Extracellular field signatures of CA1 spiking cell assemblies during sharp wave-ripple complexes

Abstract

Sharp wave-ripple complexes (SWRs) are primary population oscillatory events, observed in hippocampal local field potentials (LFPs), typically during deep sleep and awake immobility. They consist of an extensive depolarization in the CA1 dendritic layer (sharp wave) arising from population bursts in CA3, accompanied by a ~150-200 Hz LFP oscillation in the CA1 pyramidal layer (ripple). Temporal firing patterns of correlated place cells, acquired during wakeful exploration, are replayed in fast-scale during SWRs, which provides a strong indication for the participation of SWRs in memory consolidation. Yet the mechanisms that create these patterns and their particular effect on the LFP signal is largely unknown. How are the different ensembles of spiking cells encoded in the LFPs? We study this association through both a modeling and an experimental approach. Firstly, we employ a spiking network model of the CA3 and CA1 hippocampal areas that reproduces key features of SWRs based on synchronous CA3 population bursts and fast-decaying CA1 recurrent inhibition [1]. Secondly, the synaptic input on CA1 pyramidal cells is implemented in a spatially distributed population of morphologically realistic multi-compartmental models of CA1 pyramidal neurons, based on reconstructed cells [2]. The emerging extracellular fields accurately reproduce properties of SWR LFPs. By developing different subsets of CA1 cells that fire during ripples, we explore in a systematic fashion the influence of spiking cell assemblies on the emerging extracellular fields. In particular, we show how different spatiotemporal distributions of spiking cells give rise to differences in depth-profile and current source density (CSD) characteristics of raw and filtered fields. Finally, we apply our analysis to a set of LFPs and unit activity from multiple CA1 layers in the rat hippocampus, recorded in vivo [3]. We correlate the spiking activity of individual cells and cell assemblies, firing in sequence, with features of the depth profile and CSDs of LFPs within multiple CA1 layers. Based on our modeling results, we attempt to trace these features of the recorded LFPs back to the individual ensembles that gave rise to each ripple episode. This work offers a new approach to the decoding of ongoing cell assemblies based on extracellular current flows. Differences in the emerging SWR field activity may play an important role in information processing during memory consolidation.