A neural hub for holistic courtship displays

Courtship displays often involve the concerted production of several distinct courtship behaviors. The neural circuits that enable the concerted production of the component behaviors of a courtship display are not well understood. Here, we identify a midbrain cell group (A11) that enables male zebra finches to produce their learned songs in concert with various other behaviors, including female-directed orientation, pursuit, and calling. Anatomical mapping reveals that A11 is at the center of a complex network including the song premotor nucleus HVC as well as brainstem regions crucial to calling and locomotion. Notably, lesioning A11 terminals in HVC blocked female-directed singing but did not interfere with female-directed calling, orientation, or pursuit. In contrast, lesioning A11 cell bodies strongly reduced and often abolished all female-directed courtship behaviors. However, males with either type of lesion still produced songs when in social isolation. Lastly, imaging calcium-related activity in A11 terminals in HVC showed that during courtship, A11 signals HVC about female-directed calls and during female-directed singing, about the transition from simpler introductory notes to the acoustically more complex syllables that depend intimately on HVC for their production. These results show how a brain region important to reproduction in both birds and mammals enables holistic courtship displays in male zebra finches, which include learning songs, calls, and other non-vocal behaviors.