Schaffer commissural inputs regulate the stability of CA1 spatial representation

Neuronal representations of the world are dynamic. A striking example is the rapid remapping of the hippocampal spatial code, which occurs even when the environment and behavior remain unchanged. Here, we tested the possibility that CA3 Schaffer commissural inputs to CA1 control the stability of the cellular place representation in dorsal CA1. By combining longitudinal two-photon calcium imaging of CA1 place cells with optogenetic stimulation of contralateral presynaptic CA3 neurons in mice running on a linear treadmill, we demonstrate that CA3 inputs regulate the CA1 place code. Activation of CA3 cells both induced a small pool of new CA1 place cells and altered the pre-existing CA1 place code. The latter occurred through an unbiased shift of existing place fields specifically, and not through modifications of place field precision or a complete loss of place tuning in pre-existing place cells. All CA3-driven changes in the CA1 allocentric place code were transient and almost completely disappeared by the next day. Taken together, these results confirm a role for Schaffer commissural inputs in regulating CA1-encoded spatial representations, thus possibly contributing to the rapid scaffolding and remapping of spatial memories.