The nonapeptides oxytocin and vasopressin have been implicated in a variety of social behaviors. In zebra finches, oxytocin antagonists decrease pairing in both sexes, and pairing, in turn, increases expression of both mesotocin (the avian homologue of oxytocin) and vasotocin (the avian homologue of vasopressin). Increases in mesotocin and vasotocin mRNA are correlated with the amount of directed singing by males. Thus, in the present study, we examined the hypothesis that activation of cells containing nonapeptide receptors in song-related regions (ventral tegmental area, lateral septum, and medial preoptic nucleus) would also be correlated with directed singing in males. To rule out the possibility that these regions are involved in general pairing motivation, we also included females as subjects. In the ventral tegmental area, males had higher ZENK and V1aR than females and paired animals (regardless of sex) had higher ZENK and V1aR than did unpaired animals. In the medial preoptic nucleus, paired animals had higher ZENK than did unpaired animals, and there were no sex or pairing effects in the lateral septum. Only ZENK + V1aR in the medial preoptic nucleus was correlated with singing in males. These findings suggest that pairing is associated activation of nonapeptide receptors in the ventral tegmental area and the medial preoptic nucleus, but there is only partial evidence that courtship singing accounts for these findings.