Competing Responses to a Single Stimulus Provides a Model for Decision-Making in Drosophila

Proper decision-making is crucial to the day-to-day lives of all organisms, whether the situation requiring a choice be mundane and seemingly trivial, or critical and life-or-death. Simply defined, a decision occurs when an organism is presented with input stimuli that induce multiple alternative responses, but given the situation a single behavioral response can only be selected and executed as motor output. Given its importance, decision-making studies have been performed in numerous organisms, across numerous academic disciplines.One advantage that Drosophila melanogaster possesses as a model organism is the vast array of neurogenetic tools available to answer biological questions. Given the experimental utility of the fruit fly, we set out to use Drosophila to study the behavioral mechanisms and neurophysiology underlying decision-making. We developed a two-choice assay that simultaneously measures the positional aversion and egg-laying attraction responses flies exhibit to a single environmental compound. Using our straightforward yet robust assay, we use acetic acid preferences to substantiate the Drosophila oviposition program as a model for choice-like behavior. Subsequently, we identified a number of genes potentially important to the Drosophila oviposition program, and initially characterized the sensory systems and brain regions mediating these responses.Next, to expand our acetic acid-based model for choice-like behavior into a more general paradigm of decision-making, and to perform more in-depth analysis of the neural circuitry governing this process, we modified our assay to employ bitter-tasting compounds like lobeline that induce contradictory positional and egg-laying responses. Subsequently, we identified the specific sensory neurons that mediate these preferences, and surprisingly find that the same gustatory receptor is required for both responses. We show Drosophila can employ tissue-specific activation of taste-neurons expressing this same receptor complex to elicit these very different and competing behavioral responses. Finally, we identified a higher-order brain structure, the mushroom body, which is an intersection point between the neural circuits governing the competing positional aversion and egg-laying attraction pathways, thereby offering suggestive evidence that the mushroom body is a candidate integration center in a true decision-making process that occurs within the Drosophila oviposition program