Disruption of hierarchical predictive coding during sleep.
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.
Cognitive Neuroimaging Unit, Institut National de la Santé et de la Recherche Médicale, U992, F-91191 Gif/Yvette, France; NeuroSpin Center, Institute of BioImaging, Commissariat à l'Energie Atomique, F-91191 Gif/Yvette, France; strauss.mel@gmail.com stanislas.dehaene@cea.fr.
Melanie
M
Strauss
Cognitive Neuroimaging Unit, Institut National de la Santé et de la Recherche Médicale, U992, F-91191 Gif/Yvette, France; NeuroSpin Center, Institute of BioImaging, Commissariat à l'Energie Atomique, F-91191 Gif/Yvette, France; Institut du Cerveau et de la Moelle Épinière Research Center, Institut National de la Santé et de la Recherche Médicale, U975 Paris, France;
Jacobo D
JD
Sitt
Cognitive Neuroimaging Unit, Institut National de la Santé et de la Recherche Médicale, U992, F-91191 Gif/Yvette, France; NeuroSpin Center, Institute of BioImaging, Commissariat à l'Energie Atomique, F-91191 Gif/Yvette, France; Institut du Cerveau et de la Moelle Épinière Research Center, Institut National de la Santé et de la Recherche Médicale, U975 Paris, France;
Jean-Remi
JR
King
Centre du sommeil et de la vigilance, Hôpital de l'Hôtel Dieu, Assistance Publique - Hôpitaux de Paris, F-75004 Paris, France; Equipe Vigilance Fatigue Sommeil, Université Paris-Descartes, 75006 Paris, France;
Maxime
M
Elbaz
Cognitive Neuroimaging Unit, Institut National de la Santé et de la Recherche Médicale, U992, F-91191 Gif/Yvette, France; NeuroSpin Center, Institute of BioImaging, Commissariat à l'Energie Atomique, F-91191 Gif/Yvette, France;
Leila
L
Azizi
Cognitive Neuroimaging Unit, Institut National de la Santé et de la Recherche Médicale, U992, F-91191 Gif/Yvette, France; NeuroSpin Center, Institute of BioImaging, Commissariat à l'Energie Atomique, F-91191 Gif/Yvette, France;
Marco
M
Buiatti
Institut du Cerveau et de la Moelle Épinière Research Center, Institut National de la Santé et de la Recherche Médicale, U975 Paris, France;
Lionel
L
Naccache
Cognitive Neuroimaging Unit, Institut National de la Santé et de la Recherche Médicale, U992, F-91191 Gif/Yvette, France; NeuroSpin Center, Institute of BioImaging, Commissariat à l'Energie Atomique, F-91191 Gif/Yvette, France;
Virginie
V
van Wassenhove
Cognitive Neuroimaging Unit, Institut National de la Santé et de la Recherche Médicale, U992, F-91191 Gif/Yvette, France; NeuroSpin Center, Institute of BioImaging, Commissariat à l'Energie Atomique, F-91191 Gif/Yvette, France; Department of Life Sciences, Université Paris 11, 91400 Orsay, France; and Chair of Experimental Cognitive Psychology, Collège de France, F-75005 Paris, France strauss.mel@gmail.com stanislas.dehaene@cea.fr.
Stanislas
S
Dehaene
D000222:Adaptation, Physiological; D000293:Adolescent; D000328:Adult; D004569:Electroencephalography; D018913:Event-Related Potentials, P300 / Q000502:physiology*; D006801:Humans; D007091:Image Processing, Computer-Assisted; D015225:Magnetoencephalography; D012677:Sensation; D012890:Sleep / Q000502:physiology*; D013016:Sound; D014851:Wakefulness / Q000502:physiology; D055815:Young Adult
MMN; P300; magnetoencephalography; mismatch response; prediction