An Independent Coding Scheme for Distance versus Position in the Hippocampus

Animals navigate using cognitive maps of their environment, integrating external landmarks and distances between them. Hippocampal place cells are the neuronal substrate of these cognitive maps. However, while hippocampal allocentric position coding in reference to external landmarks is well characterized, the determinants of idiothetic hippocampal distance coding remain poorly understood. Using virtual reality, electrophysiological recordings in mice, and local cue manipulations we could dissociate distance from position coding. In the cue-poor condition, we found pervasive distance coding with high distance indices in all bidirectional place cells including both superficial and deep CA1 pyramidal cells. In this condition, the mapping of distance onto a low-dimensional manifold and rigid distance relationships between place fields suggested strong attractor dynamics similar to those observed for grid cells. Inactivation of the medial septum (MS), which disrupts grid cells, significantly reduced both distance coding and rigid distance dynamics, suggesting an alteration (but not complete abolition) of the underlying attractor. In contrast, allocentric position coding could be observed in cue-rich environments, predominantly engaged deep CA1 pyramidal cells, and persisted during MS inactivation. These results are consistent with a selective contribution of grid cells and associated rigid attractor dynamics to hippocampal idiothetic distance coding but not allocentric position coding.