Disrupted neural tracking of sound localization during non-rapid eye movement sleep

Spatial hearing in humans is a high-level auditory process that is crucial to rapid sound localization in the environment. Both neurophysiological models with animals and neuroimaging evidence from human subjects in the wakefulness stage suggest that the localization of auditory objects is mainly located in the posterior auditory cortex. However, whether this cognitive process is preserved during sleep remains unclear. To fill this research gap, we investigated the sleeping brain's capacity to identify sound locations by recording simultaneous electroencephalographic (EEG) and magnetoencephalographic (MEG) signals during wakefulness and non-rapid eye movement (NREM) sleep in human subjects. Using the frequency-tagging paradigm, the subjects were presented with a basic syllable sequence at 5 Hz and a location change that occurred every three syllables, resulting in a sound localization shift at 1.67 Hz. The EEG and MEG signals were used for sleep scoring and neural tracking analyses, respectively. Neural tracking responses at 5 Hz reflecting basic auditory processing were observed during both wakefulness and NREM sleep, although the responses during sleep were weaker than those during wakefulness. Cortical responses at 1.67 Hz, which correspond to the sound location change, were observed during wakefulness regardless of attention to the stimuli but vanished during NREM sleep. These results for the first time indicate that sleep preserves basic auditory processing but disrupts the higher-order brain function of sound localization.