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Humans can learn new information during sleep

Nature Neuroscience volume 15, pages 1460–1465 (2012)Cite this article

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Abstract

During sleep, humans can strengthen previously acquired memories, but whether they can acquire entirely new information remains unknown. The nonverbal nature of the olfactory sniff response, in which pleasant odors drive stronger sniffs and unpleasant odors drive weaker sniffs, allowed us to test learning in humans during sleep. Using partial-reinforcement trace conditioning, we paired pleasant and unpleasant odors with different tones during sleep and then measured the sniff response to tones alone during the same nights' sleep and during ensuing wake. We found that sleeping subjects learned novel associations between tones and odors such that they then sniffed in response to tones alone. Moreover, these newly learned tone-induced sniffs differed according to the odor pleasantness that was previously associated with the tone during sleep. This acquired behavior persisted throughout the night and into ensuing wake, without later awareness of the learning process. Thus, humans learned new information during sleep.

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Figure 1: Partial-reinforcement trace conditioning between tones and odors during sleep.
Figure 2: EEG spectral analysis verified sleep during learning.
Figure 3: The sniff response revealed learning during sleep.
Figure 4: The sniff response revealed learning during NREM and REM sleep.

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References

  1. Hennevin, E., Huetz, C. & Edeline, J.M. Neural representations during sleep: from sensory processing to memory traces. Neurobiol. Learn. Mem. 87, 416–440 (2007).

    Article  Google Scholar 

  2. Portas, C.M. et al. Auditory processing across the sleep-wake cycle: simultaneous EEG and fMRI monitoring in humans. Neuron 28, 991–999 (2000).

    Article  CAS  Google Scholar 

  3. Rasch, B., Buchel, C., Gais, S. & Born, J. Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 315, 1426–1429 (2007).

    Article  CAS  Google Scholar 

  4. Rudoy, J.D., Voss, J.L., Westerberg, C.E. & Paller, K.A. Strengthening individual memories by reactivating them during sleep. Science 326, 1079 (2009).

    Article  CAS  Google Scholar 

  5. Antony, J.W., Gobel, E.W., O′Hare, J.K., Reber, P.J. & Paller, K.A. Cued memory reactivation during sleep influences skill learning. Nat. Neurosci. 15, 1114–1116 (2012).

    Article  CAS  Google Scholar 

  6. Clark, R.E., Manns, J.R. & Squire, L.R. Classical conditioning, awareness, and brain systems. Trends Cogn. Sci. 6, 524–531 (2002).

    Article  Google Scholar 

  7. Maho, C. & Bloch, V. Responses of hippocampal cells can be conditioned during paradoxical sleep. Brain Res. 581, 115–122 (1992).

    Article  CAS  Google Scholar 

  8. Hennevin, E., Hars, B., Maho, C. & Bloch, V. Processing of learned information in paradoxical sleep: relevance for memory. Behav. Brain Res. 69, 125–135 (1995).

    Article  CAS  Google Scholar 

  9. Fifer, W.P. et al. Newborn infants learn during sleep. Proc. Natl. Acad. Sci. USA 107, 10320–10323 (2010).

    Article  CAS  Google Scholar 

  10. Beh, H.C. & Barratt, P.E. Discrimination and conditioning during sleep as indicated by the electroencephalogram. Science 147, 1470–1471 (1965).

    Article  CAS  Google Scholar 

  11. Ikeda, K. & Morotomi, T. Classical conditioning during human NREM sleep and response transfer to wakefulness. Sleep 19, 72–74 (1996).

    Article  CAS  Google Scholar 

  12. Bruce, D.J., Evans, C.R., Fenwick, P.B. & Spencer, V. Effect of presenting novel verbal material during slow-wave sleep. Nature 225, 873–874 (1970).

    Article  CAS  Google Scholar 

  13. Emmons, W.H. & Simon, C.W. The non-recall of material presented during sleep. Am. J. Psychol. 69, 76–81 (1956).

    Article  CAS  Google Scholar 

  14. Peigneux, P., Laureys, S., Delbeuck, X. & Maquet, P. Sleeping brain, learning brain. The role of sleep for memory systems. Neuroreport 12, A111–A124 (2001).

    Article  CAS  Google Scholar 

  15. Wood, J.M., Bootzin, R.R., Kihlstrom, J.F. & Schacter, D.L. Implicit and explicit memory for verbal information presented during sleep. Psychol. Sci. 3, 236–239 (1992).

    Article  Google Scholar 

  16. Simon, C.W. & Emmons, W.H. Responses to material presented during various levels of sleep. J. Exp. Psychol. 51, 89–97 (1956).

    Article  CAS  Google Scholar 

  17. Lehmann, D. & Koukkou, M. Computer analysis of EEG wakefulness-sleep patterns during learning of novel and familiar sentences. Electroencephalogr. Clin. Neurophysiol. 37, 73–84 (1974).

    Article  CAS  Google Scholar 

  18. Tani, K. & Yoshii, N. Efficiency of verbal learning during sleep as related to the EEG pattern. Brain Res. 17, 277–285 (1970).

    Article  CAS  Google Scholar 

  19. Woodruff-Pak, D.S. & Disterhoft, J.F. Where is the trace in trace conditioning? Trends Neurosci. 31, 105–112 (2008).

    Article  CAS  Google Scholar 

  20. Arzi, A. et al. The influence of odorants on respiratory patterns in sleep. Chem. Senses 35, 31–40 (2010).

    Article  Google Scholar 

  21. Badia, P., Wesensten, N., Lammers, W., Culpepper, J. & Harsh, J. Responsiveness to olfactory stimuli presented in sleep. Physiol. Behav. 48, 87–90 (1990).

    Article  CAS  Google Scholar 

  22. Carskadon, M.A., Acebo, C. & Jenni, O.G. Regulation of adolescent sleep: implications for behavior. Ann. NY Acad. Sci. 1021, 276–291 (2004).

    Article  Google Scholar 

  23. Stuck, B.A. et al. Arousal responses to olfactory or trigeminal stimulation during sleep. Sleep 30, 506–510 (2007).

    Article  Google Scholar 

  24. Bensafi, M. et al. Olfactomotor activity during imagery mimics that during perception. Nat. Neurosci. 6, 1142–1144 (2003).

    Article  CAS  Google Scholar 

  25. Mainland, J. & Sobel, N. The sniff is part of the olfactory percept. Chem. Senses 31, 181–196 (2006).

    Article  Google Scholar 

  26. Resnik, J., Sobel, N. & Paz, R. Auditory aversive learning increases discrimination thresholds. Nat. Neurosci. 14, 791–796 (2011).

    Article  CAS  Google Scholar 

  27. Iber, C., Ancoli-Israel, S., Chesson, A. & Quan, S.F. The AASM Manual for the Scoring of Sleep and Associated Events (American Academy of Sleep Medicine, Westchester, Illinois, 2007).

  28. Olbrich, E. & Achermann, P. Analysis of the temporal organization of sleep spindles in the human sleep EEG using a phenomenological modeling approach. J. Biol. Phys. 34, 241–249 (2008).

    Article  Google Scholar 

  29. Walker, M.P. & Stickgold, R. Sleep, memory and plasticity. Annu. Rev. Psychol. 57, 139–166 (2006).

    Article  Google Scholar 

  30. Goel, N., Kim, H. & Lao, R.P. An olfactory stimulus modifies nighttime sleep in young men and women. Chronobiol. Int. 22, 889–904 (2005).

    Article  Google Scholar 

  31. Deschênes, M., Moore, J. & Kleinfeld, D. Sniffing and whisking in rodents. Curr. Opin. Neurobiol. 22, 243–250 (2012).

    Article  Google Scholar 

  32. Laing, D.G. Natural sniffing gives optimum odor perception for humans. Perception 12, 99–117 (1983).

    Article  CAS  Google Scholar 

  33. Dudai, Y. The restless engram: consolidations never end. Annu. Rev. Neurosci. 35, 227–247 (2012).

    Article  CAS  Google Scholar 

  34. Bramham, C.R. & Srebro, B. Synaptic plasticity in the hippocampus is modulated by behavioral state. Brain Res. 493, 74–86 (1989).

    Article  CAS  Google Scholar 

  35. Barnes, D.C., Chapuis, J., Chaudhury, D. & Wilson, D.A. Odor fear conditioning modifies piriform cortex local field potentials both during conditioning and during post-conditioning sleep. PLoS ONE 6, e18130 (2011).

    Article  CAS  Google Scholar 

  36. Gais, S. & Born, J. Declarative memory consolidation: mechanisms acting during human sleep. Learn. Mem. 11, 679–685 (2004).

    Article  Google Scholar 

  37. Mednick, S.C., Cai, D.J., Shuman, T., Anagnostaras, S. & Wixted, J.T. An opportunistic theory of cellular and systems consolidation. Trends Neurosci. 34, 504–514 (2011).

    Article  CAS  Google Scholar 

  38. Wilson, D.A. & Yan, X. Sleep-like states modulate functional connectivity in the rat olfactory system. J. Neurophysiol. 104, 3231–3239 (2010).

    Article  Google Scholar 

  39. Wilson, D.A. Single-unit activity in piriform cortex during slow-wave state is shaped by recent odor experience. J. Neurosci. 30, 1760–1765 (2010).

    Article  CAS  Google Scholar 

  40. Wilson, D.A., Hoptman, M.J., Gerum, S.V. & Guilfoyle, D.N. State-dependent functional connectivity of rat olfactory system assessed by fMRI. Neurosci. Lett. 497, 69–73 (2011).

    Article  CAS  Google Scholar 

  41. Marshall, L., Helgadottir, H., Molle, M. & Born, J. Boosting slow oscillations during sleep potentiates memory. Nature 444, 610–613 (2006).

    Article  CAS  Google Scholar 

  42. Nir, Y. & Tononi, G. Dreaming and the brain: from phenomenology to neurophysiology. Trends Cogn. Sci. 14, 88–100 (2010).

    Article  Google Scholar 

  43. Bekinschtein, T.A. et al. Classical conditioning in the vegetative and minimally conscious state. Nat. Neurosci. 12, 1343–1349 (2009).

    Article  CAS  Google Scholar 

  44. Nakano, T., Homae, F., Watanabe, H. & Taga, G. Anticipatory cortical activation precedes auditory events in sleeping infants. PLoS ONE 3, e3912 (2008).

    Article  Google Scholar 

  45. Nir, Y. et al. Regional slow waves and spindles in human sleep. Neuron 70, 153–169 (2011).

    Article  CAS  Google Scholar 

  46. Vyazovskiy, V.V. et al. Local sleep in awake rats. Nature 472, 443–447 (2011).

    Article  CAS  Google Scholar 

  47. Livneh, U. & Paz, R. An implicit measure of olfactory performance for non-human primates reveals aversive and pleasant odor conditioning. J. Neurosci. Methods 192, 90–95 (2010).

    Article  Google Scholar 

  48. Price, J.L. Olfactory system. in The Human Nervous System (ed. Paxinos, G.) 979–1001 (Academic Press, San Diego, 1990).

  49. Weinberger, N.M. Physiological memory in primary auditory cortex: characteristics and mechanisms. Neurobiol. Learn. Mem. 70, 226–251 (1998).

    Article  CAS  Google Scholar 

  50. Murakami, M., Kashiwadani, H., Kirino, Y. & Mori, K. State-dependent sensory gating in olfactory cortex. Neuron 46, 285–296 (2005).

    Article  CAS  Google Scholar 

  51. Bruck, D., Ball, M., Thomas, I. & Rouillard, V. How does the pitch and pattern of a signal affect auditory arousal thresholds? J. Sleep Res. 18, 196–203 (2009).

    Article  Google Scholar 

  52. Johnson, B.N. & Sobel, N. Methods for building an olfactometer with known concentration outcomes. J. Neurosci. Methods 160, 231–245 (2007).

    Article  Google Scholar 

  53. Johnson, B.N., Russell, C., Khan, R.M. & Sobel, N. A comparison of methods for sniff measurement concurrent with olfactory tasks in humans. Chem. Senses 31, 795–806 (2006).

    Article  Google Scholar 

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Acknowledgements

We would like to thank R. Paz for advice. This work was supported by the James S. McDonnell Foundation.

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Authors and Affiliations

  1. Department of Neurobiology, Weizmann Institute of Science, Rehovot, Israel

    Anat Arzi, Limor Shedlesky, Mor Ben-Shaul & Noam Sobel

  2. Sleep Disorders Unit, Loewenstein Rehabilitation Hospital, Raanana, Israel

    Khitam Nasser & Arie Oksenberg

  3. School of Behavioral Sciences, Academic College of Tel Aviv - Jaffa, Jaffa, Israel

    Ilana S Hairston

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  1. Anat Arzi
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Contributions

A.A. conceived the idea. A.A. and N.S. designed experiments. A.A., L.S. and M.B.-S. carried out the experiments. A.A. analyzed the data. K.N., A.O. and A.A. carried out sleep scoring. A.A., I.S.H., A.O. and N.S. wrote the manuscript.

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Correspondence to Anat Arzi.

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Arzi, A., Shedlesky, L., Ben-Shaul, M. et al. Humans can learn new information during sleep. Nat Neurosci 15, 1460–1465 (2012). https://doi.org/10.1038/nn.3193

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