Sexual failure decreases sweet taste perception in male <i>Drosophila</i> via dopaminergic signaling.

Abstract

Sweet taste perception, a critical aspect of the initiation of feeding behavior, is primarily regulated by an animal's internal metabolic state. However, non-metabolic factors, such as motivational and emotional states, can also influence peripheral sensory processing and hence feeding behavior. While mating experience is known to induce motivational and emotional changes, its broader impact on other innate behaviors, such as feeding, remains largely uncharacterized. In this study, we demonstrated that the mating failure of male fruit flies suppressed sweet taste perception via dopamine signaling in specific neural circuitry. Upon repetitive failure in courtship, male flies exhibited a sustained yet reversible decline of sweet taste perception, as measured by the proboscis extension reflex (PER) towards sweet tastants as well as the neuronal activity of sweet-sensing Gr5a⁺ neurons in the proboscis. Mechanistically, we identified a small group of dopaminergic neurons projecting to the subesophageal zone (SEZ) and innervating with Gr5a⁺ neurons as the key modulator. Repetitive sexual failure decreased the activity of these dopaminergic neurons and in turn, suppressed Gr5a⁺ neurons via Dop1R1 and Dop2R receptors. Our findings revealed a critical role for dopaminergic signaling in integrating reproductive experience with appetitive sensory processing, providing new insights into the complex interactions between different innate behaviors and the role of brain's reward systems in regulating internal motivational and emotional states.