Diversity in neural firing dynamics supports both rigid and learned hippocampal sequences

Coding what is known and what is new Do neural activity patterns during sleep reflect the replay of a novel experience or an invariant preexisting dynamic? Grosmark and Buzsáki observed that both familiar and novel aspects of learned information are replayed during synchronous bursts of activity in the hippocampus. Familiarity was encoded by fast-firing less-modifiable neurons that showed rate and sequence correlations that persisted into postlearning sleep. The novel features of an experience were represented by a different set of slowly firing and highly plastic cells. Science, this issue p. 1440 Sleep replay combines preexisting firing patterns of fast-firing neurons and a small fraction of responsive, slow-firing neurons. Cell assembly sequences during learning are “replayed” during hippocampal ripples and contribute to the consolidation of episodic memories. However, neuronal sequences may also reflect preexisting dynamics. We report that sequences of place-cell firing in a novel environment are formed from a combination of the contributions of a rigid, predominantly fast-firing subset of pyramidal neurons with low spatial specificity and limited change across sleep-experience-sleep and a slow-firing plastic subset. Slow-firing cells, rather than fast-firing cells, gained high place specificity during exploration, elevated their association with ripples, and showed increased bursting and temporal coactivation during postexperience sleep. Thus, slow- and fast-firing neurons, although forming a continuous distribution, have different coding and plastic properties.