Causal Influence of Visual Cues on Hippocampal Directional Selectivity

Abstract

Hippocampal neurons show selectivity with respect to visual cues in primates, including humans, but this has never been found in rodents. To address this long-standing discrepancy, we measured hippocampal activity from rodents during real-world random foraging. Surprisingly, ∼ 25% of neurons exhibited significant directional modulation with respect to visual cues. To dissociate the contributions of visual and vestibular cues, we made similar measurements in virtual reality, in which only visual cues were informative. Here, we found significant directional modulation despite the severe loss of vestibular information, challenging prevailing theories of directionality. Changes in the amount of angular information in visual cues induced corresponding changes in head-directional modulation at the neuronal and population levels. Thus, visual cues are sufficient for-and play a predictable, causal role in-generating directionally selective hippocampal responses. These results dissociate hippocampal directional and spatial selectivity and bridge the gap between primate and rodent studies.