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 that include learning songs calls and other non-vocal behaviors.
