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Sleep to forget: interference of fear memories during sleep

Abstract

Memories are consolidated and strengthened during sleep. Here we show that memories can also be weakened during sleep. We used a fear-conditioning paradigm in mice to condition footshock to an odor (conditioned stimulus (CS)). Twenty-four hours later, presentation of the CS odor during sleep resulted in an enhanced fear response when tested during subsequent wake. However, if the re-exposure of the CS odor during sleep was preceded by bilateral microinjections of a protein synthesis inhibitor into the basolateral amygdala, the subsequent fear response was attenuated. These findings demonstrate that specific fear memories can be selectively reactivated and either strengthened or attenuated during sleep, suggesting the potential for developing sleep therapies for emotional disorders.

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References

  1. Quirk GJ et al. Erasing fear memories with extinction training. J Neurosci 2010; 30: 14993–14997.

    Article  CAS  PubMed Central  Google Scholar 

  2. Schiller D et al. Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 2010; 463: 49–53.

    Article  CAS  PubMed Central  Google Scholar 

  3. Bouton ME . Context and behavioral processes in extinction. Learn Mem 2004; 11: 485–494.

    Article  PubMed Central  Google Scholar 

  4. Myers KM, Davis M . Mechanisms of fear extinction. Mol Psychiatry 2007; 12: 120–150.

    Article  CAS  Google Scholar 

  5. Honig WK, Urcuioli PJ . The legacy of Guttman and Kalish (1956): Twenty-five years of research on stimulus generalization. J Exp Anal Behav 1981; 36: 405–445.

    Article  CAS  PubMed Central  Google Scholar 

  6. Rasch B, Born J . About sleep's role in memory. Physiol Rev 2013; 93: 681–766.

    Article  CAS  PubMed Central  Google Scholar 

  7. Antony JW, Gobel EW, O'Hare JK, Reber PJ, Paller KA . Cued memory reactivation during sleep influences skill learning. Nat Neurosci 2012; 15: 1114–1116.

    Article  CAS  PubMed Central  Google Scholar 

  8. Diekelmann S, Buchel C, Born J, Rasch B . Labile or stable: opposing consequences for memory when reactivated during waking and sleep. Nat Neurosci 2011; 14: 381–386.

    Article  CAS  Google Scholar 

  9. Diekelmann S, Biggel S, Rasch B, Born J . Offline consolidation of memory varies with time in slow wave sleep and can be accelerated by cuing memory reactivations. Neurobiol Learn Mem 2012; 98: 103–111.

    Article  PubMed Central  Google Scholar 

  10. Paller KA, Voss JL . Memory reactivation and consolidation during sleep. Learn Mem 2004; 11: 664–670.

    Article  PubMed Central  Google Scholar 

  11. Rasch B, Buchel C, Gais S, Born J . Odor cues during slow-wave sleep prompt declarative memory consolidation. Science 2007; 315: 1426–1429.

    Article  CAS  PubMed Central  Google Scholar 

  12. Rudoy JD, Voss JL, Westerberg CE, Paller KA . Strengthening individual memories by reactivating them during sleep. Science 2009; 326: 1079.

    Article  CAS  PubMed Central  Google Scholar 

  13. van Dongen EV et al. Memory stabilization with targeted reactivation during human slow-wave sleep. Proc Natl Acad Sci USA 2012; 109: 10575–10580.

    Article  CAS  PubMed Central  Google Scholar 

  14. Nader K, Schafe GE, Le Doux JE . Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 2000; 406: 722–726.

    Article  CAS  Google Scholar 

  15. Graves LA, Heller EA, Pack AI, Abel T . Sleep deprivation selectively impairs memory consolidation for contextual fear conditioning. Learn Mem 2003; 10: 168–176.

    Article  PubMed Central  Google Scholar 

  16. Harris JA, Jones ML, Bailey GK, Westbrook RF . Contextual control over conditioned responding in an extinction paradigm. J Exp Psychol Anim Behav Process 2000; 26: 174–185.

    Article  CAS  PubMed Central  Google Scholar 

  17. Wanisch K, Wotjak CT . Time course and efficiency of protein synthesis inhibition following intracerebral and systemic anisomycin treatment. Neurobiol Learn Mem 2008; 90: 485–494.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Drs Chuluun Bayarsaikhan and Antoine Adamantidis for their help. AR was supported by NARSAD Young Investigator Award. Other grant support that contributed to this study are an NSF predoctoral fellowship to MM; grants from NIMH and the Klarman Family Foundation to LdL; and grants from NIH as well as DSRTF, and RDSF to HCH.

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Correspondence to H Craig Heller.

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Rolls, A., Makam, M., Kroeger, D. et al. Sleep to forget: interference of fear memories during sleep. Mol Psychiatry 18, 1166–1170 (2013). https://doi.org/10.1038/mp.2013.121

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