Early warning signals regarding environmental suitability in the Drosophila antenna

Abstract

HighlightsA novel geotaxis assay showed high intensity odorant exposures are harmful to fliesRepulsion at high odor intensities can be a protective mechanismOlfactory receptor neuron (ORN) excitability abruptly changes with odor intensityA linear combination of ORN activities can robustly predict intensity-dependent behavioral repulsionSummaryThe olfactory system is uniquely positioned to warn an organism of environmental threats. Whether and how it encodes such information is not understood. Here, we examined this issue in the fruit fly Drosophila melanogaster. We found that intensity-dependent repulsion to chemicals safeguarded flies from harmful, high-intensity vapor exposures. To understand how sensory input changed as the odor valence switched from innocuous to threatening, we recorded from olfactory receptor neurons (ORNs) in the fly antenna. Primarily, we observed two response non-linearities: recruitment of non-active ORNs at higher intensities, and abrupt transitions in neural excitability from regular spiking to high-firing oscillatory regime. Although non-linearities observed in any single ORN was not a good indicator, a simple linear combination of firing events from multiple neurons provided robust recognition of threating/repulsive olfactory stimuli. In sum, our results reveal how information necessary to avoid environmental threats may also be encoded in the insect antenna.