Motivational Control of Drosophila Copulation Across Timescales

Abstract

Behavioral choices incorporate information obtained over vastly different timescales: from experiences the animal had days or even years ago, to real-time information about the environment and progress of a behavior. How do the neurons that ultimately make the choice to begin, persist in, or terminate a behavior integrate all this information? The relatively simple brain of the fly – and the still simpler sexually dimorphic circuitry that controls reproductive behavior – presents an opportunity to gain mechanistic insight into how behavior is calibrated to reflect life experience. Courtship emerges over the first three days of life as a male reaches sexual maturity. Once in adulthood, courtship is vigorous until the animal achieves its goal of copulation, after which it is decreased and takes three days to recover. I show that the similarity between these timescales is no coincidence: hormones take advantage of the same neural circuit motifs that regulate satiety after repeatedly mating to implement sexual abstinence in adolescence. I next show that like courtship, the motivation to copulate is changed by recent mating experience. I found that dopaminergic neurons in the ventral nervous system signal through the D2 receptor to the ~8 Copulation Decision Neurons (CDNs), which cause mating termination when pushed past threshold. The immediate consequence of this signaling is the elevation of intracellular CaMKII, whose activity changes the ability of the CDNs to integrate information compelling the male to terminate copulation. The long-term impact of this signaling is that the CDNs become gradually desensitized to motivating dopamine as the animal mates, making both current and future copulations increasingly prone to premature termination when challenged. Finally, I examine the timed progression of the many subcomponents of copulatory behavior. I identify a population of neurons that seem to affect all known aspects of copulation and argue that their role may be to serve as a master timekeeper that regulates the sequence and duration of each event. Together this work surveys how the motivation to mate evolves from the moment a juvenile fly ecloses, through the dynamics of a first mating, and after many mating experiences.