Disrupted neural tracking of sound localization during non-rapid eye movement sleep
Yan Wang,
Lingxi Lu,
Guangyuan Zou,
Li Zheng,
Lang Qin,
Qihong Zou,
Jia-Hong Gao
Affiliations
Yan Wang
Center for MRI Research, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China; Chinese Institute for Brain Research, Beijing 102206, China; PKU-IDG/McGovern Institute for Brain Research, Peking University, Beijing 100871, China
Lingxi Lu
Center for the Cognitive Science of Language, Beijing Language and Culture University, Beijing 100083, China; Corresponding author at: Center for the Cognitive Science of Language, Beijing Language and Culture University
Guangyuan Zou
Center for MRI Research, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China
Li Zheng
Center for MRI Research, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China
Lang Qin
Center for MRI Research, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China
Qihong Zou
Center for MRI Research, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China; Corresponding author at: Center for the Cognitive Science of Language, Beijing Language and Culture University
Jia-Hong Gao
Center for MRI Research, Academy for Advanced Interdisciplinary Studies, Peking University, Beijing 100871, China; PKU-IDG/McGovern Institute for Brain Research, Peking University, Beijing 100871, China; Beijing City Key Lab for Medical Physics and Engineering, Institution of Heavy Ion Physics, School of Physics, Peking University, Beijing 100871, China; National Biomedical Imaging Center, Peking University, Beijing 100871, China; Corresponding authors at: Center for MRI Research, Academy for Advanced Interdisciplinary Studies, Peking University.
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.
