Local Field Potentials Encode Place Cell Ensemble Activation during Hippocampal Sharp Wave Ripples

Abstract

Whether the activation of spiking cell ensembles can be encoded in the local field potential (LFP) remains unclear. We address this question by combining in vivo electrophysiological recordings in the rat hippocampus with realistic biophysical modeling, and explore the LFP of place cell sequence spiking ("replays") during sharp wave ripples. We show that multi-site perisomatic LFP amplitudes, in the ∼150-200 Hz frequency band, reliably reflect spatial constellations of spiking cells, embedded within non-spiking populations, and encode activation of local place cell ensembles during in vivo replays. We find spatiotemporal patterns in the LFP, which remain consistent between sequence replays, in conjunction with the ordered activation of place cell ensembles. Clustering such patterns provides an efficient segregation of replay events from non-replay-associated ripples. This work demonstrates how spatiotemporal ensemble spiking is encoded extracellularly, providing a window for efficient, LFP-based detection and monitoring of structured population activity in vivo.