Attenuated Fast Steady-State Visual Evoked Potentials During Human Sleep

Abstract

During sleep, external sensory events rarely elicit a behavioral response or affect perception. However, how sensory processing differs between wakefulness and sleep remains unclear. A major difficulty in this field stems from using brief auditory stimuli that often trigger nonspecific high-amplitude "K-complex" responses and complicate interpretation. To overcome this challenge, here we delivered periodic visual flicker stimulation across sleep and wakefulness while recording high-density electroencephalography (EEG) in humans. We found that onset responses can be separated from frequency-specific steady-state visual evoked potentials (SSVEPs) selectively observed over visual cortex. Sustained SSVEPs in response to fast (8/10 Hz) stimulation are substantially stronger in wakefulness than in both nonrapid eye movement (NREM) and REM sleep, whereas SSVEP responses to slow (3/5 Hz) stimulation are stronger in both NREM and REM sleep than in wakefulness. Despite wake-like spontaneous activity, responses in REM sleep were similar to those in NREM sleep and different than wakefulness, in accordance with perceptual disconnection during REM sleep. Finally, analysis of amplitude and phase in single trials revealed that stronger fast SSVEPs in wakefulness are driven by more consistent phase locking and increased induced power. These results suggest that the sleeping brain is unable to effectively synchronize large neuronal populations in response to rapid sensory stimulation.