Scream's roughness confers a privileged access to the brain during sleep

Abstract

During sleep, recognizing threatening signals is crucial to know when to wake up and when to continue vital sleep functions. Screaming is perhaps the most salient and efficient signal for communicating danger at a distance or in conditions of limited visibility. Beyond the intensity or the pitch of the sound, rapid modulations of sound pressure in the so-called roughness range (i.e. 30-150 Hz) are particularly powerful in capturing attention and accelerating reactions. Roughness is an acoustic feature that characterizes alarm signals such as screams. However, whether rough sounds are also processed in a privileged manner during sleep is unknown. We tested this hypothesis by stimulating sleeping human participants with low-intensity screams and neutral calls. We found that screams trigger more reliable and better time-locked responses in wakefulness and NREM sleep. In addition, screams boosted sleep spindles, suggesting elevated stimulus salience. The increase in sleep spindle power was linearly proportional to the roughness of vocalizations, but not to their pitch. These findings demonstrate that, even at low sound intensity, screams roughness conveys stimulus relevance and enhances processing in both the waking and sleeping states. Preserved differential neural responses based on stimulus salience may ensure adaptive reactions -and ultimately survival- in a state where the brain is mostly disconnected from external inputs.