Emergence of stable sensory and dynamic temporal representations in the hippocampus during working memory

Hippocampal networks form maps of experience through spiking sequences that encode sensory cues, space or time. But whether distinct rules govern the emergence, stability and plasticity of externally driven and internally-generated representations remains unclear. Using two-photon calcium imaging, we recorded CA1 pyramidal populations across multiple days, while mice learned and performed an olfactory, delayed, working-memory task. We observed anatomically intermixed spiking sequences, comprised of odor-cells encoding olfactory cues, followed by time-cells encoding odor-specific delay time-points. Odor-cells were reliably activated across trials and retained stable fields over days and different delays. In contrast, time-cells exhibited sparse, unreliable activation and labile fields that remapped over days and extended delays. Moreover, the number of odor-cells remained stable, whereas time-cells increased over days during learning of the task, but not during passive exposure. Therefore, multi-modal representations with distinct learning-related dynamics and stability can co-exist in CA1, likely driven by different neurophysiological and plasticity mechanisms.