Abstract

Juxtaglomerular neurons represent one of the largest cellular populations in the mammalian olfactory bulb yet their role for signal processing remains unclear. We used two-photon imaging and electrophysiological recordings to clarify the in vivo properties of these cells and their functional organization in the juxtaglomerular space. Juxtaglomerular neurons coded for many perceptual characteristics of the olfactory stimulus such as (1) identity of the odorant, (2) odorant concentration, (3) odorant onset, and (4) offset. The odor-responsive neurons clustered within a narrow area surrounding the glomerulus with the same odorant specificity, with ~80% of responding cells located ≤20 μm from the glomerular border. This stereotypic spatial pattern of activated cells persisted at different odorant concentrations and was found for neurons both activated and inhibited by the odorant. Our data identify a principal glomerulus with a narrow shell of juxtaglomerular neurons as a basic odor coding unit in the glomerular layer and underline the important role of intraglomerular circuitry.

Highlights

  • The mammalian olfactory epithelium consists of a single layer of non-interacting olfactory receptor neurons (ORNs)

  • We show that juxtaglomerular neurons code for many perceptual characteristics of the olfactory stimulus including the identity of the odorant, odorant concentration as well as onset and offset of the odorant application

  • The spontaneous activity of juxtaglomerular neurons can be entrained by spontaneous firing of olfactory sensory neurons (Duchamp-Viret et al, 1999; Tan et al, 2010) and/or can result from intrinsic/synaptic activity within the local glomerular network (Hayar et al, 2004; Pignatelli et al, 2005; Liu and Shipley, 2008; De Saint Jan et al, 2009; Stakic et al, 2011)

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Summary

Introduction

The mammalian olfactory epithelium consists of a single layer of non-interacting olfactory receptor neurons (ORNs). Each ORN typically expresses only one type of olfactory receptor protein (Chess et al, 1994; Serizawa et al, 2000), which defines its odorant selectivity. Axons of thousands of ORNs expressing the same olfactory receptor protein converge onto a few (usually two) discrete glomeruli in one olfactory bulb (Vassar et al, 1994; Mombaerts et al, 1996). In the glomeruli the ORN axons synapse on the principal mitral/tufted neurons of the bulb and on local interneurons. The juxtaglomerular neurons have rich synaptic connections with each other They target both input [ORN axon terminals (Aroniadou-Anderjaska et al, 2000; McGann et al, 2005; Murphy et al, 2005)] and output (mitral/tufted) neurons of the bulb

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