Diversity of pheromone temporal coding disruptions by plant volatiles

Abstract

Moth pheromone-sensitive olfactory receptor neurons (Phe-ORNs) encode the intermittent structure of pheromone plumes through precisely timed spikes, a mechanism that is essential for odor plume tracking behavior in flying insects. However, natural olfactory scenes are composed of diverse volatile plant compounds (VPCs) with complex temporal dynamics whose effects on pheromone signal intermittency encoding remain unclear. Two lines of research, encoding of pheromone intermittency and background interference, remain largely disconnected. Here, we performed electrophysiological recordings from moth Phe-ORNs to quantify their responses to turbulent plume-like flickering pheromone stimuli in constant or fluctuating backgrounds of a diversity of VPCs. We found that some VPCs reversibly disrupted the temporal coding of various subregions of the pheromone stimulus and the trial-to-trial variability. While Phe-ORN activation by VPCs partially accounted for the decrease in coding performance, Phe-ORN gain reduction was insufficient to explain the full extent of the disruption. Some VPCs disrupt temporal coding without activating Phe-ORNs, and others activate Phe-ORNs without altering temporal coding. A continuous background noise can induce strong adaptation and limit dynamic range, whereas a fluctuating background can interfere with pheromone pulse encoding by disrupting spike timing. Altogether, these results indicate that the pheromone detection system must contend with multiple forms of background noise rather than a uniform disturbance. Timing is key for olfactory navigation, and our results raise questions regarding how downstream circuits would process noisy sensory inputs. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=196 SRC="FIGDIR/small/713794v1_ufig1.gif" ALT="Figure 1"> View larger version (39K): org.highwire.dtl.DTLVardef@1c44fb6org.highwire.dtl.DTLVardef@14d5982org.highwire.dtl.DTLVardef@12f94a2org.highwire.dtl.DTLVardef@c731ee_HPS_FORMAT_FIGEXP M_FIG C_FIG