A large majority of awake hippocampal sharp-wave ripples feature spatial trajectories with momentum

Abstract

During periods of rest, hippocampal place cells feature bursts of activity called sharp-wave ripples (SWRs). Heuristic approaches have revealed that a small fraction of SWRs appear to "simulate" trajectories through the environment, called awake hippocampal replay. However, the functional role of a majority of these SWRs remains unclear. We find, using Bayesian model comparison of state-space models to characterize the spatiotemporal dynamics embedded in SWRs, that almost all SWRs of foraging rodents simulate such trajectories. Furthermore, these trajectories feature momentum, or inertia in their velocities, that mirrors the animals' natural movement, in contrast to replay events during sleep, which lack such momentum. Last, we show that past analyses of replayed trajectories for navigational planning were biased by the heuristic SWR sub-selection. Our findings thus identify the dominant function of awake SWRs as simulating trajectories with momentum and provide a principled foundation for future work on their computational function.