Theta and Gamma Coordination of Hippocampal Networks during Waking and Rapid Eye Movement Sleep

Abstract

Rapid eye movement (REM) sleep has been considered a paradoxical state because, despite the high behavioral threshold to arousing perturbations, gross physiological patterns in the forebrain resemble those of waking states. To understand how intrahippocampal networks interact during REM sleep, we used 96 site silicon probes to record from different hippocampal subregions and compared the patterns of activity during waking exploration and REM sleep. Dentate/CA3 theta and gamma synchrony was significantly higher during REM sleep compared with active waking. In contrast, gamma power in CA1 and CA3-CA1 gamma coherence showed significant decreases in REM sleep. Changes in unit firing rhythmicity and unit-field coherence specified the local generation of these patterns. Although these patterns of hippocampal network coordination characterized the more common tonic periods of REM sleep (ϳ95% of total REM), we also detected large phasic bursts of local field potential power in the dentate molecular layer that were accompanied by transient increases in the firing of dentate and CA1 neurons. In contrast to tonic REM periods, phasic REM epochs were characterized by higher theta and gamma synchrony among the dentate, CA3, and CA1 regions. These data suggest enhanced dentate processing, but limited CA3-CA1 coordination during tonic REM sleep. In contrast, phasic bursts of activity during REM sleep may provide windows of opportunity to synchronize the hippocampal trisynaptic loop and increase output to cortical targets. We hypothesize that tonic REM sleep may support off-line mnemonic processing, whereas phasic bursts of activity during REM may promote memory consolidation.

Global slowing of network oscillations in mouse neocortex by diazepam

“…For analyzing the sleep-wake cycle we therefore did not distinguish waking immobility as a separate state in the present study. REM sleep is heterogeneous and can be divided into tonic and phasic REM (Sakai et al, 1973), the latter characterized by brief periods of increased theta amplitude and frequency, ponto-geniculo-occipital spikes, muscle twitches, increased eye movements and vegetative arousal (Montgomery et al, 2008). Phasic REM was detected with a MATLAB program based on methods adapted from Mizuseki et al (2011) and covered less than 3% of total REM duration (for detailed analysis of phasic versus tonic REM, see Branka ck et al, 2012).…”

On the Universal Mechanism Underlying Conscious Systems and the Foundations for a Theory of Consciousness

“…This relation between long-range synchronization and consciousness has been multiply corroborated on the basis of different experimental paradigms (Crick & Koch, 1990;Desmedt & Tomberg, 1994 Moreover, it was found that gamma synchrony shows up not only during conscious awareness of an external stimulus, but also in altered states of consciousness, such as meditation (Lutz, Greischar, Rawlings, Ricard, & Davidson, 2004) and REM sleep (Llinás & Ribary, 1993;Montgomery, Sirota, & Buzsáki, 2008). From this neurophysiological perspective, it is the binding of distributed neurons into functionally coherent assemblies that accounts for the unified nature of conscious experience (Singer, 2015).…”

Increased mesiotemporal delta activity characterizes virtual navigation in humans

“…Recently there has been much progress in understanding the role of theta oscillations in organizing neuronal activity in animals (O' Keefe & Dostrovsky, 1971;O'Keefe & Recce, 1993;Nádasdy et al, 1999;Huerta & Lisman, 1993;Montgomery et al, 2008). This knowledge resulted in functional theories implicating theta in memory and other cognitive processes.…”