Neural Markers of Responsiveness to the Environment in Human Sleep.

ABSTRACT

UNLABELLED Sleep is characterized by a loss of behavioral responsiveness. However, recent research has shown that the sleeping brain is not completely disconnected from its environment. How neural activity constrains the ability to process sensory information while asleep is yet unclear. Here, we instructed human volunteers to classify words with lateralized hand responses while falling asleep. Using an electroencephalographic (EEG) marker of motor preparation, we show how responsiveness is modulated across sleep. These modulations are tracked using classic event-related potential analyses complemented by Lempel-Ziv complexity (LZc), a measure shown to track arousal in sleep and anesthesia. Neural activity related to the semantic content of stimuli was conserved in light non-rapid eye movement (NREM) sleep. However, these processes were suppressed in deep NREM sleep and, importantly, also in REM sleep, despite the recovery of wake-like neural activity in the latter. In NREM sleep, sensory activations were counterbalanced by evoked down states, which, when present, blocked further processing of external information. In addition, responsiveness markers correlated positively with baseline complexity, which could be related to modulation in sleep depth. In REM sleep, however, this relationship was reversed. We therefore propose that, in REM sleep, endogenously generated processes compete with the processing of external input. Sleep can thus be seen as a self-regulated process in which external information can be processed in lighter stages but suppressed in deeper stages. Last, our results suggest drastically different gating mechanisms in NREM and REM sleep. SIGNIFICANCE STATEMENT Previous research has tempered the notion that sleepers are isolated from their environment. Here, we pushed this idea forward and examined, across all sleep stages, the brain's ability to flexibly process sensory information, up to the decision level. We extracted an EEG marker of motor preparation to determine the completion of the sensory processing chain and explored how it is constrained by baseline and evoked neural activity. In NREM sleep, slow waves elicited by stimuli appeared to block response preparation. We also used a novel analytic approach (Lempel-Ziv complexity) and showed that the ability to process external information correlates with neural complexity. A reversal of the correlation between complexity and motor indices in REM sleep suggests drastically different gating mechanisms across sleep stages.