Delayed, Reduced and Redundant: Information Processing of Prediction Errors during Sleep

Abstract

During sleep, the human brain transitions to a sentinel processing mode, enabling the continued processing of environmental stimuli despite the absence of consciousness. Here, 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 during an 8-hour sleep opportunity monitored via polysomnography in a cross-sectional study. 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 particularly during N3 and REM, although ERP amplitudes increased with deeper NREM sleep. In addition, we observed delayed information encoding during sleep and 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 delayed processing, 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.