Context-dependent activation of a social behavior brain network associates with learned vocal production

Abstract

Abstract In zebra finches, an avian brain network for vocal control undergoes context-dependent patterning of song-dependent activation. Previous studies in zebra finches also implicate the importance of dopaminergic input in producing context-appropriate singing behavior. In mice, it has been shown that oxytocinergic neurons originated in the paraventricular nucleus of the hypothalamus (PVN) synapse directly onto dopamine neurons in the ventral tegmental area (VTA), implicating the necessity of oxytocin signaling from the PVN for producing a context-appropriate song. Both avian and non-avian axonal tract-tracing studies indicate high levels of PVN innervation by the social behavior network. Here, we hypothesize that the motivation for PVN oxytocin neurons to trigger dopamine release originates in the social behavior network, a highly conserved and interconnected collection of six regions implicated in various social and homeostatic behaviors. We found that expression of the neuronal activity marker EGR1 was not strongly correlated with song production in any of the regions of the social behavior network. However, when EGR1expression levels were normalized to the singing rate, we found significantly higher levels of expression in the social behavior network regions except the medial preoptic area during a social female-directed singing context compared to a non-social undirected singing context. Our results suggest neuronal activity within the male zebra finch social behavior network influences the synaptic release of oxytocin from PVN onto dopaminergic projection neurons in the VTA, which in turn signals to the vocal control network to allow for context-appropriate song production.