Septohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression

Abstract Parvalbumin-containing projection neurons of the medial-septum-diagonal band of Broca ( $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB ) are essential for hippocampal rhythms and learning operations yet are poorly understood at cellular and synaptic levels. We combined electrophysiological, optog...

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Autores principales:	Feng Yi, Tavita Garrett, Karl Deisseroth, Heikki Haario, Emily Stone, J. Josh Lawrence
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2021
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/2f570e14e471448898db0f4dcce22397
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spelling	oai:doaj.org-article:2f570e14e471448898db0f4dcce223972021-12-02T13:56:47ZSeptohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression10.1038/s41598-020-80245-w2045-2322https://doaj.org/article/2f570e14e471448898db0f4dcce223972021-01-01T00:00:00Zhttps://doi.org/10.1038/s41598-020-80245-whttps://doaj.org/toc/2045-2322Abstract Parvalbumin-containing projection neurons of the medial-septum-diagonal band of Broca ( $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB ) are essential for hippocampal rhythms and learning operations yet are poorly understood at cellular and synaptic levels. We combined electrophysiological, optogenetic, and modeling approaches to investigate $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB neuronal properties. $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB neurons had intrinsic membrane properties distinct from acetylcholine- and somatostatin-containing MS-DBB subtypes. Viral expression of the fast-kinetic channelrhodopsin ChETA-YFP elicited action potentials to brief (1–2 ms) 470 nm light pulses. To investigate $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB transmission, light pulses at 5–50 Hz frequencies generated trains of inhibitory postsynaptic currents (IPSCs) in CA1 stratum oriens interneurons. Using a similar approach, optogenetic activation of local hippocampal PV ( $$\hbox {PV}_{\text{HC}}$$ PV HC ) neurons generated trains of $$\hbox {PV}_{\text{HC}}$$ PV HC -mediated IPSCs in CA1 pyramidal neurons. Both synapse types exhibited short-term depression (STD) of IPSCs. However, relative to $$\hbox {PV}_{\text{HC}}$$ PV HC synapses, $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB synapses possessed lower initial release probability, transiently resisted STD at gamma (20–50 Hz) frequencies, and recovered more rapidly from synaptic depression. Experimentally-constrained mathematical synapse models explored mechanistic differences. Relative to the $$\hbox {PV}_{\text{HC}}$$ PV HC model, the $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB model exhibited higher sensitivity to calcium accumulation, permitting a faster rate of calcium-dependent recovery from STD. In conclusion, resistance of $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB synapses to STD during short gamma bursts enables robust long-range GABAergic transmission from MS-DBB to hippocampus.Feng YiTavita GarrettKarl DeisserothHeikki HaarioEmily StoneJ. Josh LawrenceNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-20 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Feng Yi Tavita Garrett Karl Deisseroth Heikki Haario Emily Stone J. Josh Lawrence Septohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression
description	Abstract Parvalbumin-containing projection neurons of the medial-septum-diagonal band of Broca ( $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB ) are essential for hippocampal rhythms and learning operations yet are poorly understood at cellular and synaptic levels. We combined electrophysiological, optogenetic, and modeling approaches to investigate $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB neuronal properties. $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB neurons had intrinsic membrane properties distinct from acetylcholine- and somatostatin-containing MS-DBB subtypes. Viral expression of the fast-kinetic channelrhodopsin ChETA-YFP elicited action potentials to brief (1–2 ms) 470 nm light pulses. To investigate $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB transmission, light pulses at 5–50 Hz frequencies generated trains of inhibitory postsynaptic currents (IPSCs) in CA1 stratum oriens interneurons. Using a similar approach, optogenetic activation of local hippocampal PV ( $$\hbox {PV}_{\text{HC}}$$ PV HC ) neurons generated trains of $$\hbox {PV}_{\text{HC}}$$ PV HC -mediated IPSCs in CA1 pyramidal neurons. Both synapse types exhibited short-term depression (STD) of IPSCs. However, relative to $$\hbox {PV}_{\text{HC}}$$ PV HC synapses, $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB synapses possessed lower initial release probability, transiently resisted STD at gamma (20–50 Hz) frequencies, and recovered more rapidly from synaptic depression. Experimentally-constrained mathematical synapse models explored mechanistic differences. Relative to the $$\hbox {PV}_{\text{HC}}$$ PV HC model, the $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB model exhibited higher sensitivity to calcium accumulation, permitting a faster rate of calcium-dependent recovery from STD. In conclusion, resistance of $$\hbox {PV}_{\text{MS-DBB}}$$ PV MS-DBB synapses to STD during short gamma bursts enables robust long-range GABAergic transmission from MS-DBB to hippocampus.
format	article
author	Feng Yi Tavita Garrett Karl Deisseroth Heikki Haario Emily Stone J. Josh Lawrence
author_facet	Feng Yi Tavita Garrett Karl Deisseroth Heikki Haario Emily Stone J. Josh Lawrence
author_sort	Feng Yi
title	Septohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression
title_short	Septohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression
title_full	Septohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression
title_fullStr	Septohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression
title_full_unstemmed	Septohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression
title_sort	septohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression
publisher	Nature Portfolio
publishDate	2021
url	https://doaj.org/article/2f570e14e471448898db0f4dcce22397
work_keys_str_mv	AT fengyi septohippocampaltransmissionfromparvalbuminpositiveneuronsfeaturesrapidrecoveryfromsynapticdepression AT tavitagarrett septohippocampaltransmissionfromparvalbuminpositiveneuronsfeaturesrapidrecoveryfromsynapticdepression AT karldeisseroth septohippocampaltransmissionfromparvalbuminpositiveneuronsfeaturesrapidrecoveryfromsynapticdepression AT heikkihaario septohippocampaltransmissionfromparvalbuminpositiveneuronsfeaturesrapidrecoveryfromsynapticdepression AT emilystone septohippocampaltransmissionfromparvalbuminpositiveneuronsfeaturesrapidrecoveryfromsynapticdepression AT jjoshlawrence septohippocampaltransmissionfromparvalbuminpositiveneuronsfeaturesrapidrecoveryfromsynapticdepression
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Septohippocampal transmission from parvalbumin-positive neurons features rapid recovery from synaptic depression

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