Behavior-dependent activity patterns of GABAergic long-range projecting neurons in the rat hippocampus.

Linda Katona,Ornella Valenti,Ben Micklem,Peter Somogyi,Dimitrios Kotzadimitriou,Thomas Klausberger,Tim J Viney,Daniel A Swiejkowski,Zsolt Borhegyi

doi:10.1002/hipo.22696

Abstract

ABSTRACTLong‐range glutamatergic and GABAergic projections participate in temporal coordination of neuronal activity in distributed cortical areas. In the hippocampus, GABAergic neurons project to the medial septum and retrohippocampal areas. Many GABAergic projection cells express somatostatin (SOM+) and, together with locally terminating SOM+ bistratified and O‐LM cells, contribute to dendritic inhibition of pyramidal cells. We tested the hypothesis that diversity in SOM+ cells reflects temporal specialization during behavior using extracellular single cell recording and juxtacellular neurobiotin‐labeling in freely moving rats. We have demonstrated that rare GABAergic projection neurons discharge rhythmically and are remarkably diverse. During sharp wave‐ripples, most projection cells, including a novel SOM+ GABAergic back‐projecting cell, increased their activity similar to bistratified cells, but unlike O‐LM cells. During movement, most projection cells discharged along the descending slope of theta cycles, but some fired at the trough jointly with bistratified and O‐LM cells. The specialization of hippocampal SOM+ projection neurons complements the action of local interneurons in differentially phasing inputs from the CA3 area to CA1 pyramidal cell dendrites during sleep and wakefulness. Our observations suggest that GABAergic projection cells mediate the behavior‐ and network state‐dependent binding of neuronal assemblies amongst functionally‐related brain regions by transmitting local rhythmic entrainment of neurons in CA1 to neuronal populations in other areas. © 2016 The Authors Hippocampus Published by Wiley Periodicals, Inc.

Highlights

Co-ordinated activation of neuronal populations is required for the formation of representations in the cortex and for supporting behavior
The group of unlabeled interneurons recorded in stratum oriens may include O-LM cells (McBain et al, 1994; Maccaferri et al, 2000; Varga et al, 2012; Katona et al, 2014), horizontal bistratified, basket and axo-axonic cells (McBain et al, 1994; Sik et al, 1995; Maccaferri et al, 2000; Losonczy et al, 2002; Ganter et al, 2004; Varga et al, 2014) and various long-range projecting GABAergic cell types (Sik et al, 1994, 1995; Gulyas et al, 2003; Jinno et al, 2007)
Trilaminar cells, a distinct type of projection neuron (Sik et al, 1995; Ferraguti et al, 2005), are not present in this sample, as their prolonged high frequency (>200 Hz) bursts of action potentials is a unique feature of their firing pattern

Summary

Introduction

Co-ordinated activation of neuronal populations is required for the formation of representations in the cortex and for supporting behavior. Oscillatory network states may arise through local interactions and/or through the interactions of different cortical areas mediated via long-range glutamatergic and GABAergic projections (Amaral and Witter, 1989; Caputi et al, 2013). Pyramidal cell activation is governed by glutamatergic inputs from cortical and subcortical areas (Amaral and Witter, 1989; Somogyi et al, 2014) and by neuromodulatory afferents originating in subcortical brain regions. Another major contributor to changes in pyramidal cell excitability is inhibition via subcellular-domain specific GABAergic synaptic innervation. Axo-axonic cells target exclusively the axon initial segment, whereas basket cells innervate cell bodies and proximal dendrites

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Conclusion