Behavioral and brain responses to verbal stimuli reveal transient periods of cognitive integration of the external world during sleep

Abstract

Sleep has long been considered as a state of behavioral disconnection from the environment, without reactivity to external stimuli. Here we questioned this 'sleep disconnection' dogma by directly investigating behavioral responsiveness in 49 napping participants (27 with narcolepsy and 22 healthy volunteers) engaged in a lexical decision task. Participants were instructed to frown or smile depending on the stimulus type. We found accurate behavioral responses, visible via contractions of the corrugator or zygomatic muscles, in most sleep stages in both groups (except slow-wave sleep in healthy volunteers). Across sleep stages, responses occurred more frequently when stimuli were presented during high cognitive states than during low cognitive states, as indexed by prestimulus electroencephalography. Our findings suggest that transient windows of reactivity to external stimuli exist during bona fide sleep, even in healthy individuals. Such windows of reactivity could pave the way for real-time communication with sleepers to probe sleep-related mental and cognitive processes.