A dopamine-gated learning circuit underpins reproductive state-dependent odor preference in Drosophila females

Abstract

Motherhood induces a drastic, sometimes long-lasting, change in internal state and behavior in most female animals. Here, we show that a mating-induced increase in olfactory attraction of female Drosophila flies to nutrients relies on interconnected neural pathways in the two higher olfactory brain regions, the lateral horn (LH) and the mushroom body (MB). Using whole brain calcium imaging, we find that mating does not induce a global change in the activity of the whole brain nor of entire brain regions, suggesting specific neuronal or network changes in the olfactory system. Systematic behavioral screening and electron microscopy (EM) connectomics identify two types of LH output neurons required for the attraction of females to polyamines -one of them previously implicated in the processing of male pheromones. In addition, we characterize multiple MB pathways capable of inducing or suppressing polyamine attraction, with synaptic connections to the identified LH neurons and a prominent role for the β′1 compartment. Moreover, β′1 dopaminergic neurons are modulated by mating and are sufficient to replace mating experience in virgins inducing the lasting behavioral switch in female preference. Taken together, our data in the fly suggests that reproductive state-dependent expression of female choice behavior is regulated by a dopamine-gated distributed learning circuit comprising both higher olfactory brain centers.