Neuronal sequences during theta rely on behavior-dependent spatial maps

Abstract

Navigation through space involves learning and representing relationships between past, current, and future locations. In mammals, this might rely on the hippocampal theta phase code, where in each cycle of the theta oscillation, spatial representations provided by neuronal sequences start behind the animal’s true location and then sweep forward. However, the exact relationship between theta phase, represented position and true location remains unclear and even paradoxical. Here, we formalize previous notions of ‘spatial’ or ‘temporal’ theta sweeps that have appeared in the literature. We analyze single-cell and population variables in unit recordings from rat CA1 place cells and compare them to model simulations based on each of these schemes. We show that neither spatial nor temporal sweeps quantitatively accounts for how all relevant variables change with running speed. To reconcile these schemes with our observations, we introduce ‘behavior-dependent’ sweeps, in which theta sweep length and place field properties, such as size and phase precession, vary across the environment depending on the running speed characteristic of each location. These behavior-dependent spatial maps provide a structured heterogeneity that is essential for understanding the hippocampal code.

Keywords

• hippocampus
• place cell
• theta oscillation
• phase precession
• theta sequence
• neural coding