HIPPOCAMPAL DYNAMICS SUPPORTING FEAR LEARNING BY OBSERVATION

Learning about danger, not from one's own direct experience, but by observing others', is a crucial adaptive strategy for avoiding life-threatening situations. Rodents acquire fear vicariously by witnessing conspecifics in distress. The hippocampus -organized into functionally distinct sub-domains along its septotemporal axis- and critical for memories of our own experiences, also contributes to 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.

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 -but not a control safe context- in which they witness a conspecific receive electrical footshocks. 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 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 obsrvation, we found a relative stabilization of the spatial representation associated with the shock context in the intermediate hippocampus.

Our results reveal mechanisms by which hippocampal neurons, particularly within the intermediate subregions, encode and consolidate vicarious fear memories.