Differential Emergence and Stability of Sensory and Temporal Representations in Context-Specific Hippocampal Sequences

Hippocampal spiking sequences encode external stimuli and spatiotemporal intervals, linking sequential experiences in memory, but the dynamics controlling the emergence and stability of such diverse representations remain unclear. Using two-photon calcium imaging in CA1 while mice performed an olfactory working-memory task, we recorded stimulus-specific sequences of “odor-cells” encoding olfactory stimuli followed by “time-cells” encoding time points in the ensuing delay. Odor-cells were reliably activated and retained stable fields during changes in trial structure and across days. Time-cells exhibited sparse and dynamic fields that remapped in both cases. During task training, but not in untrained task exposure, time-cell ensembles increased in size, whereas odor-cell numbers remained stable. Over days, sequences drifted to new populations with cell activity progressively converging to a field and then diverging from it. Therefore, CA1 employs distinct regimes to encode external cues versus their variable temporal relationships, which may be necessary to construct maps of sequential experiences. [Display omitted] •Spiking sequences in CA1 encode odor-stimuli and delay time in a working memory task•Odor-fields are stable, whereas time-fields remap across days and trial alterations•Time-cell numbers increase during learning the task, not when passively exposed to it•Cell activity progressively converges to a field and then diverges from it over days Taxidis et al. demonstrate that odor-specific spiking sequences in the hippocampus combine robust and stable encoding of olfactory stimuli with highly dynamic temporal codes that increase during learning of a working memory task. This combination allows the linking of fixed external elements and their variable temporal relationships in memory space.