The theta paradox: 4-8 Hz EEG oscillations reflect both local sleep and cognitive control

Abstract

Human brain activity generates electroencephalographic (EEG) oscillations that 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", the former has been investigated far less but is considered to be a marker for local sleep 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 performing 6 tasks under 3 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 were task-dependent, with a visual-spatial task and short-term memory 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 during a spatial game. This suggests that theta caused by sleep deprivation may preferentially occur in cortical areas not involved in ongoing behavior. While our results find differences in topography from frontal midline theta, they raise the possibility that a common mechanism may underly both theta oscillations during cognition and during sleep deprivation.