Labile or stable: opposing consequences for memory when reactivated during waking and sleep

Abstract

Memory consolidation is a dynamic process. Reconsolidation theory assumes that reactivation during wakefulness transiently destabilizes memories, requiring them to reconsolidate in order to persist. Memory reactivation also occurs during slow-wave sleep (SWS) and is assumed to underlie the consolidating effect of sleep. Here, we tested whether the same principle of transient destabilization applies to memory reactivation during SWS. We reactivated memories in humans by presenting associated odor cues either during SWS or wakefulness. Reactivation was followed by an interference task to probe memory stability. As we expected, reactivation during waking destabilized memories. In contrast, reactivation during SWS immediately stabilized memories, thereby directly increasing their resistance to interference. Functional magnetic resonance imaging revealed that reactivation during SWS mainly activated hippocampal and posterior cortical regions, whereas reactivation during wakefulness primarily activated prefrontal cortical areas. Our results show that reactivation of memory serves distinct functions depending on the brain state of wakefulness or sleep.

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Figure 1: Experimental procedures and memory performance after odor reactivation.
Figure 2: Brain activity associated with odor-induced memory reactivation during wakefulness and sleep.

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Acknowledgements

We thank I. Wilhelm for helpful discussions and J. Martens, F. Hobrack, M. Palm and K. Müller for assistance with data collection. This work was supported by grants from the Deutsche Forschungsgemeinschaft (SFB 654 and SFB TR 58).

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Contributions

S.D., J.B. and B.R. designed the experiments and wrote the paper. S.D. and B.R. carried out the experiments and analyzed the data. C.B. provided analytic tools.

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Correspondence to Jan Born or Björn Rasch.

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The authors declare no competing financial interests.

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Supplementary Tables 1–5 and Supplementary Results (PDF 43 kb)

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Diekelmann, S., Büchel, C., Born, J. et al. Labile or stable: opposing consequences for memory when reactivated during waking and sleep. Nat Neurosci 14, 381–386 (2011). https://doi.org/10.1038/nn.2744

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