Control of Drosophila Courtship by Mating Drive

Abstract

Most behaviors are not just actions and reactions, but are the result of self-evaluation and are the means of self-fulfillment. This means that the same external context (e.g. food) can hold different meaning to an animal depending on its internal context (e.g. Am I hungry?). The nervous system creates motivational states such as hunger and thirst to reflect an animal’s physiological needs and to catalyze the context-to-behavior translations. I have developed a model to study how mating drive emerges from neuronal circuitry to impact courtship behaviors in male Drosophila. I show, for the first time, that male flies have a transiently and cumulatively reduced mating drive after repeated matings. Mating drive is encoded by dedicated dopaminergic neurons in the fly brain, whose activity is reduced after matings. This dopaminergic activity gates courtship initiation by influencing P1 neurons, which also integrate sensory information about females and command the initiation of courtship. Mating drive therefore converges with sensory information about females at the point of behavioral selection. I next show that motivation controls the propensity to initiate courtship by desensitizing P1 neurons to the inhibitory component of sensory stimulation. The same motivational signal also prolongs courtship by promoting recurrent excitation at the P1 locus, thereby coordinating the initiation and maintenance of a behavior. Finally, I map out the upstream, sexually dimorphic circuitry that updates the motivational dopaminergic activity during matings, in order to ensure that the male reaches satiety after exhausting his reproductive capacity. I found that the inhibitory products (e.g., the channel Task7) that are made during high motivation also dampen the recovery of circuit activity, matching the 3-day recovery of the male’s reproductive capacity. Taken together, this neuronal architecture instantiates the full cycle of motivational control, where prior behavioral outcomes tune the current drive state and bias future behavioral choices.