Chemosensory Coding by Neurons in the Coeloconic Sensilla of theDrosophilaAntenna

Abstract

Odor coding is based on the diverse sensitivities and response properties of olfactory receptor neurons (ORNs). In the Drosophila antenna, ORNs are housed in three major morphological types of sensilla. Although investigation of the Drosophila olfactory system has been expanding rapidly, the ORNs in one of these types, the coeloconic sensilla, have been essentially unexplored. We define four functional types of coeloconic sensilla through extracellular physiological recordings. Each type contains at least two neurons, with a total of at least seven distinct ORN classes that vary remarkably in their breadth of tuning. Analysis of 315 odorant-ORN combinations reveals how these neurons sample odor space via both excitation and inhibition. We identify a class of neurons that is narrowly tuned to small amines, and we find humidity detectors that define a cellular basis for hygroreception in Drosophila. The temporal dynamics of responses vary widely, enhancing the potential for complexity in the odor code. Molecular and genetic analysis shows that a broadly tuned ORN, antennal coeloconic 3B (ac3B), requires the odor receptor gene Or35a for its response in vivo. The activity of ac3B is not required for the response of the other ORN within that sensillum, ac3A. The functional analysis presented here, revealing a combination of highly specialized neurons and a broadly tuned ORN, along with the ancient origin of coeloconic sensilla, suggests that the specificities of these ORNs may reflect basic needs of an ancestral insect.