Diminished Auditory Responses during NREM Sleep Correlate with the Hierarchy of Language Processing.
Natural sleep provides a powerful model system for studying the neuronal correlates of awareness and state changes in the human brain. To quantitatively map the nature of sleep-induced modulations in sensory responses we presented participants with auditory stimuli possessing different levels of linguistic complexity. Ten participants were scanned using functional magnetic resonance imaging (fMRI) during the waking state and after falling asleep. Sleep staging was based on heart rate measures validated independently on 20 participants using concurrent EEG and heart rate measurements and the results were confirmed using permutation analysis. Participants were exposed to three types of auditory stimuli: scrambled sounds, meaningless word sentences and comprehensible sentences. During non-rapid eye movement (NREM) sleep, we found diminishing brain activation along the hierarchy of language processing, more pronounced in higher processing regions. Specifically, the auditory thalamus showed similar activation levels during sleep and waking states, primary auditory cortex remained activated but showed a significant reduction in auditory responses during sleep, and the high order language-related representation in inferior frontal gyrus (IFG) cortex showed a complete abolishment of responses during NREM sleep. In addition to an overall activation decrease in language processing regions in superior temporal gyrus and IFG, those areas manifested a loss of semantic selectivity during NREM sleep. Our results suggest that the decreased awareness to linguistic auditory stimuli during NREM sleep is linked to diminished activity in high order processing stations.
Department of Neurobiology, Weizmann Institute of Science, Rehreovot 76100, Israel.
Meytal
http://orcid.org/0000-0002-4037-8505
M
Wilf
Department of Neurobiology, Weizmann Institute of Science, Rehreovot 76100, Israel.
Michal
M
Ramot
Department of Biological Services, Weizmann Institute of Science, Rehovot 76100, Israel.
Edna
E
Furman-Haran
Department of Neurobiology, Weizmann Institute of Science, Rehreovot 76100, Israel.
Anat
A
Arzi
Shalvata Mental Health Care Center, School of Medicine, Tel Aviv University, Tel Aviv, Israel.
Yechiel
Y
Levkovitz
Department of Neurobiology, Weizmann Institute of Science, Rehreovot 76100, Israel.
Rafael
R
Malach
D000161:Acoustic Stimulation; D000328:Adult; D001303:Auditory Cortex / Q000000981:diagnostic imaging* / Q000502:physiology; D001931:Brain Mapping; D004569:Electroencephalography; D005260:Female; D006339:Heart Rate; D006801:Humans; D007802:Language; D008279:Magnetic Resonance Imaging; D009474:Neurons / Q000502:physiology; D012890:Sleep / Q000502:physiology*; D012894:Sleep Stages / Q000502:physiology; D013788:Thalamus / Q000000981:diagnostic imaging* / Q000503:physiopathology