Ephaptic coupling between olfactory receptor neurons is sensitive to relative stimulus timing: Implications for odour source discrimination

Abstract

Insect olfactory receptor neurons (ORNs) are often co-localized within sensilla and exhibit non-synaptic reciprocal inhibition through ephaptic coupling. It has been postulated that this inhibition aids odour source discrimination, as synchronous arrival of different odour molecules (odorants) from a single source should increase ephaptic inhibition, whereas asynchronous arrival of odorants from different sources should decrease ephaptic inhibition. However, it was as yet unknown whether temporal arrival patterns of different odorants indeed modulate ephaptic inhibition, since past studies have focused on ephaptic inhibition of sustained ORN responses to prolonged and constant odour stimuli. However, most natural odour stimuli are not constant but rather transient and fluctuate as a result of dispersion in turbulent plumes in the air. To investigate the role of ephaptic inhibition in olfaction within turbulent environments, we recorded co-localized ORNs in the fruit fly Drosophila melanogaster exposed to dynamic odorant mixtures. We found that ephaptic inhibition does modulate transient ORN responses, and the strength of ephaptic inhibition decreases as the synchrony between arriving odorants decreases. These results support the hypothesis that ephaptic inhibition aids odour source discrimination.