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During nest building in zebra finches (Taeniopygia guttata), several regions in the social behaviour network and the dopaminergic reward system, two neural circuits involved in social behaviour, appear to be active in male and female nest-building finches. As the nonapeptides mesotocin and vasotocin, and the neurotransmitter dopamine, play important roles in avian social behaviour, we tested the hypothesis that mesotocinergic-vasotocinergic and dopaminergic neuronal populations in the social behaviour network and dopaminergic reward system, respectively, are active during nest building. We combined immunohistochemistry for Fos (an indirect marker of neuronal activity) and arginine vasotocin, mesotocin, or tyrosine hydroxylase on brain tissue from nest-building and non-nest-building male and female zebra finches and compared Fos immunoreactivity in these neuronal populations with the variation in nest-building behaviour. Fos immunoreactivity in all three types of neuronal populations increased with some aspect of nest building: (1) higher immunoreactivity in a mesotocinergic neuronal population of nest-building finches compared to controls; (2) increased immunoreactivity in the vasotocinergic neuronal populations the more material picked up by nest-building males and the more time a male spent in the nest with his mate, and (3) increased immunoreactivity in a dopaminergic neuronal population the longer a male nest-building finch spent in the nest with his mate. Together these findings provide evidence for a role of the mesotocinergic-vasotocinergic and dopaminergic systems in avian nest building. This article is protected by copyright. All rights reserved.