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.
Highlights
A primary goal of olfaction research is to understand how complex olfactory scenes that occur in natural environment are processed by the olfactory system, in particular for orientation behaviors to odor sources
We show that the moth olfactory system encodes olfactory scenes simulating variable distances from the odor source by characterizing puff onsets and offsets
We focus on how olfactory receptor neurons (ORNs) and antennal lobe projection neurons (PNs) encode the temporal characteristics of the pheromone plume in the Noctuid moth Agrotis ipsilon
Summary
A primary goal of olfaction research is to understand how complex olfactory scenes that occur in natural environment are processed by the olfactory system, in particular for orientation behaviors to odor sources. Until recently natural odor stimuli were not described quantitatively. Most studies of olfactory physiology are restricted to static and whitenoise stimuli, limiting our understanding of dynamic olfactory coding. Realistic olfactory input signals were used to analyze olfactory coding [1,2,3], they were uncontrolled, so preventing to explore specific features of the olfactory signals and large distances to the odor source. A recent paper generated naturalistic odor plumes and described how adaption from olfactory receptor neurons (ORNs) to stimulus mean and variance contribute to encode intermittent odor stimuli [4]. We pursue a novel approach to the study of olfactory coding
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