Single cell transcriptomic representation of social dominance in prefrontal cortex and the influence of preweaning maternal and postweaning social environment

Abstract

Social dominance encompasses winning dyadic contests and gaining priority access to resources and reproduction. Dominance is influenced by environmental factors, particularly during early postnatal life and adolescence. A disinhibitory medial prefrontal cortex (mPFC) microcircuit has been implicated in the expression of dominance in the “tube test” social competition paradigm in mice, but the neuroplasticity underlying dominance is not known. We previously reported that male pups raised by physically active (wheel-running, as opposed to sedentary) dams exhibit tube test dominance and increased reproductive fitness, and here we show that social isolation from weaning also increases dominance. By using single cell transcriptomics, we tested if increased dominance in these models is associated with a specific transcriptional profile in one or more cell-types in the mPFC. The preweaning maternal effect, but not postweaning social isolation, caused gene expression changes in pyramidal neurons. However, both the effect of maternal exercise and social isolation induced the coordinated downregulation of synaptic channel, receptor, and adhesion genes in parvalbumin positive (PV) interneurons, suggesting that development of dominance is accompanied by impaired PV interneuron-mediated inhibition of pyramidal cells. This study may help understand environmentally induced transcriptional plasticity in the PFC and its relationship to tube test dominance.