Task-specific roles of local interneurons for inter- and intraglomerular signaling in the insect antennal lobe.

Debora Fusca,Peter Kloppenburg

doi:10.7554/elife.65217

Abstract

Local interneurons (LNs) mediate complex interactions within the antennal lobe, the primary olfactory system of insects, and the functional analog of the vertebrate olfactory bulb. In the cockroach Periplaneta americana, as in other insects, several types of LNs with distinctive physiological and morphological properties can be defined. Here, we combined whole-cell patch-clamp recordings and Ca2+ imaging of individual LNs to analyze the role of spiking and nonspiking LNs in inter- and intraglomerular signaling during olfactory information processing. Spiking GABAergic LNs reacted to odorant stimulation with a uniform rise in [Ca2+]i in the ramifications of all innervated glomeruli. In contrast, in nonspiking LNs, glomerular Ca2+ signals were odorant specific and varied between glomeruli, resulting in distinct, glomerulus-specific tuning curves. The cell type-specific differences in Ca2+ dynamics support the idea that spiking LNs play a primary role in interglomerular signaling, while they assign nonspiking LNs an essential role in intraglomerular signaling.

Highlights

Local interneurons (LNs) with markedly different functional phenotypes are crucial for odor information processing in the insect antennal lobe (AL)
This study investigated the role of spiking and nonspiking LNs for inter- and intraglomerular signaling during olfactory information processing
Local interneurons of the insect AL are a heterogeneous group of neurons, consisting of different neuronal subpopulations with clearly defined, sometimes fundamentally different functional phenotypes

Summary

Introduction

Local interneurons (LNs) with markedly different functional phenotypes are crucial for odor information processing in the insect antennal lobe (AL). The LNs in the AL are the functional equivalent of granule cells, and periglomerular and short axon cells in the vertebrate olfactory bulb (Ennis et al, 2015; Shepherd et al, 2004) They help to structure the odor representation in the AL, shaping the tuning profiles of the olfactory projection (output) neurons. LNs originally have been characterized as GABAergic and multiglomerular (Distler, 1989; Hoskins et al, 1986; Waldrop et al, 1987) They can generate Na+-driven action potentials (Chou et al, 2010; Christensen et al, 1993; Husch et al, 2009a; Seki et al, 2010) or Ca2+-driven spikelets (Laurent and Davidowitz, 1994). They can be excitatory, distributing excitatory synaptic input to (projection) neurons in other glomeruli (Assisi et al, 2012; Huang et al, 2010; Yaksi and Wilson, 2010)

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