The coding of safety-danger boundaries by the amygdala and hippocampus: an ecological risky foraging investigation in rats

Abstract

Contemporary fear research focuses heavily on learned/acquired fear, as opposed to innate/instinctive fear, through the use of the Pavlovian fear conditioning paradigm. However, fear conditioning studies have limited translational applicability because, by focusing on specific responses (such as freezing) in a small experimental chamber, they confine the natural behaviors of animals. In contrast, ethological approaches can provide a more comprehensive understanding of the brain’s fear system because they mimic the risky situations that animals face in the real world. This dissertation investigated how the basal nucleus of the amygdala (BA; implicated in fear processing) and the dorsal hippocampus (dHPC; implicated in spatial processing) interact during ‘approach food-avoid predator’ conflict situations in rats. The first study employed a simultaneous recording technique to reveal the characteristics of BA and dHPC cells during risky foraging behaviors. The results showed that the BA neurons encode the valence of events whereas the dHPC place cells build the spatial representation with a distance gradient of fear. The two regions together showed selective modulation of neural activity based upon spike synchrony during the interaction with a predatory threat; that is, dHPC cells that displayed synchronized firing with the BA cells displayed remapping of their place fields. The second study demonstrated that optogenetic stimulation of BA neurons was sufficient to produce defensive behaviors in the absence of explicit threats. The third study showed that optical stimulations of BA cells altered the stability of place cells in the dHPC. Based on these findings, I propose a neural model of fear signals from the BA influencing spatial coding in the dHPC, which serves to provide the safety-danger boundary information.