Functional interactions of dopamine cell groups reflect personality, sex, and social context in highly social finches

Abstract

Dopamine (DA) is well known for its involvement in novelty-seeking, learning, and goal-oriented behaviors such as social behavior. However, little is known about how DA modulates social processes differentially in relation to sex and behavioral phenotype (e.g., personality). Importantly, the major DA cell groups (A8–A15) are conserved across all amniote vertebrates, and thus broadly relevant insights may be obtained through investigations of avian species such as zebra finches (Taeniopygia guttata), which express a human-like social organization based on biparental nuclear families that are embedded within larger social groups. We here build upon a previous study that quantified multidimensional personality structures in male and female zebra finches using principal components analysis (PCA) of extensive behavioral measures in social and nonsocial contexts. These complex dimensions of behavioral phenotype can be characterized as Social competence/dominance, Gregariousness, and Anxiety. Here we analyze Fos protein expression in DA neuronal populations in response to social novelty and demonstrate that the Fos content of multiple dopamine cell groups is significantly predicted by sex, personality, social context, and their interactions. In order to further investigate coordinated neuromodulation of behavior across multiple DA cell groups, we also conducted a PCA of neural variables (DA cell numbers and their phasic Fos responses) and show that behavioral PCs are associated with unique suites of neural PCs. These findings demonstrate that personality and sex are reflected in DA neuron activity and coordinated patterns of neuromodulation arising from multiple DA cell groups.