Motherhood induces a drastic, sometimes long-lasting, change in internal state and behavior in many female animals. How a change in reproductive state or the discrete event of mating modulates specific female behaviors is still incompletely understood. Using calcium imaging of the whole brain of Drosophila females, we find that mating does not induce a global change in brain activity. Instead, mating modulates the pheromone response of dopaminergic neurons innervating the fly's learning and memory center, the mushroom body (MB). Using the mating-induced increased attraction to the odor of important nutrients, polyamines, we show that disruption of the female fly's ability to smell, for instance the pheromone cVA, during mating leads to a reduction in polyamine preference for days later indicating that the odor environment at mating lastingly influences female perception and choice behavior. Moreover, dopaminergic neurons including innervation of the β'1 compartment are sufficient to induce the lasting behavioral increase in polyamine preference. We further show that MB output neurons (MBON) of the β'1 compartment are activated by pheromone odor and their activity during mating bidirectionally modulates preference behavior in mated and virgin females. Their activity is not required, however, for the expression of polyamine attraction. Instead, inhibition of another type of MBON innervating the β'2 compartment enables expression of high odor attraction. In addition, the response of a lateral horn (LH) neuron, AD1b2, which output is required for the expression of polyamine attraction, shows a modulated polyamine response after mating. Taken together, our data in the fly suggests that mating-related sensory experience regulates female odor perception and expression of choice behavior through a dopamine-gated learning circuit.

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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.