Tissue-Specific Activation of a Single Gustatory Receptor Produces Opposing Behavioral Responses in Drosophila

Abstract

Understanding sensory systems that perceive environmental inputs and neural circuits that select appropriate motor outputs is essential for studying how organisms modulate behavior and make decisions necessary for survival. Drosophila melanogaster oviposition is one such important behavior, in which females evaluate their environment and choose to lay eggs on substrates they may find aversive in other contexts. We employed neurogenetic techniques to characterize neurons that influence the choice between repulsive positional and attractive egg-laying responses toward the bitter-tasting compound lobeline. Surprisingly, we found that neurons expressing Gr66a, a gustatory receptor normally involved in avoidance behaviors, receive input for both attractive and aversive preferences. We hypothesized that these opposing responses may result from activation of distinct Gr66a-expressing neurons. Using tissue-specific rescue experiments, we found that Gr66a-expressing neurons on the legs mediate positional aversion. In contrast, pharyngeal taste cells mediate the egg-laying attraction to lobeline, as determined by analysis of mosaic flies in which subsets of Gr66a neurons were silenced. Finally, inactivating mushroom body neurons disrupted both aversive and attractive responses, suggesting that this brain structure is a candidate integration center for decision-making during Drosophila oviposition. We thus define sensory and central neurons critical to the process by which flies decide where to lay an egg. Furthermore, our findings provide insights into the complex nature of gustatory perception in Drosophila. We show that tissue-specific activation of bitter-sensing Gr66a neurons provides one mechanism by which the gustatory system differentially encodes aversive and attractive responses, allowing the female fly to modulate her behavior in a context-dependent manner.

Molecular and Cellular Organization of Taste Neurons in Adult Drosophila Pharynx

“…It is possible that these pharyngeal taste neurons may be involved in other behaviors, such as choice of oviposition substrate, as has been reported for Gr66a (Joseph and Heberlein, 2012). Alternatively, their roles in feeding behaviors may be dependent on the context, such as prior experience, internal state, or complexity of food substrate.…”

Competing dopamine neurons drive oviposition choice for ethanol in Drosophila

“…Despite the strong drive to lay eggs on a suitable substrate, the flies' choice to dwell on this substrate is uncorrelated. For example, whereas flies prefer to lay eggs on a food containing either acetic acid or lobeline, they show positional avoidance of the same substrates (15,25). To test whether this was also the case for ethanol, we tested the relationship between oviposition and positional preference (0% vs. 5%; Fig.…”

Diverse roles for theDrosophilafructose sensor Gr43a

“…13 The only established role for pharyngeal taste neurons has been reported for the VCSO, where bitter sensing (Gr66a expressing) neurons contribute to egg laying preference on lobeline containing food substrates. 19 This is interesting, because bitter chemicals sensed by labial or tarsal neurons suppress feeding responses in proboscis extension reflex (PER) assays. 20 Regardless, we observed no co-expression between Gr43a and Gr66a in any pharyngeal taste neurons.…”