Environmental Geometry Aligns the Hippocampal Map during Spatial Reorientation

Abstract

Summary 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.

Hippocampal Place Fields Maintain a Coherent and Flexible Map across Long Timescales

“…While some comparisons produced results consistent with these predictions, in most cases we found that mice utilized a coherent map: a configuration of place fields that maintain the same angle and distance from one another. Consistent with recent studies [14,15], however, we found that coherent maps frequently rotated in a manner that does not utilize specific arena cues or larger room cues for orientation. Maps were flexible as mice frequently employed a coherent map between the two different arenas while simultaneously modulating activity in a subset of cells to discriminate between them.…”

“…As noted in the introduction, instability observed in previous studies during random foraging [18,19] could result from global remapping of place fields (Figure 2A, top). Alternatively, we hypothesized that the trial-by-trial rotations of place fields observed in a recent study [14] might persist over longer time scales (Figure 2A, bottom). In agreement with this study, we likewise found that place fields frequently rotated together coherently between sessions by maintaining the same distance and angle from each other (Figure 2C–D).…”

“…Alternatively, a recent study [14] demonstrated that disoriented mice frequently ignore purely visual cues and instead utilize geometry to concurrently reorient themselves and their place field maps. In support of this work, in many cases where two sessions shared a coherent spatial map, place fields rotated incongruously with arena cues (Figure 3A).…”

“…If mice utilize the geometry of the room to orient their spatial maps [14,15], is the stability of these maps worse in more rotationally uniform arenas? To investigate this, we divided the arena into 45 degree bins and examined the distribution of mean place field rotations between sessions (Figure 3E).…”

“…These studies have shown that, when disoriented, rodents utilize the geometry of an environment rather than single visual cues to reorient [11–13]. Recent studies extended this result by demonstrating that spatially tuned cells in the hippocampus and medial entorhinal cortex concurrently reorient their firing locations in accordance with the animal’s behavior during reorientation to environmental geometry [14,15] (see [16] for review). Thus, while in many cases global remapping underlies place field instability observed upon repeated exposures to an environment, in other cases this instability might result from the coherent re-alignment of the spatial map to a cue undetected by the experimenter.…”