Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Brief Communication
  • Published:

Stimulus-specific enhancement of fear extinction during slow-wave sleep

Abstract

Sleep can strengthen memory for emotional information, but whether emotional memories can be specifically targeted and modified during sleep is unknown. In human subjects who underwent olfactory contextual fear conditioning, re-exposure to the odorant context in slow-wave sleep promoted stimulus-specific fear extinction, with parallel reductions of hippocampal activity and reorganization of amygdala ensemble patterns. Thus, fear extinction may be selectively enhanced during sleep, even without re-exposure to the feared stimulus itself.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Behavioral results.
Figure 2: Sleep-related modulatory effects of target odorant re-exposure on fMRI activity.

Similar content being viewed by others

References

  1. Walker, M.P. & Stickgold, R. Neuron 44, 121–133 (2004).

    Article  CAS  Google Scholar 

  2. Diekelmann, S., Buchel, C., Born, J. & Rasch, B. Nat. Neurosci. 14, 381–386 (2011).

    Article  CAS  Google Scholar 

  3. Antony, J.W. et al. Nat. Neurosci. 15, 1114–1116 (2012).

    Article  CAS  Google Scholar 

  4. Rasch, B., Buchel, C., Gais, S. & Born, J. Science 315, 1426–1429 (2007).

    Article  CAS  Google Scholar 

  5. Bendor, D. & Wilson, M.A. Nat. Neurosci. 15, 1439–1444 (2012).

    Article  CAS  Google Scholar 

  6. Barnes, D.C., Chapuis, J., Chaudhury, D. & Wilson, D.A. PLoS ONE 6, e18130 (2011).

    Article  CAS  Google Scholar 

  7. Payne, J.D. & Kensinger, E.A. J. Cogn. Neurosci. 23, 1285–1297 (2011).

    Article  Google Scholar 

  8. Arzi, A. et al. Nat. Neurosci. 15, 1460–1465 (2012).

    Article  CAS  Google Scholar 

  9. Stout, S.C. & Miller, R. Behav. Processes 66, 7–16 (2004).

    Article  Google Scholar 

  10. Gottfried, J.A. & Dolan, R.J. Nat. Neurosci. 7, 1144–1152 (2004).

    Article  CAS  Google Scholar 

  11. Anagnostaras, S.G., Gale, G.D. & Fanselow, M.S. Hippocampus 11, 8–17 (2001).

    Article  CAS  Google Scholar 

  12. Milad, M.R. et al. Biol. Psychiatry 62, 446–454 (2007).

    Article  Google Scholar 

  13. Hobin, J.A., Ji, J. & Maren, S. Hippocampus 16, 174–182 (2006).

    Article  CAS  Google Scholar 

  14. Burwell, R.D. & Amaral, D.G. J. Comp. Neurol. 398, 179–205 (1998).

    Article  CAS  Google Scholar 

  15. Han, J.H. et al. Science 323, 1492–1496 (2009).

    Article  CAS  Google Scholar 

  16. Bouton, M.E. Biol. Psychiatry 52, 976–986 (2002).

    Article  Google Scholar 

  17. Herry, C. et al. Nature 454, 600–606 (2008).

    Article  CAS  Google Scholar 

  18. Wang, S.H., Teixeira, C.M., Wheeler, A.L. & Frankland, P.W. Nat. Neurosci. 12, 253–255 (2009).

    Article  Google Scholar 

  19. Huff, N.C., Hernandez, J.A., Blanding, N.Q. & LaBar, K.S. Behav. Neurosci. 123, 834–843 (2009).

    Article  Google Scholar 

  20. Mednick, S.C. et al. Trends Neurosci. 34, 504–514 (2011).

    Article  CAS  Google Scholar 

  21. Li, W., Howard, J.D., Parrish, T.B. & Gottfried, J.A. Science 319, 1842–1845 (2008).

    Article  CAS  Google Scholar 

  22. Howard, J.D. et al. Nat. Neurosci. 12, 932–938 (2009).

    Article  CAS  Google Scholar 

  23. Cousineau, D. Tutorials Quant. Meth. Psych. 1, 42–45 (2005).

    Article  Google Scholar 

  24. Iber, C., Ancoli-Israel, S., Chesson, A.L. & Quan, S.F. (American Academy of Sleep Medicine, 2007).

  25. Delorme, A. & Makeig, S. J. Neurosci. Methods 134, 9–21 (2004).

    Article  Google Scholar 

  26. Esterman, M., Tamber-Rosenau, B.J., Chiu, Y.C. & Yantis, S. Neuroimage 50, 572–576 (2010).

    Article  Google Scholar 

  27. Mai, J.K., Assheuer, J. & Paxinos, G. Atlas of the Human Brain (Academic Press, 1997).

Download references

Acknowledgements

We thank P. Zee, C. Westerberg and K.N. Wu for technical assistance, and J. Radulovic and K. Paller for insightful discussions. Support was provided from the US National Institutes of Health to K.K.H. (F32MH091967, T32NS047987) and to J.A.G. (R01DC010014, R21DC012014), and from the Northwestern University Center for Translational Imaging.

Author information

Authors and Affiliations

Authors

Contributions

K.K.H. conceived the experiment. K.K.H. and J.A.G. designed the research. K.K.H. conducted the research and analyzed the data. J.D.H. performed multivariate analyses. C.Z. performed spectral power analysis. All of the authors prepared the manuscript.

Corresponding author

Correspondence to Katherina K Hauner.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Tables 1–3 and Supplementary Figures 1 and 2 (PDF 2790 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hauner, K., Howard, J., Zelano, C. et al. Stimulus-specific enhancement of fear extinction during slow-wave sleep. Nat Neurosci 16, 1553–1555 (2013). https://doi.org/10.1038/nn.3527

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3527

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing