Comparison of Sleep Spindles and Theta Oscillations in the Hippocampus

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 (Ͼ90 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.

Regulation of Hippocampal Firing by Network Oscillations during Sleep

“…These oscillations showed similar across-sleep patterns in both neocortex and hippocampus. Given the absence of direct thalamic projections, except through reuniens, hippocampal spindles and slow waves are in fact likely inherited from the entorhinal cortex [15, 19, 20]. Additionally, the state-dependent firing patterns we observed were consistent with those in the barrel cortex [8]; putative interneurons comprised roughly half of recorded neurons in ref [8], and were weighed more due to their higher firing rates.…”

“…SWRs and spindles are well suited for driving plasticity [1, 12-14] and were observable in the hippocampal LFP ( Figure 2A-B ; [15]), modulating neuronal spiking ( Figure S3A ). SWRs coincided with spindles ( Figure 2C ) and were phase-locked to the trough of the spindle oscillation ( Figure 2D ).…”

Neuronal Firing Rate Homeostasis Is Inhibited by Sleep and Promoted by Wake

“…1F, 3E) raises the question of whether average firing is modulated by behavioral state or environmental factors. The reported effects of sleeping and waking on neocortical firing properties in freely behaving animals have been inconsistent, with some studies finding little effect on average firing (Evarts et al, 1962; Aton et al, 2009; Grossmark et al, 2012; Hengen et al, 2013), and others reporting differences of 25% or more (Abasolo et al, 2015; Steriade et al, 2001; Sullivan et al, 2014); generally these studies either followed the same neurons across very few epochs of each state or followed different ensembles across many epochs. Here we were able to compare the firing properties of the same neurons across many iterations of sleep and wake.…”

Pharmaco-EEG Studies in Animals: A History-Based Introduction to Contemporary Translational Applications

“…It is obvious that drug effects on animal PGO waves will be difficult to translate, since - although PGO waves have also been described in man - such waves are best observed with intracranial electrodes, which are outside the scope of clinical p-EEG. Anatomical differences are the prime reason that drug effects on theta rhythms, which are characteristic for rodent waking and REM sleep, cannot be translated to effects on scalp REM sleep EEG in humans, since the theta of rodent REM sleep and waking is generated primarily by the hippocampus [55], which, due to the limited thickness of the cortex, is easily picked up by epidural or scalp EEG electrodes. Theta rhythms are also observed in human cortical EEG, albeit with a somewhat lower frequency (4-7 Hz instead of 6-10 Hz in rodents) and are of cortical origin [101].…”