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Morphometric disparities between grouped Drosophila olfactory receptor neurons revealed using a novel electron microscopy method

Abstract

Olfactory receptor neurons (ORNs) housed in the same sensory hair in Drosophila can inhibit each other through direct electrical interactions, termed ephaptic interactions. A systematic electrophysiological survey conducted in our lab showed that neighboring ORNs have different electrotonic properties in most sensilla, indicating that ephaptic interactions between these neurons are asymmetric. We hypothesized that the asymmetry arises from the size differences between grouped ORNs. To test the hypothesis, we developed a versatile and widely applicable method, termed CryoChem, to enable genetically labeled cellular structures to be faithfully preserved using cryofixation and then imaged with 3D electron microscopy (EM) techniques. By combining CryoChem and serial block-face scanning electron microscopy (SBEM), we imaged and generated 3D reconstructions of genetically identified ORNs and their neighboring neurons housed in the same sensory hair. Our morphometric analysis reveals that the sizes of neighboring ORNs are indeed different. The physically larger ORN in a pair is the dominant neuron in ephaptic interactions. In addition, our electric circuit model suggests that the size difference between compartmentalized ORNs is a key factor driving the asymmetry observed empirically. The findings of this study provide insight into how morphometric features of a neuron can directly impact circuit interactions in other ephaptic environments.

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