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Rapid astrocyte-dependent facilitation amplifies multi-vesicular release in hippocampal synapses

Synaptic facilitation is a major form of short-term plasticity typically driven by an increase in residual presynaptic calcium. Using near-total internal reflection fluorescence (near-TIRF) imaging of single vesicle release in cultured hippocampal synapses, we demonstrate a distinctive, release-depe...

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Autores principales: Myeong, Jongyun, Klyachko, Vitaly A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9805313/
https://www.ncbi.nlm.nih.gov/pubmed/36516768
http://dx.doi.org/10.1016/j.celrep.2022.111820
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author Myeong, Jongyun
Klyachko, Vitaly A.
author_facet Myeong, Jongyun
Klyachko, Vitaly A.
author_sort Myeong, Jongyun
collection PubMed
description Synaptic facilitation is a major form of short-term plasticity typically driven by an increase in residual presynaptic calcium. Using near-total internal reflection fluorescence (near-TIRF) imaging of single vesicle release in cultured hippocampal synapses, we demonstrate a distinctive, release-dependent form of facilitation in which probability of vesicle release is higher following a successful glutamate release event than following a failure. This phenomenon has an onset of ≤500 ms and lasts several seconds, resulting in clusters of successful release events. The release-dependent facilitation requires neuronal contact with astrocytes and astrocytic glutamate uptake by EAAT1. It is not observed in neurons grown alone or in the presence of astrocyte-conditioned media. This form of facilitation dynamically amplifies multi-vesicular release. Facilitation-evoked release events exhibit spatial clustering and have a preferential localization toward the active zone center. These results uncover a rapid astrocyte-dependent form of facilitation acting via modulation of multi-vesicular release and displaying distinctive spatiotemporal properties.
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spelling pubmed-98053132022-12-31 Rapid astrocyte-dependent facilitation amplifies multi-vesicular release in hippocampal synapses Myeong, Jongyun Klyachko, Vitaly A. Cell Rep Article Synaptic facilitation is a major form of short-term plasticity typically driven by an increase in residual presynaptic calcium. Using near-total internal reflection fluorescence (near-TIRF) imaging of single vesicle release in cultured hippocampal synapses, we demonstrate a distinctive, release-dependent form of facilitation in which probability of vesicle release is higher following a successful glutamate release event than following a failure. This phenomenon has an onset of ≤500 ms and lasts several seconds, resulting in clusters of successful release events. The release-dependent facilitation requires neuronal contact with astrocytes and astrocytic glutamate uptake by EAAT1. It is not observed in neurons grown alone or in the presence of astrocyte-conditioned media. This form of facilitation dynamically amplifies multi-vesicular release. Facilitation-evoked release events exhibit spatial clustering and have a preferential localization toward the active zone center. These results uncover a rapid astrocyte-dependent form of facilitation acting via modulation of multi-vesicular release and displaying distinctive spatiotemporal properties. 2022-12-13 /pmc/articles/PMC9805313/ /pubmed/36516768 http://dx.doi.org/10.1016/j.celrep.2022.111820 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/ (https://creativecommons.org/licenses/by-nc-nd/4.0/) ).
spellingShingle Article
Myeong, Jongyun
Klyachko, Vitaly A.
Rapid astrocyte-dependent facilitation amplifies multi-vesicular release in hippocampal synapses
title Rapid astrocyte-dependent facilitation amplifies multi-vesicular release in hippocampal synapses
title_full Rapid astrocyte-dependent facilitation amplifies multi-vesicular release in hippocampal synapses
title_fullStr Rapid astrocyte-dependent facilitation amplifies multi-vesicular release in hippocampal synapses
title_full_unstemmed Rapid astrocyte-dependent facilitation amplifies multi-vesicular release in hippocampal synapses
title_short Rapid astrocyte-dependent facilitation amplifies multi-vesicular release in hippocampal synapses
title_sort rapid astrocyte-dependent facilitation amplifies multi-vesicular release in hippocampal synapses
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9805313/
https://www.ncbi.nlm.nih.gov/pubmed/36516768
http://dx.doi.org/10.1016/j.celrep.2022.111820
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