Overlapping representations in the ventral hippocampus support rapid fear memory retrieval

The dorsal and ventral hippocampus (dCA1 and vCA1) are critical for contextual fear conditioning. The canonical theory states that the hippocampus generates dissimilar context representations to prevent interference and facilitate discrimination between contexts. Here, to test this, we monitored dCA1 and vCA1 context representations as mice were instantaneously transitioned between threatening and neutral contexts. Fear conditioning induced representational changes in both subregions, but the change was larger in vCA1 and scaled with freezing. During discrimination testing, threatening and neutral context representations were more similar in vCA1, whereas dCA1 representations remained distinct. During retrieval, vCA1 reinstated the threatening context representation faster and more strongly than dCA1, and the relative dominance of the two representations in vCA1 predicted freezing. These results reveal an unrecognized coding strategy in vCA1: fear learning increases representational overlap, consistent with a shallower attractor landscape, which may permit rapid transitions between neutral and threatening memories.