A midbrain-cortical dopamine circuit drives sexually-motivated singing

Adult male zebra finches sing in two distinct social contexts: an “undirected song” produced when in isolation from other birds, and a “directed song” that it sings to a nearby female. Song production is regulated by a specialized vocal motor network (the “song system”), which receives inputs from a variety of neuromodulatory regions that are highly conserved in all vertebrates, and which are likely to provide information to the song system about social context that could drive directed singing. To test this idea, we recorded male zebra finch while they sang in the presence and absence of a female and lesioned either dopamine (DA) terminals in HVC, a part of the song production circuity, or DA cell bodies in the midbrain dopaminergic group A11, an area thought to be involved in social behavior and which is the major dopaminergic input to HVC. Either type of lesion abolished the males’ ability to produce female-directed songs, even though males in both experimental groups continued singing undirected songs. Furthermore, birds with DA lesions in HVC still showed courtship behaviors, including extensive production of introductory notes and orientation to the female. In contrast, birds with DA lesions in A11 failed to orient or call to the female. Finally, we found that when we optogenetically activated A11 terminals in HVC, males sang longer directed-bouts and overall increased their directed-singing rate. Together, these results support the idea that dopaminergic inputs from A11 to HVC in male finches convey a social context-dependent signal important to female-directed singing.