Asymmetric ephaptic inhibition between compartmentalized olfactory receptor neurons

Ye Zhang,Eric A Bushong,Mark H Ellisman,Li-An Chu,Tin Ki Tsang,Jürgen Reingruber,Chih-Ying Su,Ann-Shyn Chiang

doi:10.1038/s41467-019-09346-z

Abstract

In the Drosophila antenna, different subtypes of olfactory receptor neurons (ORNs) housed in the same sensory hair (sensillum) can inhibit each other non-synaptically. However, the mechanisms underlying this underexplored form of lateral inhibition remain unclear. Here we use recordings from pairs of sensilla impaled by the same tungsten electrode to demonstrate that direct electrical (“ephaptic”) interactions mediate lateral inhibition between ORNs. Intriguingly, within individual sensilla, we find that ephaptic lateral inhibition is asymmetric such that one ORN exerts greater influence onto its neighbor. Serial block-face scanning electron microscopy of genetically identified ORNs and circuit modeling indicate that asymmetric lateral inhibition reflects a surprisingly simple mechanism: the physically larger ORN in a pair corresponds to the dominant neuron in ephaptic interactions. Thus, morphometric differences between compartmentalized ORNs account for highly specialized inhibitory interactions that govern information processing at the earliest stages of olfactory coding.

Highlights

In the Drosophila antenna, different subtypes of olfactory receptor neurons (ORNs) housed in the same sensory hair can inhibit each other non-synaptically
Taking advantage of the powerful genetic toolkit of Drosophila melanogaster, we showed that olfactory receptor neurons (ORNs) housed in the same sensory hair, or sensillum, can inhibit each other, and that such lateral inhibition can modulate odor-guided behavior[11]
How does one prove that ORNs inhibit each other ephaptically if the inhibition is not mediated by any manipulatable target? We addressed this question by testing whether direct electrical interaction is sufficient to cause inhibition between ORNs

Summary

Introduction

In the Drosophila antenna, different subtypes of olfactory receptor neurons (ORNs) housed in the same sensory hair (sensillum) can inhibit each other non-synaptically. First observed between two axons brought together experimentally[4,5], ephaptic interaction takes place between uninsulated neuronal processes packed into an electrically isolated microenvironment[2,3] Such an arrangement commonly occurs in fascicles containing bundles of unmyelinated axons, such as the mammalian olfactory nerve[6] and the interoceptive sensory system[7], as well as in regions of the nervous system including the fish hindbrain, mammalian cerebellum, hippocampus, and retina[1,2,3,8,9]. Ephaptic interaction is notoriously difficult to study because it is enabled by high extracellular resistance and density of neural membranes[2,3], none of which are amenable to in vivo experimental manipulation It remains unclear whether and how ephaptic interaction by itself is sufficient to influence circuit function. D. melanogaster, the Or22a receptor is expressed in the largespike “A” neuron in the antennal basiconic sensilla of type 3

Methods

Results

Conclusion