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

Feng Yi; Tavita Garrett; Karl Deisseroth; Heikki Haario; Emily Stone; J. Josh Lawrence

doi:10.1038/s41598-020-80245-w

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

Feng Yi
, Tavita Garrett
, Karl Deisseroth
, Heikki Haario
, Emily Stone
, J. Josh Lawrence

Mathematical Sciences

Research output: Contribution to journal › Article › peer-review

5 Scopus citations

Abstract

Parvalbumin-containing projection neurons of the medial-septum-diagonal band of Broca (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 PV _MS-DBB neuronal properties. 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 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 (PV _HC) neurons generated trains of PV _HC-mediated IPSCs in CA1 pyramidal neurons. Both synapse types exhibited short-term depression (STD) of IPSCs. However, relative to PV _HC synapses, 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 PV _HC model, the PV _MS-DBB model exhibited higher sensitivity to calcium accumulation, permitting a faster rate of calcium-dependent recovery from STD. In conclusion, resistance of PV _MS-DBB synapses to STD during short gamma bursts enables robust long-range GABAergic transmission from MS-DBB to hippocampus.

Original language	English
Article number	2117
Journal	Scientific Reports
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41598-020-80245-w
State	Published - Dec 2021

Funding

Support was from NIH R01 NS069689 (JJL), NS069689-04S1 (TG), NCRR P20RR015583 (JJL), and TTUHSC start-up funds (JJL). P20RR015583, P20RR017670, and P20GM10356 grants supported core facilities. We thank Drs. April D. Johnston and Benjamin B. Holloway for preliminary optogenetics experiments in PV-CRE mice, Drs. Ed Calloway (Salk Institute) and Silvia Arber (University of Basel, Switzerland) for PV-CRE mice, Drs. Mas-simo Scanziani and Z. Josh Huang for SOM-CRE mice, Dr. Viktor Varga for comments on an earlier version of the manuscript, helpful discussions with Dr. Vladislav Sekulić during the course of these studies, and Dr. Volker Neugebauer and the Garrison Institute on Aging (TTUHSC) for assistance with publication costs.

Funder number
NS069689-04S1
P20RR015583

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title = "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 (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 PV MS-DBB neuronal properties. 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 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 (PV HC) neurons generated trains of PV HC-mediated IPSCs in CA1 pyramidal neurons. Both synapse types exhibited short-term depression (STD) of IPSCs. However, relative to PV HC synapses, 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 PV HC model, the PV MS-DBB model exhibited higher sensitivity to calcium accumulation, permitting a faster rate of calcium-dependent recovery from STD. In conclusion, resistance of PV MS-DBB synapses to STD during short gamma bursts enables robust long-range GABAergic transmission from MS-DBB to hippocampus.",

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AU - Stone, Emily

AU - Lawrence, J. Josh

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

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