State transitions in the statistically stable place cell population are determined by rate of perceptual change

Abstract

The hippocampus plays a central role in mammalian navigation and memory, yet an implementational understanding of the rules that govern the granularity of location encoding and the spatial-statistics of the population as a whole are lacking. We analysed large numbers of CA1 place fields recorded while rats foraged in environments up to 8.75 m2. We found that place cell propensities to form fields were proportional to open-field area, gamma-distributed, and conserved across environments. The properties of place fields varied positionally with a denser distribution of smaller fields near boundaries. Remarkably, field size and density were in a dynamic equilibrium, such that population-level activity statistics remained constant. We showed that the rate of transition through the statistically stable place cell population matched the rate of change in the animals' visual scenes - demonstrating that the resolution of the spatial-memory system is bounded by perceptual information afforded by the environment.