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

Abstract

Learning where danger lurks by observing others requires linking another individual's distress to one's own representation of space. How the hippocampus implements this mapping is unknown. We recorded Neuropixels activity across the dorsal, intermediate and ventral hippocampus of male rats during contextual fear learning by observation, subsequent rest and recall. Observers showed increased immobility in the context where they had witnessed a conspecific receive footshocks, with substantial inter-individual variability. Pyramidal neurons were recruited by shock observation, with enriched shock-excited cells in the intermediate hippocampus. In the dorsal and intermediate hippocampus, shock-observation responses scaled with baseline place-field firing, revealing a gain-like conjunctive code between observed distress and observer's position. Following learning, shock-context spatial representations were selectively stabilized in the intermediate hippocampus, and post-learning sharp-wave ripples preferentially reactivated shock-context ensembles, especially in animals expressing contextual freezing. These findings identify candidate hippocampal mechanisms by which socially acquired threat information are mapped onto the observer's spatial representation and consolidated into memory.