Place field precision during an episode predicts place field fate across episodes

Spatial memories are represented by hippocampal place cells during navigation. This spatial code is dynamic, undergoing changes across time – known as drift – and across changes in internal state, even while navigating the same spatial environment with consistent behavior. A dynamic spatial code may be a way for the hippocampus to track distinct episodes that occur at different times or during different internal states and update spatial memories. Changes to the spatial code include place fields that remap to new locations and place fields that vanish, while others are stable. However, what determines place field fate across episodes remains unclear. We measured the lap-by-lap properties of place cells in mice during navigation for a block of trials in a rewarded virtual environment. We then had mice navigate the same spatial environment for another block of trials either separated by a day (a distinct temporal episode) or during the same session but with reward removed to change reward expectation (a distinct internal state episode). We found that, as a population, place cells with remapped place fields across episodes had lower spatial precision during navigation in the initial episode. Place cells with stable or vanished place fields generally had higher spatial precision. We conclude that place cells with less precise place fields have greater spatial flexibility, allowing them to respond to, and track, distinct episodes in the same spatial environment, while place cells with precise place fields generally preserve spatial information when their fields reappear.