The time course and organization of hippocampal replay

The mechanisms by which the brain replays neural activity sequences remain unknown. Recording from large ensembles of hippocampal place cells in freely behaving rats, we observed that replay content is strictly organized over multiple timescales and governed by self-avoidance. After movement cessation, replays avoided the animal’s previous path for 3 seconds. Chains of replays avoided self-repetition over a shorter timescale. We used a continuous attractor model of neural activity to demonstrate that neuronal fatigue both generates replay sequences and produces self-avoidance over the observed timescales. In addition, replay of past experience became predominant later into the stopping period, in a manner requiring cortical input. These results indicate a mechanism for replay generation that unexpectedly constrains which sequences can be produced across time.