and awake rest. SWR-associated replay is thought to be critical for the creation and maintenance of long-term memory. In order to identify the cellular and network mechanisms of SWRs and replay, we constructed and simulated a data-driven model of area CA3 of the hippocampus. Our results show that the chain-like structure of recurrent excitatory interactions established during learning not only determines the content of replay, but is essential for the generation of the SWRs as well. We find that bidirectional replay requires the interplay of the experimentally confirmed, temporally symmetric plasticity rule, and cellular adaptation. Our model provides a unifying framework for diverse phenomena involving hippocampal plasticity, representations, and dynamics, and suggests that the structured neural codes induced by learning may have greater influence over cortical network states than previously appreciated. eLife Sciences Publications, Ltd 2022-01-18 /pmc/articles/PMC8865846/ /pubmed/35040779 http://dx.doi.org/10.7554/eLife.71850 Text en © 2022, Ecker et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Computational and Systems Biology
Ecker, András
Bagi, Bence
Vértes, Eszter
Steinbach-Németh, Orsolya
Karlócai, Mária R
Papp, Orsolya I
Miklós, István
Hájos, Norbert
Freund, Tamás F
Gulyás, Attila I
Káli, Szabolcs
Hippocampal sharp wave-ripples and the associated sequence replay emerge from structured synaptic interactions in a network model of area CA3
title Hippocampal sharp wave-ripples and the associated sequence replay emerge from structured synaptic interactions in a network model of area CA3
title_full Hippocampal sharp wave-ripples and the associated sequence replay emerge from structured synaptic interactions in a network model of area CA3
title_fullStr Hippocampal sharp wave-ripples and the associated sequence replay emerge from structured synaptic interactions in a network model of area CA3
title_full_unstemmed Hippocampal sharp wave-ripples and the associated sequence replay emerge from structured synaptic interactions in a network model of area CA3
title_short Hippocampal sharp wave-ripples and the associated sequence replay emerge from structured synaptic interactions in a network model of area CA3
title_sort hippocampal sharp wave-ripples and the associated sequence replay emerge from structured synaptic interactions in a network model of area ca3
topic Computational and Systems Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8865846/
https://www.ncbi.nlm.nih.gov/pubmed/35040779
http://dx.doi.org/10.7554/eLife.71850
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