Environmental Geometry Aligns the Hippocampal Map during Spatial Reorientation

Abstract

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.

Keywords: cognitive map; disorientation; geometric module; hippocampus; navigation; place cells; spatial geometry; spatial reorientation.

Figure 1. Spatial geometry orients a reliable hippocampal map following disorientation in a rectangular chamber

A) Schematic of the rectangular chamber and the polarizing visual cue. Note that two rotations of this chamber, 0° an d 180°, result in geometrically equivalent shapes. B) Example rate maps from the first 8 trials for three place cells, two of which were simultaneously recorded (blue shading). Black line indicates the location of the visual cue. C) Quantification of best match rotations. To quantify the orientation of rate maps across trials for each place cell, the rotation that yielded the best match (highest correlation) between the two rate maps for each pair of trials was determined. D) Distribution of best match rotations across animals, computed as the percent of pairwise trial comparisons for which each rotation yielded the best match. The 0° and 180° rotations most ofte n and equally often yielded the best match, mirroring the rotational symmetry of the rectangular chamber. All error bars denote ±1 standard error of the mean (SEM) across animals. See also Figure S1. **p<0.01

Figure 2. Spatial geometry orients a reliable hippocampal map following disorientation in a square and isosceles triangular chamber

A) Schematic of the square chamber and the polarizing visual cue. Note that four rotations of the square chamber, 0°, 90°, 180°, and 270°, result in geometrically equivalent shapes. B) Example rate maps from the first 8 trials in the square chamber for three place cells, two of which were simultaneously recorded (blue shading). Black line indicates the location of the visual cue. C) Distribution of best match rotations across animals in the square chamber. This distribution did not differ from chance, mirroring the rotational symmetry of the square chamber. D) Schematic of the isosceles triangular chamber and the polarizing visual cue. Note that this chamber lacks rotational symmetry. E) Example rate maps from the first 8 trials in the triangular chamber for three place cells, two of which were simultaneously recorded (blue shading). Black line indicates the location of the visual cue. F) Distribution of best match rotations across animals in the triangular chamber. Only a rotation of 0° yielded the best match more often than chance, mirroring the lack of rotational symmetry of this chamber. All error bars denote ±1 SEM across animals. See also Figure S1. ***p<0.001

Figure 3. The orientation of the recovered hippocampal map predicts search behavior during a spatial reorientation task on a trial-by-trial basis

A) Schematic of the chamber with the rewarded (R) and geometric error (G) locations noted, and the corresponding distribution of first searches (mean ± (SEM)). B) Examples of place cell rate maps and search behavior from the first 8 trials during the spatial reorientation paradigm. C) Distribution of best match rotations across animals during the spatial reorientation paradigm. Rotations of 0° and 180° most often and equally often yielded the best match, mirroring the rotational symmetry of the chamber. D) Schematic of the behavior prediction analysis. To predict behavior on each trial, two average maps were created by combining either all other correct or all other geometric error search trials for each cell. Then, the population vector correlation between the to-be-predicted trial rate maps and each of the average behavior rate maps were calculated, and the behavior corresponding to the higher correlation was predicted. E) Individual and average prediction accuracy. F) Prediction accuracy using only data from cumulatively longer time intervals starting from the beginning of the to-be-predicted trial (top), and the cumulative distribution of the time of first search (bottom). G) Example average behavior rate maps, including all trials with the corresponding behavior. H) Cumulative distributions of correlations between the average correct map and the average geometric error map, either rotated 180° or unrotated, compared to a shuffled control. All error bars denote ±1 SEM across animals. See also Figure S2. **p<0.01; ***p<0.001