DYNAMICS OF REMAPPING ACROSS THE SPATIAL NAVIGATION CIRCUIT

Spatial navigation relies on the coordination between metric representations from grid cell modules, spatial anchoring by place and border cells, and directional reference frames encoded by head-direction cells. Together, these signals form a coherent map supporting navigation. During active, high-speed exploration of familiar environments, internal population manifolds and their anchoring to external space are tightly coupled. Sensory changes can trigger transitions between stored maps through remapping. While remapping has been described from a temporally averaged perspective, the rules governing fine-timescale dynamics of these transitions remain poorly understood.

Here, we investigate remapping dynamics across the spatial navigation system using simultaneous Neuropixels recordings from four chronic implant sites during exploration of open fields across five rooms. We decode spatial position, environment identity, and internal manifold stability across regions, allowing us to track at fine timescales how strongly representations are anchored to physical space and how internally stable they are. By comparing these measures across regions, we assess timing and coordination of remapping as animals re-enter familiar environments, under both partial and global reorganization.

We find that transitions into familiar environments can transiently appear as disruptions of spatial coding, but sometimes instead reflect persistence of a representation associated with a previously visited environment. In these cases, head-direction representations stabilize immediately upon entry, grid representations follow within seconds, and spatial representations in subiculum and hippocampal CA1 stabilize later. Together, these results point toward remapping as a coordinated process across regions and provide a population-level framework for understanding spatial map recall during naturalistic behavior.