The Intermediate Hippocampus Integrates Shock-Observation and Spatial Information during Observational Fear Memory

In the wild, learning about danger, not from one's own direct experience, but by observing the experiences of others is a crucial adaptive strategy for avoiding life-threatening situations. A growing body of evidence demonstrates that rodents can acquire fear vicariously by witnessing conspecifics in distress. The hippocampus, organized in functionally distinct sub-domains along its septotemporal axis, and critical for the formation and consolidation of memories, has recently been shown to be necessary for contextual vicarious fear learning in rodents. However, the neuronal mechanisms by which hippocampal circuits map others' distress onto an observer's own spatial representations remain poorly understood. To address this question, we recorded single-unit activity from the dorsal, intermediate, and ventral hippocampus of observer rats engaged in a vicarious fear-learning task. In this paradigm, animals learn to fear a shock context in which they witness a conspecific receive electrical footshocks, but not a safe context in which the same conspecific was present in a neutral state. We show that: 1) neurons both from the dorsal and intermediate hippocampus conjunctively encode witnessing a shock delivered to a conspecific and the place where it was observed, although shock observation recruited a larger proportion of pyramidal neurons within the intermediate hippocampus, 2) during a subsequent rest, the patterns of spiking activity associated with the shock context were preferentially reactivated, particularly in the intermediate hippocampus and 3) while spatial representations corresponding to both the safe and shock context reorganized in nearly all subregion of the hippocampus following shock observation, we found a relative stabilization of the spatial representation associated with the shock context for pyramidal cells recorded from the intermediate hippocampus. Our results reveal multiple neuronal mechanisms by which hippocampal neurons, particularly within the intermediate subregions, encode and consolidate vicarious fear memories.