Theta Phase-Coordinated Memory Reactivation Reoccurs in a Slow-Oscillatory Rhythm during NREM Sleep - PubMed (original) (raw)

Theta Phase-Coordinated Memory Reactivation Reoccurs in a Slow-Oscillatory Rhythm during NREM Sleep

Thomas Schreiner et al. Cell Rep. 2018.

Abstract

It has been proposed that sleep's contribution to memory consolidation is to reactivate prior encoded information. To elucidate the neural mechanisms carrying reactivation-related mnemonic information, we investigated whether content-specific memory signatures associated with memory reactivation during wakefulness reoccur during subsequent sleep. We show that theta oscillations orchestrate the reactivation of memories during both wakefulness and sleep. Reactivation patterns during sleep autonomously re-emerged at a rate of ∼1 Hz, indicating a coordination by slow oscillatory activity.

Keywords: EEG; consolidation; episodic memory; memory reactivation; oscillations; phase similarity; retrieval; sleep; theta.

Copyright © 2018 The Authors. Published by Elsevier Inc. All rights reserved.

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Graphical abstract

Figure 1

Figure 1

Experimental Design and Behavioral Results (A) Participants performed a vocabulary-learning task in the evening. They learned to associate Dutch words (cues) with German words (targets). After the initial learning phase, a cued recall, including feedback, was performed (recall1). Afterward, the cued recall was repeated without feedback (recall2). Subsequently, participants slept for 3 hr. During NREM sleep, 80 Dutch words (40 cued and 40 cued + feedback) were repeatedly presented. Memory performance was assessed in the final retrieval phase after sleep (B) Presenting single Dutch word cues during NREM sleep enhanced memory performance as compared to word-pair TMR and uncued words. Retrieval performance is indicated as percentage of recalled words, with performance before sleep set to 100%. Values are mean ± SEM. ∗∗p < 0.01.

Figure 2

Figure 2

Word-Specific Phase Similarity during Wake Retrieval (A) Significantly enhanced phase similarity during successful subsequent retrieval was observed early after cue onset (t = 0 s) in the theta range. t-values were summed across electrodes in the significant cluster. (B) t-statistics of similarity results averaged over time and electrodes indicate a peak at 5 Hz. (C) Time course and topography of phase similarity at 5 Hz, indicating a rapid reactivation of memory content. The one-second time window around the center of the strongest cluster is highlighted. For the time course, t-values were averaged across all electrodes (n = 83), showing the content-specific phase-similarity effect. The topography displays summed t-values of the averaged difference between 0 and 2.5 s. See also Figures S1, S2, and S3.

Figure 3

Figure 3

Word-Specific Phase Similarity between recall2 and TMR (A) Recurrent reactivation of recall-related phase patterns at 5 Hz during TMR emerged over right temporal electrodes. The topography displays the test statistics of the averaged difference in phase similarity between remembered and not-remembered words (0–2.5 s). The time course depicts t-values averaged across highlighted electrodes (n = 6). The phase similarity at a given time point reflects the similarity computed in a window of ±500 ms around this time point. (B) Assessing phase similarity at 5 Hz between every time point of retrieval and TMR confirmed the re-occurring pattern of similarity. (C) Source reconstruction. The difference in phase similarity for remembered and not-remembered items indicates effects in right (para)hippocampal regions and left frontal areas. (D) Frequency spectrum of the TMR similarity measures showed a ∼1 Hz periodicity of reactivation processes. Shading denotes SEM. (E) In line with behavioral predictions, providing a target stimulus after the TMR cue blocked associated reactivation processes. The time course depicts t-values averaged across highlighted electrodes in (A). Presentation of the target word is highlighted in petrol blue. Only a brief reactivation effect at 270 ms (before target word onset) emerged. The topography displays the test statistics of the averaged difference in phase similarity between remembered and not-remembered words (0–2.5 s). No significant cluster was found. See also Figures S1, S2, and S3.

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References

    1. Bendor D., Wilson M.A. Biasing the content of hippocampal replay during sleep. Nat. Neurosci. 2012;15:1439–1444. - PMC - PubMed
    1. Binder J.R., Desai R.H., Graves W.W., Conant L.L. Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb. Cortex. 2009;19:2767–2796. - PMC - PubMed
    1. Born J., Wilhelm I. System consolidation of memory during sleep. Psychol. Res. 2012;76:192–203. - PMC - PubMed
    1. Cairney S.A., Guttesen A.Á.V., El Marj N., Staresina B.P. Memory consolidation is linked to spindle-mediated information processing during sleep. Curr. Biol. 2018;28:948–954.e4. - PMC - PubMed
    1. Chen Z., Wilson M.A. Deciphering neural codes of memory during sleep. Trends Neurosci. 2017;40:260–275. - PMC - PubMed

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