Environmental Boundaries as an Error Correction Mechanism for Grid Cells

Abstract

Medial entorhinal grid cells fire in periodic, hexagonally patterned locations and are proposed to support path-integration-based navigation. The recursive nature of path integration results in accumulating error and, without a corrective mechanism, a breakdown in the calculation of location. The observed long-term stability of grid patterns necessitates that the system either performs highly precise internal path integration or implements an external landmark-based error correction mechanism. To distinguish these possibilities, we examined grid cells in behaving rodents as they made long trajectories across an open arena. We found that error accumulates relative to time and distance traveled since the animal last encountered a boundary. This error reflects coherent drift in the grid pattern. Further, interactions with boundaries yield direction-dependent error correction, suggesting that border cells serve as a neural substrate for error correction. These observations, combined with simulations of an attractor network grid cell model, demonstrate that landmarks are crucial to grid stability.

The Cognitive Architecture of Spatial Navigation: Hippocampal and Striatal Contributions

“…The predicted ''boundary vector cells'' mediating this information were subsequently found in subiculum (Barry et al, 2006;Lever et al, 2009) and mEC . Environmental boundaries also affect the firing pattern and orientation (Krupic et al, 2015;Stensola et al, 2015) of grid cells, consistent with a role in reducing cumulative error (Hardcastle et al, 2015). The complete system probably combines environmental and self-motion information to estimate location and orientation.…”

Spatial representation in the hippocampal formation: a history

“…The periodicity of the firing pattern and the variability of the grid scale suggested early on that place cells may emerge by a Fourier-like linear summation of output from grid cells with similar phase throughout the environment over a range of spatial scales 91,175 . This summation mechanism might be facilitated further by coordinated gamma-frequency oscillationsCO M M E N TA RY grid field locations in open spaces compared to locations near the walls 199 , as well as the instability of place fields in open spaces when spatially stable information is available only from border cells 195 , speak in favor of a reference function for environmental boundaries, where grid and place representations are reset and corrected from drift each time the animal encounters a salient boundary.…”

Principles governing the integration of landmark and self-motion cues in entorhinal cortical codes for navigation

“…While several works indicate that grid cell firing patterns rely on the integration of self-motion cues 2,9–11 , increasing evidence suggests that the grid pattern emerges from a complex interaction of self-motion and sensory landmark features. For example, grid cells deform in response to geometric changes in the environment, distort in polarized environments, depend on input regarding boundaries to maintain an error free map of space and, in mice, rapidly destabilize after the removal of visual landmarks 2,12–19 . Yet, many of these studies involved the complete removal of self-motion or landmark cues.…”