Grid cell distortion is associated with increased distance estimation error in polarized environments

Grid cells within the medial entorhinal cortex (MEC) exhibit a regular hexagonal pattern of firing fields,¹ which has been hypothesized to provide a universal spatial metric, supporting spatial memory and navigation. This could be used to support a cognitive map, our internal representation of external space,²^,³^,⁴^,⁵^,⁶ and consistent with this, disruption of the MEC impairs spatial memory and place cell anchoring to external visual cues.⁷^,⁸^,⁹^,¹⁰ However, the highly regular and repetitive nature of the firing fields in grid cells is also ideally suited to support path integration.¹¹^,¹²^,¹³^,¹⁴^,¹⁵^,¹⁶^,¹⁷ Indeed, genetic silencing of stellate cells in MEC results in impaired distance estimation, supporting the MEC's role in path integration.¹⁸ However, few studies have examined the role of grid cell firing during active navigation. Several studies have reported that manipulation of environmental cues, recent experience, and reward location distort the grid signal,¹⁹^,²⁰^,²¹^,²²^,²³^,²⁴^,²⁵ but most relevant here is that the grid signal distorts in polarizing environments, such as trapezoids.²⁶^,²⁷ If grid cells support distance estimation and path integration, then disruption of the grid regularity, such as that seen in polarized environments, should impair these processes. Here, we report that both rats and humans have impaired distance estimation in polarized environments. Grid regularity was again reported to be distorted in polarized environments, and this was correlated with impaired distance estimation in rats. Grid regularity was also distorted by recent experience. These findings are consistent with grid cells supporting distance estimation in navigation.