Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2024 Apr 20;14(1):9057.
doi: 10.1038/s41598-024-59696-y.

Comparing targeted memory reactivation during slow wave sleep and sleep stage 2

Julia Carbone  1   2 , Carlos Bibian  1   2 , Jan Born  1   3   4 , Cecilia Forcato  5 , Susanne Diekelmann  6   7
Affiliations

Comparing targeted memory reactivation during slow wave sleep and sleep stage 2

Julia Carbone et al. Sci Rep. .

Abstract

Sleep facilitates declarative memory consolidation, which is assumed to rely on the reactivation of newly encoded memories orchestrated by the temporal interplay of slow oscillations (SO), fast spindles and ripples. SO as well as the number of spindles coupled to SO are more frequent during slow wave sleep (SWS) compared to lighter sleep stage 2 (S2). But, it is unclear whether memory reactivation is more effective during SWS than during S2. To test this question, we applied Targeted Memory Reactivation (TMR) in a declarative memory design by presenting learning-associated sound cues during SWS vs. S2 in a counterbalanced within-subject design. Contrary to our hypothesis, memory performance was not significantly better when cues were presented during SWS. Event-related potential (ERP) amplitudes were significantly higher for cues presented during SWS than S2, and the density of SO and SO-spindle complexes was generally higher during SWS than during S2. Whereas SO density increased during and after the TMR period, SO-spindle complexes decreased. None of the parameters were associated with memory performance. These findings suggest that the efficacy of TMR does not depend on whether it is administered during SWS or S2, despite differential processing of memory cues in these sleep stages.

PubMed Disclaimer

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Memory task and experimental design. (a) During training, 30 sound-syllable-word associations were presented (German words). For each association, the sound was presented first for 2.9 s and continued accompanied by the word written on the screen and spoken aloud for 1.5 s. After a 4 s break, the next association appeared. In the cued recall test, for each association, the sound was presented for 2.9 s and continued accompanied by the first syllable of the associated word for 1.5 s. Afterwards, a microphone appeared on the screen and participants had 5 s to say the word aloud (sound continued during the entire period). Independently of their answer, correct feedback was given with the word spoken and written on the screen for 1.5 s. During Targeted memory reactivation (TMR, Reactivation), each sound was first presented alone for an average of 2.9 s, then the syllable was played once with the sound continuing in the background for another 1.5 s. After a 7 s break, the next cue was presented (until each cue was presented once). In the interference task, subjects performed the same task as for the training session with the same sounds associated to new words. During testing, each sound was presented for 0.5 s and then subjects were asked to say the word aloud. (b) Training and the cued recall test took place in the evening (22:30 h) and subjects went to bed at ~ 23:00 h. TMR took place during the first sleep cycle, with half of the cues being presented in SWS and the other half in S2 (yellow and blue lines) in counterbalanced order. In the next morning, subjects learned an interference task after 1 h of waking up. Another 30 min later, they took part in the testing session.
Figure 2
Figure 2
Memory performance and changes in oscillatory activity upon cueing during SWS and S2. (a) Participants' performance was not significantly different for cues presented in S2 or SWS. Memory change: number of correct words at testing minus number of correct words at training. Means ± SEM (vertical bars) are shown. (b) Time–frequency representations (TFR) for cues presented during S2 and SWS, each with their corresponding event-related potential (ERP, black line). Color maps show power changes relative to a 1 s baseline right before sound onset (i.e. − 4 to − 3 s). TFR were aligned at time-point zero to the syllable cue onset. Lower panel indicates timeline for the sound (symbolized by musical notes) and the syllable cue (symbolized by speaker and ‘KA’ syllable). (c) Cues presented in SWS elicited larger ERP amplitudes than those in S2. Average ERP amplitudes for single subjects as well as the means ± SEM are shown. * P < 0.05.
Figure 3
Figure 3
Density of slow oscillations (SO), fast spindles and SO-Spindle complexes. Each bar indicates density calculated within a period of interest: “Pre”, a 3-min period immediately before the cueing period; “React”, during the 3-min cueing period; and “Post”, a 3-min period immediately after the cueing period. Yellow bars correspond to S2 and blue bars to SWS. SO density is shown for frontal electrodes, fast spindle density for parietal electrodes and SO-spindle complexes density is shown for central electrodes. Means ± SEM (vertical bars) are shown. Significances indicate results of Post-hoc t-tests corrected for multiple comparisons. ** P < 0.01, *** P < 0.001.
See this image and copyright information in PMC

Similar articles

See all similar articles

References

    1. Diekelmann S, Born J. The memory function of sleep. Nat. Rev. Neurosci. 2010;11:114–126. doi: 10.1038/nrn2762. - DOI - PubMed
    1. Rasch B, Born J. About sleep’s role in memory. Physiol. Rev. 2013;93:681–766. doi: 10.1152/physrev.00032.2012. - DOI - PMC - PubMed
    1. Stickgold R. Neuroscience: A memory boost while you sleep. Nature. 2006;444:559–560. doi: 10.1038/nature05309. - DOI - PubMed
    1. Paller KA, Creery JD, Schechtman E. Memory and sleep: How Sleep cognition can change the waking mind for the better. Annu. Rev. Psychol. 2021;72:123–130. doi: 10.1146/annurev-psych-010419-050815. - DOI - PMC - PubMed
    1. Ackermann S, Rasch B. Differential effects of non-REM and REM sleep on memory consolidation? Curr. Neurol. Neurosci. Rep. 2014;14(1):10. - PubMed