Shaping of olfactory responses by taste in a new assay for operant learning in <i>Drosophila melanogaster</i>

Animals are driven to maximize food rewards and adjust their behavior to seek high-quality food and avoid low-quality options. This holds true for Drosophila melanogaster, which approaches food-associated odors and tastes while avoiding aversive ones. Despite its importance for understanding motivation, how voluntary olfactory and gustatory experiences shape fly interactions with these stimuli over time remains unclear. Here, we investigate how stimuli shape volitional behavior using our novel operant learning assay (Open-LA), which tracks individual flies as they enter/exit a region of stimuli self-administration. We analyzed the behaviors flies demonstrated when they control access to an aversive or appetitive odor or taste and analyzed how these behaviors were shaped by experience. As predicted, flies pursued apple cider vinegar and avoided benzaldehyde and showed rapid operant learning for both odors. Flies also self-administered both simulated sweet and bitter taste, which slightly altered aversive odor responses, but did not strongly enhance odor-based operant learning. These data suggest olfaction is the primary sense guiding volitional behaviors and provides a behavioral framework for examining how animals pursue positive and avoid negative stimuli.