Signatures of rapid synaptic learning in the hippocampus during novel experiences

Abstract

Neurons in the hippocampus exhibit striking selectivity for specific combinations of sensory features, forming representations which are thought to subserve episodic memory. Even during a completely novel experience, ensembles of hippocampal "place cells" are rapidly configured such that the population sparsely encodes visited locations, stabilizing within minutes of the first exposure to a new environment. What cellular mechanisms enable this fast encoding of experience? Here we leverage virtual reality and large scale neural recordings to dissect the effects of novelty and experience on the dynamics of place field formation. We show that the place fields of many CA1 neurons transiently shift locations and modulate the amplitude of their activity immediately after place field formation, consistent with rapid plasticity mechanisms driven by plateau potentials and somatic burst spiking. These motifs were particularly enriched during initial exploration of a novel context and decayed with experience. Our data suggest that novelty modulates the effective learning rate in CA1, favoring burst-driven field formation to support fast synaptic updating during new experience.