Prefrontal cortical activity predicts the extra-place field spiking of hippocampal place cells

The receptive field of a neuron describes the regions of a stimulus space where the neuron is consistently active. Sparse spiking outside of the receptive field is often considered to be noise, rather than a reflection of information processing. Whether this characterization is accurate remains unclear. We therefore contrasted the sparse, temporally isolated spiking of hippocampal CA1 place cells to the consistent, temporally adjacent spiking seen within their spatial receptive fields (“place fields”). We found that isolated spikes, which occur during locomotion, are more strongly phase coupled to hippocampal theta oscillations than adjacent spikes and, surprisingly, transiently express coherent representations of non-local spatial representations. Further, prefrontal cortical activity is coordinated with, and can predict the occurrence of future isolated spiking events. Rather than local noise within the hippocampus, sparse, isolated place cell spiking reflects a coordinated cortical-hippocampal process consistent with the generation of non-local scenario representations during active navigation.