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Abstract:
During sleep, the human brain transitions to a 'sentinel processing mode', enabling the continued processing of environmental stimuli despite the absence of consciousness. Going beyond prior research, we employed advanced information-theoretic analyses, including mutual information (MI) and co-information (co-I), alongside event-related potential (ERP) and temporal generalization analyses (TGA), to characterize auditory prediction error processing across wakefulness and sleep. We hypothesized that a shared neural code would be present across sleep stages, with deeper sleep being associated with reduced information content and increased information redundancy. To investigate this, twenty-nine young healthy participants were exposed to an auditory 'local-global' oddball paradigm during wakefulness and continued during an 8-hour sleep opportunity monitored via polysomnography. We focused on 'local' mismatch responses to a deviating fifth tone following four standard tones. ERP analyses showed that prediction error processing continued throughout all sleep stages (N1-N3, REM). Mutual information analyses revealed a substantial reduction in the amount of encoded prediction error information during sleep, although ERP amplitudes increased with deeper NREM sleep. In addition, co-information analyses showed that neural dynamics became increasingly redundant with increasing sleep depth. Temporal generalisation analyses revealed a largely shared neural code between N2 and N3 sleep, although it differed between wakefulness and sleep. Here, we showed how the neural code of the 'sentinel processing mode' changes from wake to light to deep sleep and REM, characterised by more redundant and less rich neural information in the human cortex as consciousness wanes. This altered stimulus processing reveals how neural information changes with the changes of consciousness states as we traverse the night.
