The Precision of Place Fields Governs Their Fate across Epochs of Experience.

Abstract

Spatial memories are represented by hippocampal place cells during navigation. This spatial code is dynamic, undergoing changes across time, known as representational drift, and across changes in internal state, even while navigating the same spatial environment with consistent behavior. A dynamic code may provide the hippocampus a means to track distinct epochs of experience that occur at different times or during different internal states and update spatial memories. Changes to the spatial code include place fields (PFs) that remap to new locations and place fields that vanish, while others are stable. However, what determines place field fate across epochs 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 determined the position of the place fields in another block of trials in the same spatial environment either separated by a day (a distinct temporal epoch) or during the same session but with reward removed to change reward expectation (a distinct internal state epoch). We found that place cells with remapped place fields across epochs tended to have lower spatial precision during navigation in the initial epoch. Place cells with stable or vanished place fields tended to have 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 epochs of experience in the same spatial environment, while place cells with precise place fields generally preserve spatial information when their fields reappear.