The chained activation of neuronal assemblies is thought to support major cognitive processes, including memory. In the hippocampus, this is observed during population bursts often associated with sharp-wave ripples, in the form of an ordered reactivation of neurons. However, the organization and lifetime of these assemblies remain unknown. We used calcium imaging to map patterns of synchronous neuronal activation in the CA1 region of awake mice during runs on a treadmill. The patterns were composed of the recurring activation of anatomically intermingled, but functionally orthogonal, assemblies. These assemblies reactivated discrete temporal segments of neuronal sequences observed during runs and could be stable across consecutive days. A binding of these assemblies into longer chains revealed temporally ordered replay. These modules may represent the default building blocks for encoding or retrieving experience.

SummaryThe hippocampus is essential for spatiotemporal cognition. Sequences of neuronal activation provide a substrate for this fundamental function. At the behavioral timescale, these sequences have been shown to occur either in the presence of successive external landmarks or through internal mechanisms within an episodic memory task. In both cases, activity is externally constrained by the organization of the task and by the size of the environment explored. Therefore, it remains unknown whether hippocampal activity can self-organize into a default mode in the absence of any external memory demand or spatiotemporal boundary. Here we show that, in the presence of self-motion cues, a population code integrating distance naturally emerges in the hippocampus in the form of recurring sequences. These internal dynamics clamp spontaneous travel since run distance distributes into integer multiples of the span of these sequences. These sequences may thus guide navigation when external landmarks are reduced.