Hypothalamic oxytocin and vasopressin neurons exert sex-specific effects on pair bonding, gregariousness, and aggression in finches

Abstract

Antagonism of oxytocin (OT) receptors (OTRs) impairs the formation of pair bonds in prairie voles (Microtus ochrogaster) and zebra finches (Taenioypygia guttata), and also reduces the preference for the larger of two groups ("gregariousness") in finches. These effects tend to be stronger in females. The contributions of specific peptide cell groups to these processes remain unknown, however. This issue is complicated by the fact that OTRs in finches and voles bind not only forms of OT, but also vasopressin (VP), and >10 cell groups produce each peptide in any given species. Using RNA interference, we found that knockdown of VP and OT production in the paraventricular nucleus of the hypothalamus exerts diverse behavioral effects in zebra finches, most of which are sexually differentiated. Our data show that knockdown of VP production significantly reduces gregariousness in both sexes and exerts sex-specific effects on aggression directed toward opposite-sex birds (increases in males; decreases in females), whereas OT knockdown produces female-specific deficits in gregariousness, pair bonding, and nest cup ownership; reduces side-by-side perching in both sexes; modulates stress coping; and induces hyperphagia in males. These findings demonstrate that paraventricular neurons are major contributors to the effects of VP-OT peptides on pair bonding and gregariousness; reveal previously unknown effects of sex-specific peptide on opposite-sex aggression; and demonstrate a surprising lack of effects on same-sex aggression. Finally, the observed effects of OT knockdown on feeding and stress coping parallel findings in mammals, suggesting that OT modulation of these processes is evolutionarily conserved across the amniote vertebrate classes.