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 flyDrosophila melanogasterexposed 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.

Bifurcation enhances temporal information encoding in the olfactory periphery

“…For this strategy to be successful, they must extract from the signal not only the intensity of the odor filaments they encounter but also temporal information, such as when and how frequently odor filaments arrive, how long they last, and when they end (Fig. 1A) (4,8,(14)(15)(16)(17)(18)(19)(20). Information about the timing of odor signals is also critical for detecting the direction of motion of odor filaments (21) and resolving odor sources in space (15,17).…”

“…1A) (4,8,(14)(15)(16)(17)(18)(19)(20). Information about the timing of odor signals is also critical for detecting the direction of motion of odor filaments (21) and resolving odor sources in space (15,17). To reliably extract such information from an odor signal, the olfactory system must adapt its sensitivity to the ambient statistics of the odor concentration, which in turbulent plumes can span orders of magnitude (1)(2)(3)22).…”