Power and coherence of cortical high‐frequency oscillations during wakefulness and sleep

Abstract

Recently, a novel type of fast cortical oscillatory activity that occurs between 110 and 160 Hz (high-frequency oscillations (HFO)) was described. HFO are modulated by the theta rhythm in hippocampus and neocortex during active wakefulness and REM sleep. As theta-HFO coupling increases during REM, a role for HFO in memory consolidation has been proposed. However, global properties such as the cortex-wide topographic distribution and the cortico-cortical coherence remain unknown. In this study, we recorded the electroencephalogram during sleep and wakefulness in the rat and analyzed the spatial extent of the HFO band power and coherence. We confirmed that the HFO amplitude is phase-locked to theta oscillations and is modified by behavioral states. During active wakefulness, HFO power was relatively higher in the neocortex and olfactory bulb compared to sleep. HFO power decreased during non-REM and had an intermediate level during REM sleep. Furthermore, coherence was larger during active wakefulness than non-REM, while REM showed a complex pattern in which coherence increased only in intra and decreased in inter-hemispheric combination of electrodes. This coherence pattern is different from gamma (30-100 Hz) coherence, which is reduced during REM sleep. This data show an important HFO cortico-cortical dialog during active wakefulness even when the level of theta comodulation is lower than in REM. In contrast, during REM, this dialog is highly modulated by theta and restricted to intra-hemispheric medial-posterior cortical regions. Further studies combining behavior, electrophysiology and new analytical tools are needed to plunge deeper into the functional significance of the HFO.

Communication through coherence by means of cross-frequency coupling

“…For simplicity, we focused on local field potential (LFP) recordings from three neocortical locations: the right V2 and the left and right S1 areas ( Figure 1A). Standard spectral analyses (power, inter-regional synchrony, and phase-amplitude coupling) showed that these areas exhibit activity at theta and fast-gamma frequencies during REM sleep ( Figure S1), as previously reported (Cavelli et al, 2018;Scheffer-Teixeira and Tort, 2017;Scheffzük et al, 2011). Figure 1 outlines the new analysis framework, which is as follows: first, the LFPs from two distant brain regions are filtered to extract the high-frequency components (in the depicted example, we obtained the fast gamma activity from the left and right S1; Figure 1B).…”

“…(C) Average phase-amplitude comodulograms for REM sleep epochs (computed as described in Tort et al, 2010). Note the theta modulation of fast-gamma amplitude in all analyzed neocortical regions, as previously reported (Cavelli et al, 2018;Scheffer-Teixeira and Tort, 2017;Scheffzük et al, 2011). Figure S2.…”

Nasal respiration entrains neocortical long‐range gamma coherence during wakefulness

“…Furthermore, slow waves coupled to saccadic movement are capable of modulating inter‐cortical spikes and LFP γ coherence in visual areas (Lowet et al., , ). Recently, we showed that during REM sleep hippocampal theta activity modulates the coherence of intrahemispheric high‐frequency oscillations (110–160 Hz) in medial and posterior cortices of the rat (Cavelli et al., ). In addition, the present work demonstrates that long‐range γ coherence occurs modulated by the respiratory phase, suggesting a related phenomenon.…”

“…γ Coherence has been considered a neural correlate of conscious perception (Joliot, Ribary, & Llinás, 1994;Melloni et al, 2007;Rodriguez et al, 1999;Varela et al, 2001); it decreases during sleep (Castro-Zaballa et al, 2013Cavelli et al, 2015Cavelli et al, , 2017 and is absent during narcosis (unconsciousness) induced by general anesthetics (John, 2002;Mashour, 2006;Pal, Silverstein, Lee, & Mashour, 2016). Recently, it was shown that slow oscillations such as theta rhythm of the hippocampal networks (Cavelli et al, 2018;Scheffzük et al, 2011;Tort, Scheffer-Teixeira, Souza, Draguhn, & Brankačk, 2013;Tort et al, 2008;Zhong et al, 2017), cortical potentials caused by the rhythmic movement of the eyes (Ito, Maldonado, & Grün, 2013;Lowet et al, 2018) and respiration (Ito et al, 2014;Tort, Brankačk, & Draguhn, 2018a;Zhong et al, 2017) modulate γ activity.…”

Decreased electrocortical temporal complexity distinguishes sleep from wakefulness

“…Due to the complex nature of the standard EEG and ECoG signals, traditional methods employed in neuroscience have divided the complex spectrum of the signal into frequency bands, 3, 5-9 and analyzed its changes during different cognitive functions, 4,7 and sleep states. 5,6,8 These methods only describe particular characteristics of the recorded signals and do not account for the complex nature of the cortical electric potentials. In contrast, the field of non-linear dynamics has developed measures and models that account for the complexity of the systems and their emerging interactions.…”