Parallel encoding of CO2 in attractive and aversive glomeruli by selective lateral signaling between olfactory afferents

Abstract

We describe a novel form of selective crosstalk between specific classes of primary olfactory receptor neurons (ORNs) in the Drosophila antennal lobe. Neurotransmitter release from ORNs is driven by two distinct sources of excitation: direct activity derived from the odorant receptor and stimulus-selective lateral signals originating from stereotypic subsets of other ORNs. Consequently, the level of presynaptic neurotransmitter release from an ORN can be significantly dissociated from its firing rate. Stimulus-selective lateral signaling results in the distributed representation of CO2-a behaviorally important environmental cue that directly excites a single ORN class-in multiple olfactory glomeruli, each with distinct response dynamics. CO2-sensitive glomeruli coupled to behavioral attraction respond preferentially to fast changes in CO2 concentration, whereas those coupled to behavioral aversion more closely follow absolute levels of CO2. Behavioral responses to CO2 also depend on the temporal structure of the stimulus: flies walk upwind to fluctuating, but not sustained, pulses of CO2. Stimulus-selective lateral signaling generalizes to additional odors and glomeruli, revealing a subnetwork of lateral interactions between ORNs that reshapes the spatial and temporal structure of odor representations in a stimulus-specific manner.