Complex patterns of dopamine-related gene expression in the ventral tegmental area of male zebra finches relate to dyadic interactions with long-term female partners.

Abstract

Dopaminergic projections from the ventral tegmental area (VTA) to multiple efferent targets are implicated in pair bonding, yet the role of the VTA in the maintenance of long-term pair bonds is not well characterized. Complex interactions between numerous neuromodulators modify activity in the VTA, suggesting that individual differences in patterns of gene expression in this region may explain individual differences in long-term social interactions in bonded pairs. To test this hypothesis we used RNA-seq to measure expression of over 8000 annotated genes in male zebra finches in established male-female pairs. Weighted gene co-expression network analysis identified a gene module that contained numerous dopamine-related genes with TH found to be the most connected gene of the module. Genes in this module related to male agonistic behaviors as well as bonding-related behaviors produced by female partners. Unsupervised learning approaches identified two groups of males that differed with respect to expression of numerous genes. Enrichment analyses showed that many dopamine-related genes and modulators differed between these groups, including dopamine receptors, synthetic and degradative enzymes, the avian dopamine transporter and several GABA- and glutamate-related genes. Many of the bonding-related behaviors closely associated with VTA gene expression in the two male groups were produced by the male's partner, rather than the male himself. Collectively, results highlight numerous candidate genes in the VTA that can be explored in future studies and raise the possibility that the molecular/genetic organization of the VTA may be strongly shaped by a social partner and/or the strength of the pair bond.