The modulation of social decision-making function by dominance status in male mice

An animal’s dominance status strongly affects its behavioural decision making in social contexts. While the thalamocortical circuitry involved in the establishment of male mouse social status has received much attention in the literature, it remains unclear how these representations of rank modulate downstream areas to yield distinct behavioural phenotypes. Here we report in vivo miniscope recordings from the medial preoptic area (MPOA) and the ventromedial hypothalamus (VMH) - two areas involved in social decision-making that show differential c-Fos expression depending on social rank. Recordings were made during the tube test, an established assay of social dominance – and during chemoinvestigation of male and female conspecifics. A linear model could predict tube test behaviours such as pushing, resisting, and retreating with high accuracy from the activity of both areas, suggesting their involvement in competitive behaviour. We also found differences between dominant and subordinate mice in the tuning properties and behaviour evoked neural responses in these areas and correlated these differences with the behavioural traits of the animal. Additionally, the low-dimensional population dynamics compared across mice using canonical correlation analysis (CCA) were found to be more strongly correlated between mice of the same rank compared to mice of opposite ranks, which indicates neuromodulation of these areas by dominance status. Preliminary optogenetic stimulation of projections from the medial prefrontal cortex – an area previously shown to encode dominance – to the MPOA indicates enhanced competitive performance in the tube test. Together, these results characterise the modulation of social perception in the hypothalamus by dominance rank and how that can result in distinct behavioural phenotypes. They also propose a unifying circuit model that integrates these nodes into the existing thalamocortical circuit that encodes rank.