Broadband slow-wave modulation in posterior and anterior cortex tracks distinct states of propofol-induced unconsciousness

Abstract

A controversy 5 has developed in recent years over the role that frontal and posterior cortices play in mediating consciousness and unconsciousness. One hypothesis proposes that posterior sensory and association cortices are the principal mediators of consciousness, citing evidence that strong slow-wave activity over posterior cortex during sleep disrupts the contents of dreaming. A competing hypothesis proposes that frontal-posterior interactions are critical to ignite a conscious percept, since activation of frontal cortex appears necessary for perception and can reverse unconsciousness under anesthesia. In both cases, EEG slow-waves (< 1 Hz) are considered evidence that up- and down-states are disrupting cortical activity necessary for consciousness. Here, we used anesthesia to study the interaction between the slow-wave and higher frequency activity in humans. If slow-waves are derived from underlying up and down-states, then they should modulate activity across a broad range of frequencies. We found that this broadband slow-wave modulation does occur: broadband slow-wave modulation occurs over posterior cortex when subjects initially become unconscious, but later encompasses both frontal and posterior cortex when subjects are more deeply anesthetized and likely unarousable. Based on these results, we argue that unconsciousness under anesthesia comprises several shifts in brain state that disrupt the sensory contents of consciousness distinct from arousal and awareness of those contents.\n\nSignificance StatementThe roles of frontal and posterior cortices in mediating consciousness and unconsciousness are controversial. Disruption of posterior cortex during sleep appears to suppress the contents of dreaming, yet activation of frontal cortex appears necessary for perception and can reverse unconsciousness under anesthesia. We studied the time course of regional cortical disruption, as mediated by slow-wave modulation of broadband activity, during anesthesia-induced unconsciousness in humans. We found that broadband slow-wave modulation covered posterior cortex when subjects initially became unconscious, but later encompassed both frontal and posterior cortex when subjects were deeply anesthetized and likely unarousable. This suggests that unconsciousness under anesthesia comprises several shifts in brain state that disrupt the contents of consciousness distinct from arousal and awareness of those contents.