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Sleepers track informative speech in a multitalker environment

Nature Human Behaviour volume 3, pages 274–283 (2019)Cite this article

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Abstract

Sleep is a vital need, forcing us to spend a large portion of our life unable to interact with the external world. Current models interpret such extreme vulnerability as the price to pay for optimal learning. Sleep would limit external interferences on memory consolidation1,2,3 and allow neural systems to reset through synaptic downscaling4. Yet, the sleeping brain continues generating neural responses to external events5,6, revealing the preservation of cognitive processes ranging from the recognition of familiar stimuli to the formation of new memory representations7,8,9,10,11,12,13,14,15. Why would sleepers continue processing external events and yet remain unresponsive? Here we hypothesized that sleepers enter a ‘standby mode’ in which they continue tracking relevant signals, finely balancing the need to stay inward for memory consolidation with the ability to rapidly awake when necessary. Using electroencephalography to reconstruct competing streams in a multitalker environment16, we demonstrate that the sleeping brain amplifies meaningful speech compared to irrelevant signals. However, the amplification of relevant stimuli was transient and vanished during deep sleep. The effect of sleep depth could be traced back to specific oscillations, with K-complexes promoting relevant information in light sleep, whereas slow waves actively suppress relevant signals in deep sleep. Thus, the selection of relevant stimuli continues to operate during sleep but is strongly modulated by specific brain rhythms.

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Fig. 1: Experimental procedure.
Fig. 2: Reconstruction score and decoding performance across wake and NREM sleep.
Fig. 3: Spatiotemporal integration of acoustic information.
Fig. 4: Effect of sleep spindles, K-complexes and slow waves on stimulus reconstruction.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Acknowledgements

This research was supported by ANR grants (ANR-10-LABX-0087 and ANR-10-IDEX-0001-02), by the European Research Council (ERC project METAWARE to S.K.), by the CIFAR (to S.K.), by the SFRMS and IBRO (to T.A.) and by the DGA (to M.K.). We thank S. Shamma and D. Pressnitzer for discussion, C. Girard for her assistance throughout the experiment, and N. Obin and A. Roebel for their help in constructing the stimuli. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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Author notes

  1. These authors contributed equally: Guillaume Legendre, Thomas Andrillon.

Authors and Affiliations

  1. Brain and Consciousness Group (ENS, EHESS, CNRS), Département d’Études Cognitives, École Normale Supérieure—PSL Research University, Paris, France

    Guillaume Legendre, Thomas Andrillon, Matthieu Koroma & Sid Kouider

  2. École Doctorale Cerveau Cognition Comportement, Université Pierre et Marie Curie, Paris, France

    Thomas Andrillon & Matthieu Koroma

  3. Monash Institute of Cognitive and Clinical Neuroscience, School of Psychology, Monash University, Melbourne, Victoria, Australia

    Thomas Andrillon

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  1. Guillaume Legendre
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Contributions

S.K. and T.A. designed the study. G.L., T.A. and M.K. collected the data. T.A., G.L. and S.K. analysed and interpreted the data. S.K., T.A., G.L. and M.K. wrote the paper.

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Correspondence to Sid Kouider.

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Supplementary Results, Supplementary Figures 1–7, and Supplementary Tables 1 and 2

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Legendre, G., Andrillon, T., Koroma, M. et al. Sleepers track informative speech in a multitalker environment. Nat Hum Behav 3, 274–283 (2019). https://doi.org/10.1038/s41562-018-0502-5

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