Decoding observational learning : a circuit level analysis of the social brain

Abstract

The ability to engage in appropriate social interaction is a critical component of daily life that requires integration of multiple neural processes and can be perturbed in numerous psychiatric diseases (Adolphs et al. 2003; Frith et al. 2008). One approach to begin understanding how the brain supports a complex array of social behaviors is to study innate, evolutionarily conserved social behaviors. Observational fear learning is one such social behavior that offers a distinct advantage for survival and is thus highly conserved across various species including rodents (Heyes et al. 1990; Kavaliers et al. 2001), monkeys (Mineka et al. 1984), and humans (Olsson et al. 2007). The data presented in this thesis combines in vivo electrophysiology, optogenetics, and rodent behavior in order to answer a number of questions about the role of the anterior cingulate cortex (ACC) and the basolateral amygdala (BLA) in observational fear learning. We show that both the ACC and the BLA contain neurons that show conditioned responses to the cue and are therefore neural correlates of observational fear learning. We photo-identify neurons within the ACC-BLA network and show that the ACC-BLA network has an enhanced representation of cue information when compared to out of network neurons. In addition, we show that ACC neurons that project to the BLA encode cue information. Next, we inhibit ACC input to the BLA during the cue and show that this impairs observational learning but not classical fear conditioning. Further, inhibition of ACC input to the BLA changes the cue response of a subset of BLA neurons. Lastly, we show that ACC input to the BLA is necessary for normal social interaction. Together, this data provides the first circuit level analysis of observational fear learning. It establishes that the transfer of cue information from the ACC to the BLA plays a causal role in enabling observational learning and that this same input is needed for general social behavior.