Abstract
Several network patterns allow for information exchange between the neocortex and the entorhinal-hippocampal complex, including theta oscillations and sleep spindles. How neurons are organized in these respective patterns is not well understood. We examined the cellular-synaptic generation of sleep spindles and theta oscillations in the waking rat and during rapid eye movement (REM) sleep by simultaneously recording local field and spikes in the regions and layers of the hippocampus and entorhinal cortex (EC). We show the following: (1) current source density analysis reveals that similar anatomical substrates underlie spindles and theta in the hippocampus, although the hippocampal subregions are more synchronized during spindles than theta; (2) the spiking of putative principal cells and interneurons in the CA1, CA3, and dentate gyrus subregions of the hippocampus, as well as layers 2, 3, and 5 of medial EC, are significantly phase locked to spindles detected in CA1; (3) the relationship between local field potential (LFP) phase and unit spiking differs between spindles and theta; (4) individual hippocampal principal cells generally do not fire in a rhythmic manner during spindles; (5) power in gamma (30-90 Hz) and epsilon (>90 Hz) bands of hippocampal LFP is modulated by the phase of spindle oscillations; and (6) unit firing rates during spindles were not significantly affected by whether spindles occurred during non-REM or transitions between non-REM and REM sleep. Thus, despite the similar current generator inputs and macroscopic appearance of the LFP, the organization of neuronal firing patterns during spindles bears little resemblance to that of theta oscillations.