[en] New information can be learned during sleep but the extent to which we can access this knowledge after awakening is far less understood. Using a novel Associative Transfer Learning paradigm, we show that, after hearing unknown Japanese words with sounds referring to their meaning during sleep, participants could identify the images depicting the meaning of newly acquired Japanese words after awakening (N = 22). Moreover, we demonstrate that this cross-modal generalization is implicit, meaning that participants remain unaware of this knowledge. Using electroencephalography, we further show that frontal slow-wave responses to auditory stimuli during sleep predicted memory performance after awakening. This neural signature of memory formation gradually emerged over the course of the sleep phase, highlighting the dynamics of associative learning during sleep. This study provides novel evidence that the formation of new associative memories can be traced back to the dynamics of slow-wave responses to stimuli during sleep and that their implicit transfer into wakefulness can be generalized across sensory modalities.
Disciplines :
Neurosciences & behavior
Author, co-author :
Koroma, Matthieu ; Université de Liège - ULiège > Département des sciences cliniques ; Brain and Consciousness Group (ENS, EHESS, CNRS), Département d'Études Cognitives, École Normale Supérieure, Paris, France ; École Doctorale Cerveau Cognition Comportement, Université Pierre et Marie Curie Sorbonne Universités, Paris, France
Elbaz, Maxime; Université de Paris, APHP, Hôtel-Dieu de Paris, Centre du Sommeil et de la Vigilance, EA 7330 VIFASOM Sommeil-Vigilance-Fatigue et Santé Publique, Paris, France
Léger, Damien; Université de Paris, APHP, Hôtel-Dieu de Paris, Centre du Sommeil et de la Vigilance, EA 7330 VIFASOM Sommeil-Vigilance-Fatigue et Santé Publique, Paris, France
Kouider, Sid; Brain and Consciousness Group (ENS, EHESS, CNRS), Département d'Études Cognitives, École Normale Supérieure, Paris, France
Language :
English
Title :
Learning New Vocabulary Implicitly During Sleep Transfers With Cross-Modal Generalization Into Wakefulness.
Alternative titles :
[fr] L'apprentissage implicite d'un nouveau vocabulaire durant le sommeil est transférable à l'éveil avec de la généralisation cross-modale
Original title :
[en] Learning New Vocabulary Implicitly During Sleep Transfers With Cross-Modal Generalization Into Wakefulness.
ERC - European Research Council ANR - Agence Nationale de la Recherche Direction Générale de l’Armement CIFAR - Canadian Institute for Advanced Research
Funding text :
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 SK), by the CIFAR (to SK), and by the DGA (to MK).
Andrillon T. Kouider S. (2016). Implicit memory for words heard during sleep. Neurosci. Consciousness 2016:niw014. 10.1093/nc/niw014 30356955
Andrillon T. Kouider S. (2020). The vigilant sleeper: neural mechanisms of sensory (de)coupling during sleep. Curr. Opin. Physiol. 15 47–59. 10.1016/j.cophys.2019.12.002
Andrillon T. Poulsen A. T. Hansen L. K. Léger D. Kouider S. (2016). Neural markers of responsiveness to the environment in human sleep. J. Neurosci. 36 6583–6596. 10.1523/JNEUROSCI.0902-16.2016 27307244
Andrillon T. Pressnitzer D. Léger D. Kouider S. (2017). Formation and suppression of acoustic memories during human sleep. Nat. Commun. 8:179. 10.1038/s41467-017-00071-z 28790302
Arzi A. Holtzman Y. Samnon P. Eshel N. Harel E. Sobel N. (2014). Olfactory aversive conditioning during sleep reduces cigarette-smoking behavior. J. Neurosci. 34 15382–15393. 10.1523/JNEUROSCI.2291-14.2014 25392505
Arzi A. Shedlesky L. Ben-Shaul M. Nasser K. Oksenberg A. Hairston I. S. et al. (2012). Humans can learn new information during sleep. Nat. Neurosci. 15 1460–1465. 10.1038/nn.3193 22922782
Bastien C. Campbell K. (1992). The evoked K-Complex: all-or-none phenomenon? Sleep 15 236–245. 10.1093/sleep/15.3.236 1621024
Bastuji H. García-Larrea L. Franc C. Mauguière F. (1995). Brain processing of stimulus deviance during slow-wave and paradoxical sleep: a study of human auditory evoked responses using the oddball paradigm. J. Clin. Neurophysiol. 12 155–167. 10.1097/00004691-199503000-00006 7797630
Benjamini Y. Yekutieli D. (2001). The control of the false discovery rate in multiple testing under dependency. Ann. Statistics. 29 1165–1188.
Berry D. C. Banbury S. Henry L. (1997). Transfer across form and modality in implicit and explicit memory. Quarterly J. Exp. Psychol. Hum. Exp. Psychol. 50 1–24. 10.1080/713755685 9080787
Blum D. Yonelinas A. P. (2001). Transfer across modality in perceptual implicit memory. Psychonomic Bull. Rev. 8 147–154. 10.3758/bf03196151 11340860
Blume C. del Giudice R. Lechinger J. Wislowska M. Heib D. P. J. Hoedlmoser K. et al. (2017). Preferential processing of emotionally and self-relevant stimuli persists in unconscious N2 sleep. Brain Lang. 167 72–82. 10.1016/j.bandl.2016.02.004 27039169
Bruce D. J. Evans C. R. Fenwick P. B. C. Spencer V. (1970). Effect of presenting novel verbal material during slow-wave sleep. Nature 225 873–874. 10.1038/225873a0 5415124
Canales-Johnson A. Merlo E. Bekinschtein T. A. Arzi A. (2020). Neural dynamics of associative learning during human sleep. Cereb. Cortex 30 1708–1715. 10.1093/cercor/bhz197 31690927
Cox R. van Driel J. de Boer M. Talamini L. M. (2014). Slow oscillations during sleep coordinate interregional communication in cortical networks. J. Neurosci. 34 16890–16901. 10.1523/JNEUROSCI.1953-14.2014 25505340
Dang-Vu T. T. Bonjean M. Schabus M. Boly M. Darsaud A. Desseilles M. et al. (2011). Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep. Proc. Natl. Acad. Sci. U S A. 108 15438–15443. 10.1073/pnas.1112503108 21896732
Dienes Z. Berry D. (1997). Implicit learning: below the subjective threshold. Psychonomic Bull. Rev. 4 3–23. 10.3758/BF03210769
Dorran D. Lawlor R. Coyle E. (2003). “High quality time-scale modification of speech using a peak alignment overlap-add algorithm (PAOLA),” in Proceedings of the 2003 IEEE International Conference on Acoustics, Speech, and Signal Processing, 2003. Proceedings. (ICASSP’03) (Piscataway, NJ: IEEE), 10.1109/ICASSP.2003.1198877
Halász P. (2016). The K-complex as a special reactive sleep slow wave – a theoretical update. Sleep Med. Rev. 29 34–40. 10.1016/j.smrv.2015.09.004 26606317
Iber C. Ancoli-Israel S. Chesson A. L. Quan S. F. (2007). The AASM Manual for the Scoring of Sleep and Associated Events: Rules, Terminology and Technical Specifications. Westchester, IL: American academy of sleep medicine.
Klinzing J. G. Niethard N. Born J. (2019). Mechanisms of systems memory consolidation during sleep. Nat. Neurosci. 22 1598–1610. 10.1038/s41593-019-0467-3 31451802
Kouider S. Dehaene S. (2007). Levels of processing during non-conscious perception: a critical review of visual masking. Philos. Trans. R. Soc. B: Biol. Sci. 362 857–875. 10.1098/rstb.2007.2093 17403642
Kouider S. Andrillon T. Barbosa L. S. Goupil L. Bekinschtein T. A. (2014). Inducing task-relevant responses to speech in the sleeping brain. Curr. Biol. 24 2208–2214. 10.1016/j.cub.2014.08.016 25220055
Lake B. M. Ullman T. D. Tenenbaum J. B. Gershman S. J. (2017). Building machines that learn and think like people. Behav. Brain Sci. 40 1–25. 10.1017/S0140525X16001837 27881212
Marshall L. Helgadóttir H. Mölle M. Born J. (2006). Boosting slow oscillations during sleep potentiates memory. Nature 444 610–613. 10.1038/nature05278 17086200
Massimini M. Huber R. Ferrarelli F. Hill S. Tononi G. (2004). The sleep slow oscillation as a traveling wave. J. Neurosci. 24 6862–6870. 10.1523/JNEUROSCI.1318-04.2004 15295020
Nir Y. Tononi G. (2010). Dreaming and the brain: from phenomenology to neurophysiology. Trends Cogn. Sci. 14 88–100. 10.1016/j.tics.2009.12.001 20079677
Nir Y. Staba R. J. Andrillon T. Vyazovskiy V. V. Cirelli C. Fried I. et al. (2011). Regional slow waves and spindles in human sleep. Neuron 70 153–169. 10.1016/j.neuron.2011.02.043 21482364
Oudiette D. Paller K. A. (2013). Upgrading the sleeping brain with targeted memory reactivation. Trends Cogn. Sci. 17 142–149. 10.1016/j.tics.2013.01.006 23433937
Peigneux P. Laureys S. Delbeuck X. Maquet P. (2001). Sleeping brain, learning brain. Role Sleep Memory Systems Neuroreport 12 A111–A124. 10.1097/00001756-200112210-00001 11742260
Puchkova A. N. (2020). Studies of learning during sleep: problems, progress, and perspectives. Neurosci. Behav. Physiol. 50 257–263. 10.1177/1073858406292647 16957003
Rasch B. Born J. (2013). About sleep’s role in memory. Physiol. Rev. 93 681–766. 10.1152/physrev.00032.2012 23589831
Rasch B. Büchel C. Gais S. Born J. (2007). Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 315 1426–1429. 10.1126/science.1138581 17347444
Ruch S. Henke K. (2020). Learning during sleep: a dream comes true? Trends Cogn. Sci. 24 170–172. 10.1016/j.tics.2019.12.007 31954628
Ruch S. Koenig T. Mathis J. Roth C. Henke K. (2014). Word encoding during sleep is suggested by correlations between word-evoked up-states and post-sleep semantic priming. Front. Psychol. 5:1319. 10.3389/fpsyg.2014.01319 25452740
Scott R. B. Samaha J. Chrisley R. Dienes Z. (2018). Prevailing theories of consciousness are challenged by novel cross-modal associations acquired between subliminal stimuli. Cognition 175 169–185. 10.1016/j.cognition.2018.02.008 29544152
Strauss M. Sitt J. D. King J.-R. Elbaz M. Azizi L. Buiatti M. et al. (2015). Disruption of hierarchical predictive coding during sleep. Proc. Natl. Acad. Sci. U S A. 112 E1353–E1362. 10.1073/pnas.1501026112 25737555
Torrey L. Shavlik J. (2010). “Transfer learning,” in Handbook of Research on Machine Learning Applications and Trends: Algorithms, Methods, and Techniques, eds Soria E. Martin J. Magdalena R. Martinez M. Serrano A. (Pennsylvania, PA: IGI global), 242–264.
Walker M. P. Brakefield T. Hobson J. A. Stickgold R. (2003). Dissociable stages of human memory consolidation and reconsolidation. Nature 425 616–620. 10.1038/nature01930 14534587
Wood J. M. Bootzin R. R. Kihlstrom J. F. Schacter D. L. (1992). Implicit and explicit memory for verbal information presented during sleep. Psychol. Sci. 3 236–240. 10.1111/j.1467-9280.1992.tb00035.x
Yeung N. Summerfield C. (2012). Metacognition in human decision-making: confidence and error monitoring. Philos. Trans. R. Soc. B: Biol. Sci. 367 1310–1321. 10.1098/rstb.2011.0416 22492749
Züst M. A. Ruch S. Wiest R. Henke K. (2019). Implicit vocabulary learning during sleep is bound to slow-wave peaks. Curr. Biol. 29 541–553.e7. 10.1016/j.cub.2018.12.038. 30713104
