Neural circuit mechanisms of sexual receptivity in Drosophila females

Choosing a mate is one of the most consequential decisions a female will make during her lifetime. This is particularly true for species in which females either mate repeatedly with the same partner or mate infrequently but use the sperm from a single copulation to fertilize eggs over an extended period of time. Drosophila melanogaster uses the latter strategy. Here, we characterize the neural circuitry that implements mating decisions in the female brain. A female fly signals her mating choice by opening her vaginal plates to allow a courting male to copulate1,2. Vaginal plate opening (VPO) occurs in response to the male courtship song and is dependent upon the female's mating status. We sought to understand how these exteroceptive (song) and interoceptive (mating status) inputs are integrated to control VPO. We show that VPO is triggered by a pair of female-specific descending neurons, the vpoDNs. The vpoDNs receive excitatory input from vpoEN auditory neurons, which are tuned to specific features of the melanogaster song. The song responses of vpoDNs, but not vpoENs, are attenuated upon mating, accounting for the reduced receptivity of mated females. This modulation is mediated by pC1 neurons, which encode the females mating status3,4 and also provide excitatory input to vpoDNs. The vpoDNs thus directly integrate the external and internal signals to control the mating decisions of Drosophila females.