Functional integration of a serotonergic neuron in the Drosophila antennal lobe.

Xiaonan Zhang,Quentin Gaudry

doi:10.7554/elife.16836

Abstract

Serotonin plays a critical role in regulating many behaviors that rely on olfaction and recently there has been great effort in determining how this molecule functions in vivo. However, it remains unknown how serotonergic neurons that innervate the first olfactory relay respond to odor stimulation and how they integrate synaptically into local circuits. We examined the sole pair of serotonergic neurons that innervates the Drosophila antennal lobe (the first olfactory relay) to characterize their physiology, connectivity, and contribution to pheromone processing. We report that nearly all odors inhibit these cells, likely through connections made reciprocally within the antennal lobe. Pharmacological and immunohistochemical analyses reveal that these neurons likely release acetylcholine in addition to serotonin and that exogenous and endogenous serotonin have opposing effects on olfactory responses. Finally, we show that activation of the entire serotonergic network, as opposed to only activation of those fibers innervating the antennal lobe, may be required for persistent serotonergic modulation of pheromone responses in the antennal lobe.

Highlights

We report that despite the contralaterally-projecting serotonin-immunoreactive deuterocerebral interneurons (CSDns) being the only serotonergic neurons to project to the antennal lobes (AL), robust modulation of glomeruli that respond to the male pheromone, 11-cisvaccenyl acetate, is only observed when the entire serotonergic network is stimulated in unison, rather than sole activation of the CSDns
We first performed whole-cell recordings from the CSDn to determine if odor stimulation could drive serotonin release into the antennal lobe in a fast and transient manner
We capitalized on the fact that only one pair of serotonergic neurons project to the Drosophila AL to examine how such neurons integrate into primary olfactory structures and regulate pheromone processing

Summary

Introduction

Serotonin (5-HT) is a ubiquitous neuromodulator that is found throughout phylogeny where it alters sensory (Cornide-Petronio et al, 2015; Fields, 2004; Gaudry and Kristan, 2009; Yokogawa et al, 2012), motor (Lillvis and Katz, 2013; Schwartz et al, 2005), and cognitive function (Meneses and Liy-Salmeron, 2012; Sitaraman et al, 2008; Yuan et al, 2005). While progress has been made towards these goals, it still remains unclear how endogenous serotonin is released into olfactory circuits and how it shapes odor responses. Serotonergic neurons in both mammals and insects show stimulus evoked responses (Ranade and Mainen, 2009; Hill et al, 2002; Cohen et al, 2015), but in no phylogenetic group have the odor responses been comprehensively mapped for serotonergic neurons that project to the first olfactory relay. Knowing how serotonin release correlates with olfactory sampling is critical for forming physiological models of 5-HT function in olfaction. Serotonin may serve as a gain control mechanism in the bulb if it is released during olfactory sampling, or it may boost olfactory responses should olfactory stimuli inhibit serotonergic fibers within the bulb(Dugueand Mainen, 2009)

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Results

Conclusion