Pharyngeal Taste in Drosophila – From Periphery to Brain
Feeding behaviors, guided by the taste system, serve universal and essential functions in animals. The availability of molecular genetic tools and assays to measure behavioral outcomes at high resolution in real time have made the fly, Drosophila melanogaster, an invaluable model to identify molecular components and dissect circuit logic of how the quality and quantity of ingested food is controlled. However, most investigations of taste responses have focused on neurons residing in external taste hairs in the labellum, legs, and wing margins. There remains a complex repertoire of pharyngeal taste neurons lying in an anatomical position to control food intake, which has been largely overlooked. This comparatively limited knowledge of the molecular or functional nature of internal taste neurons in the pharynx represents a critical missing link between taste sensory input and feeding behavior output. Notably, taste-guided feeding behaviors of insect disease vectors and pests impose a substantial economic and health burden in the world. An understanding of taste circuits that regulate feeding may lead to the development of behavior-modifying strategies for insect control. In this dissertation, I present a receptor-to-neuron map for all pharyngeal organs, comprising in a genetic toolkit that allows manipulation of specific cell types in the pharynx, and genetic dissection experiments to assess the roles of selected classes of pharyngeal taste neurons in food selection and intake. The results uncover mechanisms of combinatorial taste coding in pharyngeal taste neurons that mediate feeding avoidance of aversive compounds such as bitter compounds, acids, and high salts. I then report the development of a taste-blind system to examine function of individual classes of pharyngeal taste neurons in controlling food intake of appetitive tastants, such as sugars and amino acids. Finally, I describe efforts to identify potential higher-order brain neurons that control feeding behaviors, and discovery of a subset of brain neurons that might receive pharyngeal input and mediate regurgitation behavior. Taking advantage of tools established by this study for probing pharyngeal function, future investigations can accomplish a systems-level analysis of pharyngeal taste neurons and circuits, and explore functional intersections between taste input and neuroendocrine function in the brain towards guiding feeding behaviors.