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

Sci Rep. 2021 Jan 22;11(1):2117. doi: 10.1038/s41598-020-80245-w.

Abstract

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

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Algorithms
  • Animals
  • Calcium / metabolism
  • Hippocampus / cytology
  • Hippocampus / physiology*
  • Membrane Potentials / physiology
  • Mice, Transgenic
  • Models, Neurological
  • Neurons / cytology
  • Neurons / metabolism
  • Neurons / physiology*
  • Optogenetics / methods
  • Parvalbumins / metabolism*
  • Patch-Clamp Techniques
  • Septum of Brain / cytology
  • Septum of Brain / physiology*
  • Synapses / physiology*
  • Synaptic Transmission / physiology*

Substances

  • Parvalbumins
  • Calcium