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Excitatory selective LTP of supramammillary glutamatergic/GABAergic cotransmission potentiates dentate granule cell firing

Emerging evidence indicates that the functionally opposing neurotransmitters, glutamate and GABA, are coreleased from the same presynaptic terminals in some adult brain regions. The supramammillary nucleus (SuM) is one region that coreleases glutamate and GABA in the dentate gyrus (DG) through its a...

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Autores principales: Tabuchi, Eri, Sakaba, Takeshi, Hashimotodani, Yuki
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9060512/
https://www.ncbi.nlm.nih.gov/pubmed/35333647
http://dx.doi.org/10.1073/pnas.2119636119
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author Tabuchi, Eri
Sakaba, Takeshi
Hashimotodani, Yuki
author_facet Tabuchi, Eri
Sakaba, Takeshi
Hashimotodani, Yuki
author_sort Tabuchi, Eri
collection PubMed
description Emerging evidence indicates that the functionally opposing neurotransmitters, glutamate and GABA, are coreleased from the same presynaptic terminals in some adult brain regions. The supramammillary nucleus (SuM) is one region that coreleases glutamate and GABA in the dentate gyrus (DG) through its afferents. Although the SuM-DG pathway has been implicated in various brain functions, little is known about the functional roles of the peculiar features of glutamate/GABA corelease. Here, we show that depolarization of granule cells (GCs) triggers postsynaptic long-term potentiation (LTP) of glutamatergic, but not GABAergic, cotransmission at SuM-GC synapses. Moreover, the burst activity of perforant-path inputs heterosynaptically induces LTP at excitatory SuM-GC synapses. This non-Hebbian LTP requires postsynaptic Ca(2+) influx, Ca(2+)/calmodulin-dependent protein kinase II (CaMKII) activity, and exocytosis of AMPA receptors. Glutamatergic transmission-selective expression of LTP increases the excitatory drive such that SuM inputs become sufficient to discharge GCs. Our results highlight a form of LTP, which dynamically and rapidly changes the glutamatergic/GABAergic cotransmission balance and contributes to DG network activity.
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spelling pubmed-90605122022-09-25 Excitatory selective LTP of supramammillary glutamatergic/GABAergic cotransmission potentiates dentate granule cell firing Tabuchi, Eri Sakaba, Takeshi Hashimotodani, Yuki Proc Natl Acad Sci U S A Biological Sciences Emerging evidence indicates that the functionally opposing neurotransmitters, glutamate and GABA, are coreleased from the same presynaptic terminals in some adult brain regions. The supramammillary nucleus (SuM) is one region that coreleases glutamate and GABA in the dentate gyrus (DG) through its afferents. Although the SuM-DG pathway has been implicated in various brain functions, little is known about the functional roles of the peculiar features of glutamate/GABA corelease. Here, we show that depolarization of granule cells (GCs) triggers postsynaptic long-term potentiation (LTP) of glutamatergic, but not GABAergic, cotransmission at SuM-GC synapses. Moreover, the burst activity of perforant-path inputs heterosynaptically induces LTP at excitatory SuM-GC synapses. This non-Hebbian LTP requires postsynaptic Ca(2+) influx, Ca(2+)/calmodulin-dependent protein kinase II (CaMKII) activity, and exocytosis of AMPA receptors. Glutamatergic transmission-selective expression of LTP increases the excitatory drive such that SuM inputs become sufficient to discharge GCs. Our results highlight a form of LTP, which dynamically and rapidly changes the glutamatergic/GABAergic cotransmission balance and contributes to DG network activity. National Academy of Sciences 2022-03-25 2022-03-29 /pmc/articles/PMC9060512/ /pubmed/35333647 http://dx.doi.org/10.1073/pnas.2119636119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Tabuchi, Eri
Sakaba, Takeshi
Hashimotodani, Yuki
Excitatory selective LTP of supramammillary glutamatergic/GABAergic cotransmission potentiates dentate granule cell firing
title Excitatory selective LTP of supramammillary glutamatergic/GABAergic cotransmission potentiates dentate granule cell firing
title_full Excitatory selective LTP of supramammillary glutamatergic/GABAergic cotransmission potentiates dentate granule cell firing
title_fullStr Excitatory selective LTP of supramammillary glutamatergic/GABAergic cotransmission potentiates dentate granule cell firing
title_full_unstemmed Excitatory selective LTP of supramammillary glutamatergic/GABAergic cotransmission potentiates dentate granule cell firing
title_short Excitatory selective LTP of supramammillary glutamatergic/GABAergic cotransmission potentiates dentate granule cell firing
title_sort excitatory selective ltp of supramammillary glutamatergic/gabaergic cotransmission potentiates dentate granule cell firing
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9060512/
https://www.ncbi.nlm.nih.gov/pubmed/35333647
http://dx.doi.org/10.1073/pnas.2119636119
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