In songbirds, a major function of song during the breeding season is mate attraction, and song in this context can be highly sexually motivated. Vocal learning, perception, and production are regulated by the song control system, but there is no evidence that this system participates in the motivation to sing. Instead, brain regions involved in sexual motivation and arousal, including the medial preoptic nucleus (POM), bed nucleus of the stria terminalis (BST), nucleus taeniae (Tn), and area ventralis of Tsai (AVT) might regulate the motivation to sing, at least in a sexual context. The role of these nuclei and song control nuclei (area X and HVC) in vocal production within a breeding context, and other courtship behaviors, was investigated using immunocytochemistry for protein products of immediate early genes (IEGs), ZENK and c-fos (Fos), in flocks of male house sparrows (Passer domesticus) presented with females. Compared to vocalizations from other perches, vocal behavior from a nest box is more likely directed toward females, and sexually motivated. The numbers of ZENK and Fos labeled cells within rostral, but not caudal POM related positively only to vocalizations produced from a nest box. In contrast, the number of ZENK-labeled cells within area X related negatively to vocalizations from a nest box. Additionally, numbers of IEG-labeled cells within rPOM, Tn and AVT related positively to mount attempts. The results support the hypothesis that the POM interacts with the song control system to regulate sexually motivated vocal expression, and are consistent with work indicating that (a) rostral and caudal POM play distinct roles in sexual behavior, and (b) involvement of area X in song is context specific.