Environmental Geometry Aligns the Hippocampal Map during Spatial Reorientation

When a navigator's internal sense of direction is disrupted, she must rely on external cues to regain her bearings, a process termed spatial reorientation. Extensive research has demonstrated that the geometric shape of the environment exerts powerful control over reorientation behavior, but the neural and cognitive mechanisms underlying this phenomenon are not well understood. Whereas some theories claim that geometry controls behavior through an allocentric mechanism potentially tied to the hippocampus, others postulate that disoriented navigators reach their goals by using an egocentric view-matching strategy. To resolve this debate, we characterized hippocampal representations during reorientation. We first recorded from CA1 cells as disoriented mice foraged in chambers of various shapes. We found that the alignment of the recovered hippocampal map was determined by the geometry of the chamber, but not by nongeometric cues, even when these cues could be used to disambiguate geometric ambiguities. We then recorded hippocampal activity as disoriented mice performed a classical goal-directed spatial memory task in a rectangular chamber. Again, we found that the recovered hippocampal map aligned solely to the chamber geometry. Critically, we also found a strong correspondence between the hippocampal map alignment and the animal's behavior, making it possible to predict the search location of the animal from neural responses on a trial-by-trial basis. Together, these results demonstrate that spatial reorientation involves the alignment of the hippocampal map to local geometry. We hypothesize that geometry may be an especially salient cue for reorientation because it is an inherently stable aspect of the environment.