‘Fearful-Place’ Coding in the Amygdala-Hippocampal Network

Surviving in nature requires that animals be able to assess varying locations of danger in their environment. However, the neural integration of spatial-risk information remains unknown. We investigated simultaneous activities of fear-responsive basal amygdala (BA) and place-responsive dorsal hippocampus (dHPC) neurons as rats left the nest to search for food in an open space and encountered a looming robot ‘predator.’ In this ecological setting, the BA cell spiking increased to the predatory threat, the dHPC place field stability decreased but theta power increased as a function of escalating risk location, and the place cells synchronized with the predator-responsive BA cells remapped significantly more than those synchronized with predator-unresponsive BA cells. Moreover, optogenetic stimulation of BA neurons was sufficient to elicit escape behavior and disrupt place fields. These results suggest a functional interaction between the BA’s fear signal and the dHPC’s spatial coding, as animals traverse safe-danger boundaries of their environment.