Spike-history gating of plateau potentials enables closed-loop rewriting of CA1 representations

Abstract

Behavioral time scale synaptic plasticity (BTSP) allows hippocampal CA1 neurons to form or shift place fields after a single plasticity-inducing plateau potential, but what determines when individual neurons become eligible for another plasticity event remains unclear. Here we propose that recent somatic spike history provides a cell-specific gate for plateau initiation, making neurons sensitive to rising activity after relative silence while suppressing repeated plasticity during sustained firing. In a two-compartment spiking model of CA1, this gate interacts with entorhinal input to create a feedback loop in which existing representations bias subsequent plateau locations. The resulting dynamics produce gradual place-field drift, reward-associated overrepresentation, recovery of environment-specific representations after remapping, and cross-day reinstatement. Our model further predicts that stronger residual activity biases subsequent plateaus toward previous field locations, a relationship we identify by reanalyzing experimental data. Thus, the expression of neural representations can help determine when and where they are subsequently rewritten.