The Theta Paradox: 4-8 Hz EEG Oscillations Reflect Both Sleep Pressure and Cognitive Control

Abstract

Human electroencephalographic (EEG) oscillations characterize specific behavioral and vigilance states. The frequency of these oscillations is typically sufficient to distinguish a given state; however, theta oscillations (4–8 Hz) have instead been found in near-opposite conditions of drowsiness during sleep deprivation and alert cognitive control. While the latter has been extensively studied and is often referred to as “frontal midline theta,” (fmTheta) the former has been investigated far less but is considered a marker for sleep pressure during wake. In this study we investigated to what extent theta oscillations differed during cognitive tasks and sleep deprivation. We measured high-density EEG in 18 young healthy adults (nine female) performing six tasks under three levels of sleep deprivation. We found both cognitive load and sleep deprivation increased theta power in medial prefrontal cortical areas; however, sleep deprivation caused additional increases in theta in many other, predominantly frontal, areas. The sources of sleep deprivation theta (sdTheta) were task dependent, with a visual-spatial task and short-term memory (STM) task showing the most widespread effects. Notably, theta was highest in supplementary motor areas during passive music listening, and highest in the inferior temporal cortex (responsible for object recognition) during a spatial game. Furthermore, while changes in task performance were correlated with increases in theta during sleep deprivation, this relationship was not specific to the EEG of the same task and did not survive correction for multiple comparisons. Altogether, these results suggest that both during sleep deprivation and cognition theta oscillations may preferentially occur in cortical areas not involved in ongoing behavior. SIGNIFICANCE STATEMENT Electroencephalographic (EEG) research in sleep has often remained separate from research in cognition. This has led to two incompatible interpretations of the function of theta brain oscillations (4–8 Hz): that they reflect local sleep events during sleep deprivation, or that they reflect cognitive processing during tasks. With this study, we found no fundamental differences between theta oscillations during cognition and theta during sleep deprivation that would suggest different functions. Instead, our results indicate that in both cases, theta oscillations are generated by cortical areas not required for ongoing behavior. Therefore, at least in humans, theta may reflect either cortical disengagement or inhibition.

Theta and alpha EEG oscillations reflect sleep need — except during the wake maintenance zone

“…Data from the task blocks of this experiment have been previously published in Snipes et al (2022) where the overall study design, EEG preprocessing, and power analyses were established. Here, previously reported methods will only be briefly described.…”

“…Major artifacts were identified visually, and physiological artifacts (eye movements, heartbeat, muscle activity) were removed with independent component analysis (ICA). Details are provided in Snipes et al (2022).…”

“…Z-scored values were then averaged across all channels excluding the outer-edge electrodes (Figure 3), or into 3 regions of interest (ROIs): Front, Center, and Back, marked in Suppl. Figure 5-1 of Snipes et al (2022). When plotting spectrograms, a 1 Hz lowess filter was used to smooth the signal (Figure 4).…”

Characterizing endogenous delta oscillations in human MEG

“…For example, one study investigated local alpha oscillations in auditory areas in humans with depth electrodes implanted in temporal regions and reported two distinct oscillators in primary and secondary auditory areas (Billig et al, 2019; see also Haegens et al, 2014). Another study used high density EEG to show that the seemingly paradoxical observation of theta oscillations surfacing during both rest and cognitive effort reflects separable neural dynamics (Snipes et al, 2022). The sparseness and variability of oscillating populations and their differential contributions to the recorded signals likely exacerbate divergences between existing human M/EEG studies, and should thus be taken into account more thoroughly.…”

Extracting electromyographic signals from multi-channel local-field-potentials using independent component analysis without direct muscular recording

“…However, there is still a limitation of this approach in fine state discrimination of immobility states. Although theta is prominent during REM sleep, theta power during QAW can also increase with many factors including respiration [69], vestibular stimulation [70], sleepiness [71], fear [8,21,22], attention and other cognitive functions [72][73][74]. In addition, QAW theta becomes less prominent during waking immobility, eating, grooming, and defecation [72,75].…”