The Statistical Structure of the Hippocampal Code for Space as a Function of Time, Context, and Value

Hippocampal activity represents many behaviorally important variables, including context, an animal’s location within a given environmental context, time, and reward. Here we used longitudinal calcium imaging in mice, multiple large virtual environments, and differing reward contingencies to derive a unified probabilistic model of hippocampal CA1 representations centered on a single feature – the field propensity. Each cell’s propensity governs how many place fields it has per unit space, predicts its reward-related activity, and is preserved across distinct environments and over months. The propensity is broadly distributed—with many low, and some very high, propensity cells —and thus strongly shapes hippocampal representations. The result is a range of spatial codes, from sparse to dense. Propensity varied ~10-fold between adjacent cells in a salt-and-pepper fashion, indicating substantial functional differences within a presumed cell type. The stability of each cell’s propensity across conditions suggests this fundamental property has anatomical, transcriptional, and/or developmental origins.