Neural circuit mechanisms linking courtship and reward in Drosophila males

Courtship has evolved to achieve reproductive success in animal species. However, whether courtship itself has a positive value remains unclear. In the present work, we report that courtship is innately rewarding and can induce the expression of appetitive short-term memory (STM) and long-term memory (LTM) in Drosophila melanogaster males. Activation of male-specific P1 neurons is sufficient to mimic courtship-induced preference and memory performance. Surprisingly, P1 neurons functionally connect to a large proportion of dopaminergic neurons (DANs) in the protocerebral anterior medial (PAM) cluster. The acquisition of STM and LTM depends on two distinct subsets of PAM DANs that convey the courtship-reward signal to the restricted regions of the mushroom body (MB) γ and α/β lobes through two dopamine receptors, D1-like Dop1R1 and D2-like Dop2R. Furthermore, the retrieval of STM stored in the MB α′/β′ lobe and LTM stored in the MB α/β lobe relies on two distinct MB output neurons. Finally, LTM consolidation requires two subsets of PAM DANs projecting to the MB α/β lobe and corresponding MB output neurons. Taken together, our findings demonstrate that courtship is a potent rewarding stimulus and reveal the underlying neural circuit mechanisms linking courtship and reward in Drosophila males. [Display omitted] •Courtship behavior has a positive value for Drosophila males•P1 neuron activation induces a courtship-reward state by activating PAM DANs•Memory acquisition and retrieval separately utilize specific PAM DANs and MBONs•Memory consolidation requires specific PAM DANs and corresponding MBONs Shen et al. demonstrate that courtship is a strong reward in Drosophila males and drives the formation of olfactory associative learning and memory. They find that P1 neurons directly activate PAM dopaminergic neurons to trigger a reward state and further reveal the neural circuits involved in courtship-reward memory expression.