Calcium transient prevalence across the dendritic arbor predicts place field properties

Establishing the hippocampal cellular ensemble that represents an animal’s environment involves the emergence and disappearance of place fields in specific CA1 pyramidal neurons(1–4), and the acquisition of different spatial firing properties across the active population(5). While such firing flexibility and diversity have been linked to spatial memory, attention and task performance(6,7), the cellular and network origin of these place cell features is unknown. Basic integrate-and-fire models of place firing propose that such features result solely from varying inputs to place cells(8,9), but recent studies(3,10) instead suggest that place cells themselves may play an active role through regenerative dendritic events. However, due to the difficulty of performing functional recordings from place cell dendrites, no direct evidence of regenerative dendritic events exists, leaving any possible connection to place coding unknown. Using multi-plane two-photon calcium imaging of CA1 place cell somata, axons, and dendrites in mice navigating a virtual environment, we show that regenerative dendritic events do exist in place cells of behaving mice and, surprisingly, their prevalence throughout the arbor is highly spatiotemporally variable. Further, we show that the prevalence of such events predicts the spatial precision and persistence or disappearance of place fields. This suggests that the dynamics of spiking throughout the dendritic arbor may play a key role in forming the hippocampal representation of space.