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Transsynaptic modulation of presynaptic short-term plasticity in hippocampal mossy fiber synapses

The hippocampal mossy fiber synapse is a key synapse of the trisynaptic circuit. Post-tetanic potentiation (PTP) is the most powerful form of plasticity at this synaptic connection. It is widely believed that mossy fiber PTP is an entirely presynaptic phenomenon, implying that PTP induction is input...

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Autores principales: Vandael, David, Okamoto, Yuji, Jonas, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8131630/
https://www.ncbi.nlm.nih.gov/pubmed/34006874
http://dx.doi.org/10.1038/s41467-021-23153-5
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author Vandael, David
Okamoto, Yuji
Jonas, Peter
author_facet Vandael, David
Okamoto, Yuji
Jonas, Peter
author_sort Vandael, David
collection PubMed
description The hippocampal mossy fiber synapse is a key synapse of the trisynaptic circuit. Post-tetanic potentiation (PTP) is the most powerful form of plasticity at this synaptic connection. It is widely believed that mossy fiber PTP is an entirely presynaptic phenomenon, implying that PTP induction is input-specific, and requires neither activity of multiple inputs nor stimulation of postsynaptic neurons. To directly test cooperativity and associativity, we made paired recordings between single mossy fiber terminals and postsynaptic CA3 pyramidal neurons in rat brain slices. By stimulating non-overlapping mossy fiber inputs converging onto single CA3 neurons, we confirm that PTP is input-specific and non-cooperative. Unexpectedly, mossy fiber PTP exhibits anti-associative induction properties. EPSCs show only minimal PTP after combined pre- and postsynaptic high-frequency stimulation with intact postsynaptic Ca(2+) signaling, but marked PTP in the absence of postsynaptic spiking and after suppression of postsynaptic Ca(2+) signaling (10 mM EGTA). PTP is largely recovered by inhibitors of voltage-gated R- and L-type Ca(2+) channels, group II mGluRs, and vacuolar-type H(+)-ATPase, suggesting the involvement of retrograde vesicular glutamate signaling. Transsynaptic regulation of PTP extends the repertoire of synaptic computations, implementing a brake on mossy fiber detonation and a “smart teacher” function of hippocampal mossy fiber synapses.
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spelling pubmed-81316302021-05-24 Transsynaptic modulation of presynaptic short-term plasticity in hippocampal mossy fiber synapses Vandael, David Okamoto, Yuji Jonas, Peter Nat Commun Article The hippocampal mossy fiber synapse is a key synapse of the trisynaptic circuit. Post-tetanic potentiation (PTP) is the most powerful form of plasticity at this synaptic connection. It is widely believed that mossy fiber PTP is an entirely presynaptic phenomenon, implying that PTP induction is input-specific, and requires neither activity of multiple inputs nor stimulation of postsynaptic neurons. To directly test cooperativity and associativity, we made paired recordings between single mossy fiber terminals and postsynaptic CA3 pyramidal neurons in rat brain slices. By stimulating non-overlapping mossy fiber inputs converging onto single CA3 neurons, we confirm that PTP is input-specific and non-cooperative. Unexpectedly, mossy fiber PTP exhibits anti-associative induction properties. EPSCs show only minimal PTP after combined pre- and postsynaptic high-frequency stimulation with intact postsynaptic Ca(2+) signaling, but marked PTP in the absence of postsynaptic spiking and after suppression of postsynaptic Ca(2+) signaling (10 mM EGTA). PTP is largely recovered by inhibitors of voltage-gated R- and L-type Ca(2+) channels, group II mGluRs, and vacuolar-type H(+)-ATPase, suggesting the involvement of retrograde vesicular glutamate signaling. Transsynaptic regulation of PTP extends the repertoire of synaptic computations, implementing a brake on mossy fiber detonation and a “smart teacher” function of hippocampal mossy fiber synapses. Nature Publishing Group UK 2021-05-18 /pmc/articles/PMC8131630/ /pubmed/34006874 http://dx.doi.org/10.1038/s41467-021-23153-5 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Vandael, David
Okamoto, Yuji
Jonas, Peter
Transsynaptic modulation of presynaptic short-term plasticity in hippocampal mossy fiber synapses
title Transsynaptic modulation of presynaptic short-term plasticity in hippocampal mossy fiber synapses
title_full Transsynaptic modulation of presynaptic short-term plasticity in hippocampal mossy fiber synapses
title_fullStr Transsynaptic modulation of presynaptic short-term plasticity in hippocampal mossy fiber synapses
title_full_unstemmed Transsynaptic modulation of presynaptic short-term plasticity in hippocampal mossy fiber synapses
title_short Transsynaptic modulation of presynaptic short-term plasticity in hippocampal mossy fiber synapses
title_sort transsynaptic modulation of presynaptic short-term plasticity in hippocampal mossy fiber synapses
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8131630/
https://www.ncbi.nlm.nih.gov/pubmed/34006874
http://dx.doi.org/10.1038/s41467-021-23153-5
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