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

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.