Prefrontal Cortical Dynamics in Social Behavior and Dyadic Interaction
Human beings are fundamentally social animals – our daily interactions with others profoundly shape our experience, and in the best of circumstances, are among the most rewarding aspects of life. By the same token, negative social experience and prolonged social isolation can breed loneliness, anxiety, and depression. Our sociality is something that we share with most of the animal kingdom, and it is defined ultimately by our biology and our evolutionary history. Yet despite our deep and intuitive social impulses, our understanding of the biological processes in the brain that shape social perception, cognition, and behavior is still remarkably limited. One of the most important goals of modern neuroscience is to clarify the biological logic of our social experience, and in doing so, to develop a richer understanding of ourselves and our place in the world. The two studies presented in this dissertation are a step toward this goal. They aim to investigate how the brain transforms social information into behavioral decisions and how it coordinates the dynamic of social interaction when individuals engage with one another. Before describing the studies, I will first provide a discussion in chapter 1 of concepts in social neuroscience, giving a brief history of how the field has evolved out of the separate strands of ethology and cognitive neuroscience. Chapter 1 will also contain an overview of the basic neurophysiology of sensory perception and social behavior that will help to contextualize the questions addressed in the experiments and discussion of the results. In chapter 2, I will discuss methodological considerations in social neuroscience, including approaches to measure and manipulate brain activity as well as important statistical methods used to analyze relationships between social behavior and the underlying neural processes. In chapters 3 and 4, I will present two studies which each investigate the involvement of cortical dynamics in social functioning from a distinct perspective. In chapter 3, I will describe experiments performed in mice using microendoscopic calcium imaging that explore how one important social sensory feature – sex identity (male vs. female) – is encoded in the cortex of the brain. Linking measurements of neural encoding to behavior, we found that internal representations of sex identity are sexually dimorphic across male and female animals, and that in males, cortical representations of sex predict their preference toward opposite-sex interaction. Using activity-dependent optogenetic manipulations, we found that these cortical representations of sex identity bi-directionally modulate the behavioral preference of the animal toward male or female-directed interaction. This study is among the first to demonstrate a causal role for functionally defined neuronal populations in behavior, and the first to do so in a way that links native encoding of a social variable to control of social behavior. In chapter 4, I will describe experiments that investigate neural activity dynamics in the prefrontal cortex of mice while they engage in natural, dyadic interactions. This study focuses on analyzing the synchronization of neural activity across brains of interacting animals, which we identified as an emergent multi-animal neural correlate of social interaction. By analyzing the activity profiles of individual neurons in the brain, we traced the emergence of inter-brain synchronization from specific subsets of neurons that encode the behavior of each subject animal and its social partner. In aggregate, the responses of these neurons give rise to a regional activity signal that is synchronized across animals and predicts their future interaction and social relationships. This study is among the very first to examine multi-animal neural dynamics in animals, and it sets a foundation for deeper mechanistic investigation of neural processes that coordinate interaction across individuals.