Prefrontal mechanisms of pro-sociality and group interactions in mice
Embargo Date
2024-02-03
OA Version
Citation
Abstract
Social interactions between individuals, particularly within groups, constitute a vital aspect of animal survival across nearly all species. In particular, higher level, evolutionarily preserved processes and behaviors such as pro-sociality (e.g., recognition of another’s emotional state) and group interactions (e.g., competitive foraging) have been widely studied in fields of ethology, psychology, and economics. While recent neuroethological studies have examined interactive behaviors at extremes of dyads in artificial environments or herds in nature, gaining a full understanding of the neuronal mechanisms underlying these behaviors requires new approaches that examine freely behaving individuals within groups. Additionally, while there is mounting evidence pointing to the role that the dorsomedial prefrontal cortex (dmPFC) and the dACC (dorsal anterior cingulate cortex) play as a hub of the ‘social brain,’ the single-neuronal processes driving pro-social behaviors and naturalistic group interactions remain unknown. In this dissertation, I begin by reviewing previous work that has guided the study of social interactive behaviors and their neuronal mechanisms in animal models. Next, I present our novel findings and advances that combine a host of cutting-edge techniques to explore fundamental gaps in our understanding of pro-sociality and group interactions in male mice. Specifically, we find that 1) rodent dmPFC neurons differentially represent other- and self-experiences and drive prosocial ‘helping’ behaviors, and 2) the dmPFC uniquely drives competitive effort based on information about others during group foraging. I also discuss the impact of these results that may be translated to the clinic, where deficits in these behaviors are a hallmark of psychosocial illnesses such as autism spectrum disorders (ASD). Using a mouse Shank3 haploinsufficient model of ASD, I show that 3) proper Shank3 expression is necessary for prosocial decision making and that adult restoration of Shank3 expression reverses neuronal social-encoding imbalances in the dmPFC. Last, I forecast the future of social neuroethology by discussing recent technological advancements that will allow us to reveal the neural and molecular mechanisms of complex social behaviors emerging from groups of animals. Together, findings from this dissertation add to our fundamental understanding of the complex role that the dmPFC plays in social cognition and interactive behaviors. Data from these studies also reveal a remarkably rich neuronal process in the mouse prefrontal cortex that drives prosocial and competitive decision making in groups. The novel assays that I developed in these experiments also provide a unique framework to develop new treatments for psychosocial disorders in future studies.