Hippocampal Place Fields Maintain a Coherent and Flexible Map Across Long Time Scales

To provide a substrate for remembering where in space events have occurred, place cells must reliably encode the same positions across long time scales. However, in many cases place cells exhibit instability by randomly reorganizing their place fields between experiences, challenging this premise. Recent evidence suggests that, in some cases, instability could also arise from coherent rotations of place fields, as well as from random reorganization. To investigate this possibility, we performed in vivo calcium imaging in dorsal hippocampal region CA1 of freely moving mice while they explored two arenas with different geometry and visual cues across eight days. The two arenas were rotated randomly between sessions, and then connected, allowing us to probe how cue rotations, the integration of new information about the environment, and the passage of time concurrently influenced the spatial coherence of place fields. We found that spatially coherent rotations of place field maps in the same arena predominated, persisting up to six days later, and that they frequently rotated in a manner that did not match that of the arena rotation. Furthermore, place field maps were flexible, as mice frequently employed a similar, coherent configuration of place fields to represent each arena despite their differing geometry and eventual connection. These results highlight the ability of the hippocampus to retain consistent relationships between cells across long time scales and suggest that, in many cases, apparent instability might result from a coherent rotation of place fields. Kinsky et al. demonstrate that hippocampal place fields in mice maintain a stable configuration across long time scales under low attentional demand. Coherent rotations of place fields frequently occurred between sessions, indicating that in some cases instability commonly attributed to global remapping might actually be a map rotation.