The medial bed nucleus of the stria terminalis (BSTm) influences both social approach and social aversion, suggesting that this structure may play an important role in generating motivational and behavioral differences between gregarious and asocial species. However, no specific neurons have been identified within the BSTm that influence species-typical levels of sociality or that mediate approach and avoidance. Using five songbird species that differ selectively in their species-typical group sizes, we now demonstrate that vasotocin-immunoreactive (VT-ir) neurons of the BSTm exhibit very different immediate early gene responses to same-sex stimuli in gregarious and asocial species. Exposure to a same-sex conspecific increases VT-Fos colocalization in gregarious species while decreasing colocalization in relatively asocial species. We additionally demonstrate that these neurons are selectively activated by social stimuli that normally elicit affiliation (positively valenced social stimuli) but not by stimuli that elicit aversion (negatively valenced social stimuli). Constitutive Fos activity of the VT-ir neurons is also significantly greater in the gregarious species, and the two most social species express significantly more VT-ir neurons. These findings demonstrate that the properties of valence-sensitive neurons evolve in relation to sociality and indicate that gregarious species accentuate positive stimulus properties during social interactions.amygdala ͉ sociality ͉ vasopressin ͉ vasotocin T he medial bed nucleus of the stria terminalis (BSTm) is anatomically and functionally conserved in the land vertebrate classes (1-3), and in virtually all species, a subpopulation of BSTm neurons produce vasotocin (VT) or its mammalian homologue vasopressin (VP) (4, 5) (see Fig. 1). These neurons project to multiple areas of the basal forebrain [e.g., ventral pallidum and lateral septum (5, 6)], where VT͞VP influences a variety of social behaviors, sometimes in a potent and highly species-specific manner (4,7,8). For instance, differential expression of V 1a receptors in the ventral pallidum is both necessary and sufficient to account for species differences in monogamous pair-bonding (9), and V 1a receptors in the lateral septum are both necessary and sufficient for the display of social recognition in mice (10). However, despite the vast literature on VT͞VP functions, receptor distributions, sexual dimorphisms, and steroid sensitivities (4,5,7,8), almost nothing is known about BSTm VT͞VP neuronal activity as it relates to stimulus parameters, social context, and species-specific aspects of social structure. Indeed, to our knowledge, the only relevant data come from monogamous male voles, in which VP mRNA increases in the BSTm after cohabitation with a female (11).The present experiments were therefore conducted to test the hypotheses that (i) VT-immunoreactive (VT-ir) neurons in the BSTm are responsive to stimuli that elicit affiliation, and (ii) responses of these neurons evolve in relation to sociality. These hypoth...