Leveraging place field repetition to understand positional versus nonpositional inputs to hippocampal field CA1

The hippocampus is believed to encode episodic memory by binding information about the content of experience within a spatiotemporal framework encoding the location and temporal context of that experience. Previous work implies a distinction between positional inputs to the hippocampus from upstream brain regions that provide information about an animal’s location and nonpositional inputs which provide information about the content of experience, both sensory and navigational. Here, we leverage the phenomenon of ‘place field repetition’ to better understand the functional dissociation between positional and nonpositional information encoded in CA1. Rats navigated freely on a novel maze consisting of linear segments arranged in a rectilinear, city-block configuration, which combined elements of open-field foraging and linear-track tasks. Unlike typical results in open-field foraging, place fields were directionally tuned on the maze, even though the animal’s behavior was not constrained to extended, one-dimensional (1D) trajectories. Repeating fields from the same cell tended to have the same directional preference when the fields were aligned along a linear corridor of the maze, but they showed uncorrelated directional preferences when they were unaligned across different corridors. Lastly, individual fields displayed complex time dynamics which resulted in the population activity changing gradually over the course of minutes. These temporal dynamics were evident across repeating fields of the same cell. These results demonstrate that the positional inputs that drive a cell to fire in similar locations across the maze can be behaviorally and temporally dissociated from the nonpositional inputs that alter the firing rates of the cell within its place fields, offering a potential mechanism to increase the flexibility of the system to encode episodic variables within a spatiotemporal framework provided by place cells.