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

• Published in: bioRxiv
• Main Authors: Boehm, Ariane C, Friedrich, Anja B, Hunt, Sydney, Bandow, Paul, Kp Siju, De Backer, Jean-Francois, Claussen, Julia, Marie-Helen Link, Hofmann, Thomas F, Dawid, Corinna, Ilona C Grunwald Kadow
• Format: Paper
• Language: English
• Published: Cold Spring Harbor Cold Spring Harbor Laboratory Press 29.07.2022
• Subjects: Animal reproduction; Behavior; Brain; Calcium imaging; Dopamine; Dopamine receptors; Drosophila; Electron microscopy; Females; Insects; Luteinizing hormone; Mushroom bodies; Neuroimaging; Neurons; Olfactory system; Pheromones; Polyamines; Reproductive behavior; State-dependent behavior; Synapses
• DOI: 10.1101/2021.07.24.453623

Motherhood induces a drastic, sometimes long-lasting, change in internal state and behavior in most 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 beta prime 1 compartment are sufficient to replace mating experience in virgin females inducing the lasting behavioral increase in polyamine preference. We further show that MB output neurons (MBON) of the beta prime 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 beta prime 2 compartment enables expression of high polyamine 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. Competing Interest Statement The authors have declared no competing interest. Footnotes * We have revised the text extensively and added new data and interpretation to the discussion.