Behavior-Dependent Activity and Synaptic Organization of Septohippocampal GABAergic Neurons Selectively Targeting the Hippocampal CA3 Area

Abhilasha Joshi,David Dupret,Minas Salib,Tim J Viney,Peter Somogyi

doi:10.2139/ssrn.3155772

Abhilasha Joshi, David Dupret + Show 3 more

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https://doi.org/10.2139/ssrn.3155772

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Abstract

Rhythmic medial septal (MS) GABAergic input coordinates cortical theta oscillations. However, the rules of innervation of cortical cells and regions by diverse septal neurons are unknown. We report a specialized population of septal GABAergic neurons, the Teevra cells, selectively innervating the hippocampal CA3 area bypassing CA1, CA2 and DG. Teevra cells are parvalbumin-immunopositive, show the highest rhythmicity amongst MS neurons and fire with short burst duration (median, 38ms) preferentially at the trough of both CA1 theta and slow irregular oscillations, coincident with the highest hippocampal excitability. Each Teevra cell synaptically targets GABAergic axo-axonic and CCK basket cells in a restricted septo-temporal CA3 segment. The rhythmicity of their firing decreases from septal to temporal termination of individual axons. Teevra neurons coordinate oscillatory activity across the septotemporal axis and phase the firing of specific CA3 interneurons, thereby contributing to the selection of pyramidal cell assemblies at the theta trough via disinhibition.

Highlights

Activity in the hippocampal CA1 area is spatially and temporally tuned during context-dependent behavior and the spiking of pyramidal cells and interneurons is organized within theta and gamma frequency oscillatory timescales
Subpopulations of medial septal (MS) Rhythmic Neurons Based on Spike Train Dynamics: Teevra and Komal Neurons Using multichannel extracellular probes, we recorded neuronal activity in the septum of head-fixed mice (n = 7) during running (RUN) and pauses (REST) while they navigated on a virtual linear maze
MS neurons differed from adjacent lateral septal (LS) neurons both by their firing rate during locomotion and phase coupling to local field potential (LFP) theta oscillations in CA1

Summary

Introduction

Activity in the hippocampal CA1 area is spatially and temporally tuned during context-dependent behavior and the spiking of pyramidal cells and interneurons is organized within theta and gamma frequency oscillatory timescales This temporal organization is supported by well-characterized glutamatergic projections from CA3 (Amaral and Witter, 1989; Middleton and McHugh, 2016) as well as from the entorhinal cortex (EC) (Brun et al, 2008; Witter et al, 1988). These inputs mediate both dendritic excitation and feedforward inhibition (Buzsaki 1984) of pyramidal cells. The organization of MS inputs to hippocampal or cortical areas at single-cell resolution are largely unknown

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