Consistency of Spatial Representations in Rat Entorhinal Cortex Predicts Performance in a Reorientation Task

Abstract

Goal-directed behavior can be affected by environmental geometry. A classic example is the rectangular arena reorientation task, where subjects commonly confuse opposite but geometrically identical corners [1]. Until recently, little was known about how environmental geometry shapes spatial representations in a neurobehavioral context [2] (although see [3]). In the present study, we asked: Under what circumstances does the internal cognitive map predict behavior? And when does it fail to do so? To this end, we developed a variant of the classical reorientation task that allows for investigation of temporal dynamics of reorientation. We recorded head-direction (HD) cells and grid cells in the medial entorhinal cortex (MEC) of rats before, during, and after performing the task. MEC cells showed a bimodal response of being either aligned or rotated, relative to the free-foraging open-field sessions. Alignment was remarkably stable between disorientations and indicative of corner choice as a function of current and past alignment of spatial representations. Accordingly, when the cells showed consistent and properly aligned readout across multiple trials, behavioral choices were better predicted by HD and grid cell readout, with a probability of more than 70%. This was not the case when the cells did not show a stable consistent readout. Our findings indicate that entorhinal spatial representations predict corner choice, contingent on the stability and reliability of their readout. This work sets the stage for further studies on the link between the reliability of the neuronal signal and behavior, with implications for many brain systems in many organisms.

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

“…However, we also occasionally observed global remapping between sessions (Figure 2J). Consistent with previous studies [14,15], coherent maps frequently ignored visual cues for alignment between sessions (Figure 3). Analyses done assuming adherence of spatial maps to arena cues revealed relatively low correlations (Figure S5B).…”

“…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.…”

“…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).…”

“…First, as mentioned above, rats do frequently use the same map of place fields between two arenas ([29] and early sessions in [28]), even when they are permanently connected [46,47]. Second, disoriented rats frequently utilize geometry to reorient [11–13] and sometimes exhibit coherent rotations in the firing fields of upstream grid and head-direction cells in medial entorhinal cortex [15] and place cells in the hippocampus [48]. Thus, rats can also form spatial maps not tied to specific arena features.…”

“…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.…”