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.
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References
Walker, M.P. & Stickgold, R. Neuron 44, 121–133 (2004).
Diekelmann, S., Buchel, C., Born, J. & Rasch, B. Nat. Neurosci. 14, 381–386 (2011).
Antony, J.W. et al. Nat. Neurosci. 15, 1114–1116 (2012).
Rasch, B., Buchel, C., Gais, S. & Born, J. Science 315, 1426–1429 (2007).
Bendor, D. & Wilson, M.A. Nat. Neurosci. 15, 1439–1444 (2012).
Barnes, D.C., Chapuis, J., Chaudhury, D. & Wilson, D.A. PLoS ONE 6, e18130 (2011).
Payne, J.D. & Kensinger, E.A. J. Cogn. Neurosci. 23, 1285–1297 (2011).
Arzi, A. et al. Nat. Neurosci. 15, 1460–1465 (2012).
Stout, S.C. & Miller, R. Behav. Processes 66, 7–16 (2004).
Gottfried, J.A. & Dolan, R.J. Nat. Neurosci. 7, 1144–1152 (2004).
Anagnostaras, S.G., Gale, G.D. & Fanselow, M.S. Hippocampus 11, 8–17 (2001).
Milad, M.R. et al. Biol. Psychiatry 62, 446–454 (2007).
Hobin, J.A., Ji, J. & Maren, S. Hippocampus 16, 174–182 (2006).
Burwell, R.D. & Amaral, D.G. J. Comp. Neurol. 398, 179–205 (1998).
Han, J.H. et al. Science 323, 1492–1496 (2009).
Bouton, M.E. Biol. Psychiatry 52, 976–986 (2002).
Herry, C. et al. Nature 454, 600–606 (2008).
Wang, S.H., Teixeira, C.M., Wheeler, A.L. & Frankland, P.W. Nat. Neurosci. 12, 253–255 (2009).
Huff, N.C., Hernandez, J.A., Blanding, N.Q. & LaBar, K.S. Behav. Neurosci. 123, 834–843 (2009).
Mednick, S.C. et al. Trends Neurosci. 34, 504–514 (2011).
Li, W., Howard, J.D., Parrish, T.B. & Gottfried, J.A. Science 319, 1842–1845 (2008).
Howard, J.D. et al. Nat. Neurosci. 12, 932–938 (2009).
Cousineau, D. Tutorials Quant. Meth. Psych. 1, 42–45 (2005).
Iber, C., Ancoli-Israel, S., Chesson, A.L. & Quan, S.F. (American Academy of Sleep Medicine, 2007).
Delorme, A. & Makeig, S. J. Neurosci. Methods 134, 9–21 (2004).
Esterman, M., Tamber-Rosenau, B.J., Chiu, Y.C. & Yantis, S. Neuroimage 50, 572–576 (2010).
Mai, J.K., Assheuer, J. & Paxinos, G. Atlas of the Human Brain (Academic Press, 1997).
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.
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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.
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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
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DOI: https://doi.org/10.1038/nn.3527
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