Intracellular Determinants of Hippocampal CA1 Place and Silent Cell Activity in a Novel Environment

SummaryFor each environment a rodent has explored, its hippocampus contains a map consisting of a unique subset of neurons, called place cells, that have spatially tuned spiking there, with the remaining neurons being essentially silent. Using whole-cell recording in freely moving rats exploring a novel maze, we observed differences in intrinsic cellular properties and input-based subthreshold membrane potential levels underlying this division into place and silent cells. Compared to silent cells, place cells had lower spike thresholds and peaked versus flat subthreshold membrane potentials as a function of animal location. Both differences were evident from the beginning of exploration. Additionally, future place cells exhibited higher burst propensity before exploration. Thus, internal settings appear to predetermine which cells will represent the next novel environment encountered. Furthermore, place cells fired spatially tuned bursts with large, putatively calcium-mediated depolarizations that could trigger plasticity and stabilize the new map for long-term storage. Our results provide new insight into hippocampal memory formation.

► Inputs to place and silent cells as seen at soma differ from the start of exploration ► Intrinsic properties of place and silent cells differ from the start of exploration ► Large, putatively Ca2+-based depolarizations occur at the centers of place fields ► These features may underlie formation and long-term storage of hippocampal memories