Schaffer commissural inputs regulate the stability of CA1 spatial representation

Abstract

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. CA3 input to CA1 has been shown to exert a key role in triggering synaptic plasticity in place-encoding CA1 cells -- a phenomenon which could provide the cellular foundations for the remapping of the hippocampal code for space. However, how CA3 input directly contributes to place field formation and remapping of the place code in CA1 remains incompletely understood. By combining longitudinal two-photon calcium imaging of CA1 place cells with optogenetic stimulation of presynaptic CA3 neurons in mice running on a linear treadmill, we demonstrate that CA3 transiently modulates the code for allocentric space in CA1. 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 loss of place tuning in pre-existing place cells. All CA3-driven changes in the CA1 place code were transient and almost completely disappeared by the next day. Taken together, stimulation of CA3 input to CA1 cells alters CA1-encoded spatial representations, leading to a transient decrease in place field precision rather than an overrepresentation of the stimulation zone. HIGHLIGHTSO_LIOptogenetic CA3 stimulation with two-photon CA1 imaging in behaving mice C_LIO_LIStimulation of CA3 input induces a small pool of new CA1 place cells C_LIO_LIPre-existing CA1 place fields shift without loss of tuning or precision C_LIO_LICA3-driven remapping is unbiased in space and largely disappears by next day C_LI