Synaptic plasticity rules driving representational shifting in the hippocampus

Synaptic plasticity is widely thought to support memory storage in the brain, but the rules determining impactful synaptic changes in vivo are not known. We considered the trial-by-trial shifting dynamics of hippocampal place fields (PF) as an indicator of ongoing plasticity during memory formation and familiarization. By implementing different plasticity rules in computational models of spiking place cells and comparing them to experimentally measured PFs from mice navigating familiar and new environments, we found that behavioral timescale synaptic plasticity (BTSP), rather than Hebbian spike-timing-dependent plasticity (STDP), best explains PF shifting dynamics. BTSP-triggering events are rare, but more frequent during new experiences. During exploration, their probability is dynamic—it decays after PF onset, but continually drives a population-level representational drift. Additionally, our results show that BTSP occurs in CA3 but is less frequent and phenomenologically different than in CA1. Overall, our study provides a new framework to understand how synaptic plasticity continuously shapes neuronal representations during learning. Madar et al. report that behavioral timescale synaptic plasticity (BTSP), not spike-timing-dependent plasticity, explains heterogeneous place fields shifting in the hippocampus. The probability of BTSP induction follows patterned dynamics, is higher in new contexts and lower in CA3 than CA1.