Olfactory coding in the turbulent realm

Abstract

Long-distance olfactory search behaviors depend on odor detection dynamics. Due to turbulence, olfactory signals travel as bursts of variable concentration and spacing and are characterized by long-tail distributions of odor/no-odor events, challenging the computing capacities of olfactory systems. How animals encode complex olfactory scenes to track the plume far from the source remains unclear. Here we focus on the coding of the plume temporal dynamics in moths. We compare responses of olfactory receptor neurons (ORNs) and antennal lobe projection neurons (PNs) to sequences of pheromone stimuli either with white-noise patterns or with realistic turbulent temporal structures simulating a large range of distances (8 to 64 m) from the odor source. For the first time, we analyze what information is extracted by the olfactory system at large distances from the source. Neuronal responses are analyzed using linear-nonlinear models fitted with white-noise stimuli and used for predicting responses to turbulent stimuli. We found that neuronal firing rate is less correlated with the dynamic odor time course when distance to the source increases because of improper coding during long odor and no-odor events that characterize large distances. Rapid adaptation during long puffs does not preclude however the detection of puff transitions in PNs. Individual PNs but not individual ORNs encode the onset and offset of odor puffs for any temporal structure of stimuli. A higher spontaneous firing rate coupled to an inhibition phase at the end of PN responses contributes to this coding property. This allows PNs to decode the temporal structure of the odor plume at any distance to the source, an essential piece of information moths can use in their tracking behavior.\n\nAuthor SummaryLong-distance olfactory search is a difficult task because atmospheric turbulence erases global gradients and makes the plume discontinuous. The dynamics of odor detections is the sole information about the position of the source. Male moths successfully track female pheromone plumes at large distances. Here we show that the moth olfactory system encodes olfactory scenes simulating variable distances from the odor source by characterizing puff onsets and offsets. A single projection neuron is sufficient to provide an accurate representation of the dynamic pheromone time course at any distance to the source while this information seems to be encoded at the population level in olfactory receptor neurons.