Disruption of hierarchical predictive coding during sleep

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 112; no. 11; pp. E1353 - E1362
• Main Authors: Strauss, Melanie, Sitt, Jacobo D., King, Jean-Remi, Elbaz, Maxime, Azizi, Leila, Buiatti, Marco, Naccache, Lionel, van Wassenhove, Virginie, Dehaene, Stanislas
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 17.03.2015; National Acad Sciences
• Series: PNAS Plus
• Subjects: Adaptation, Physiological; Adolescent; Adult; Biological Sciences; Brain; Brain research; Correlation analysis; Ears & hearing; Electroencephalography; Event-Related Potentials, P300 - physiology; eyes; Humans; Image Processing, Computer-Assisted; Listening; Magnetoencephalography; PNAS Plus; prediction; Sensation; Sleep; Sleep - physiology; Social Sciences; Sound; Wakefulness - physiology; Young Adult; prediction; mismatch response; magnetoencephalography; P300; MMN
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.1501026112

Significance Sleeping disrupts the conscious awareness of external sounds. We investigated the stage of processing at which this disruption occurs. In the awake brain, when a regular sequence of sounds is presented, a hierarchy of brain areas uses the available regularities to predict forthcoming sounds and to respond with a series of “prediction error” signals when these predictions are violated. Using simultaneous recordings of electroencephalography and magnetoencephalography signals, we discovered that both short-term and long-term brain responses to auditory prediction errors are disrupted during non-rapid eye movement and rapid eye movement sleep; however, the brain still exhibits detectable auditory responses and a capacity to habituate to frequently repeated sounds. Thus, sleep appears to selectively affect the brain’s prediction and error detection systems. When presented with an auditory sequence, the brain acts as a predictive-coding device that extracts regularities in the transition probabilities between sounds and detects unexpected deviations from these regularities. Does such prediction require conscious vigilance, or does it continue to unfold automatically in the sleeping brain? The mismatch negativity and P300 components of the auditory event-related potential, reflecting two steps of auditory novelty detection, have been inconsistently observed in the various sleep stages. To clarify whether these steps remain during sleep, we recorded simultaneous electroencephalographic and magnetoencephalographic signals during wakefulness and during sleep in normal subjects listening to a hierarchical auditory paradigm including short-term (local) and long-term (global) regularities. The global response, reflected in the P300, vanished during sleep, in line with the hypothesis that it is a correlate of high-level conscious error detection. The local mismatch response remained across all sleep stages (N1, N2, and REM sleep), but with an incomplete structure; compared with wakefulness, a specific peak reflecting prediction error vanished during sleep. Those results indicate that sleep leaves initial auditory processing and passive sensory response adaptation intact, but specifically disrupts both short-term and long-term auditory predictive coding.