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 Mar 25;6(2):211-233.
doi: 10.3390/clockssleep6020015.

No Benefit in Memory Performance after Nocturnal Memory Reactivation Coupled with Theta-tACS

Sandrine Baselgia  1 , Florian H Kasten  2 , Christoph S Herrmann  3 , Björn Rasch  1 , Sven Paβmann  1   4
Affiliations

No Benefit in Memory Performance after Nocturnal Memory Reactivation Coupled with Theta-tACS

Sandrine Baselgia et al. Clocks Sleep. .

Abstract

Targeted memory reactivation (TMR) is an effective technique to enhance sleep-associated memory consolidation. The successful reactivation of memories by external reminder cues is typically accompanied by an event-related increase in theta oscillations, preceding better memory recall after sleep. However, it remains unclear whether the increase in theta oscillations is a causal factor or an epiphenomenon of successful TMR. Here, we used transcranial alternating current stimulation (tACS) to examine the causal role of theta oscillations for TMR during non-rapid eye movement (non-REM) sleep. Thirty-seven healthy participants learned Dutch-German word pairs before sleep. During non-REM sleep, we applied either theta-tACS or control-tACS (23 Hz) in blocks (9 min) in a randomised order, according to a within-subject design. One group of participants received tACS coupled with TMR time-locked two seconds after the reminder cue (time-locked group). Another group received tACS in a continuous manner while TMR cues were presented (continuous group). Contrary to our predictions, we observed no frequency-specific benefit of theta-tACS coupled with TMR during sleep on memory performance, neither for continuous nor time-locked stimulation. In fact, both stimulation protocols blocked the TMR-induced memory benefits during sleep, resulting in no memory enhancement by TMR in both the theta and control conditions. No frequency-specific effect was found on the power analyses of the electroencephalogram. We conclude that tACS might have an unspecific blocking effect on memory benefits typically observed after TMR during non-REM sleep.

Keywords: memory; non-REM sleep; targeted memory reactivation; transcranial alternating current stimulation.

PubMed Disclaimer

Conflict of interest statement

The authors declare no conflicts of interest.

Figures

Figure 1
Figure 1
(A) Experimental procedure. Participants learned 140 Dutch–German word pairs before sleep. During subsequent non-REM sleep, 84 Dutch cues were presented again. The cueing of vocabulary occurred during the first two sleep cycles: in one cycle, the cues were coupled with theta-tACS, and in the other cycle, they were coupled with a control stimulation (in the beta frequency range). The order of the stimulation was randomised. One group of participants (n = 21) received a continuous stimulation, while the other group (n = 16) received a time-locked stimulation (0.5 s after each cue onset). In each cycle, we alternated TMR blocks coupled with stimulation with TMR blocks without stimulation until a maximum of 5 blocks or until REM sleep was noticed. In the morning, participants were tested on the German translation of the Dutch words using a cued recall procedure. (B) Difference between continuous and time-locked stimulation. The continuous stimulation was started at the beginning of the TMR blocks and lasted for its whole duration (9 min). The time-locked stimulation was a 2 s stimulation, applied 0.5 s after each TMR cue of the 9 min block. (C) Relative difference between pre- and post-sleep recall—with performance of the pre-sleep recall set to 100%—in the continuous and time-locked groups for TMR cues coupled with theta-tACS, TMR cues coupled with a control stimulation and unpresented words (uncued). Neither time-locked nor continuous stimulation with theta-tACS during the re-exposure of Dutch words increased memory performance tested after sleep. Thus, stimulation with theta-tACS either during or shortly after the TMR of Dutch words did not improve memory consolidation compared with a control stimulation and with unpresented words.
Figure 2
Figure 2
Averaged oscillatory responses to words presented during non-REM sleep recorded in all channels (F3, F4, P3, P4, F7, F8, Fz, FC5, FC6, CP1, CP2, CP5, CP6, Pz). (A) Oscillatory power changes for all words (Hits, Misses) presented during non-REM sleep in both groups (continuous, time-locked). Word presentation during sleep led to the typical brain response encompassing an increase in the slow-wave activity (SWA), theta, and alpha bands (1–12 Hz), followed by an increase in the spindle and beta frequency bands (11–25 Hz). A similar pattern was observed in both groups individually, as shown in (B) for the continuous group and in (C) for the time-locked group. (D) Comparison of the oscillatory power changes between the continuous and the time-locked group: when comparing the general response between both groups, a higher beta power (21–25 Hz) was found in the continuous group, 0.89–1.09 s after cue onset, in the frontal regions (F3, F4, F7, F8, Fz, FC5, FC6; p = 0.028), as illustrated with the black dashed box. (E) Comparison of the oscillatory power changes between Hits and Misses combined for all conditions and groups: no difference was found.
Figure 3
Figure 3
Averaged oscillatory differences between Hits and Misses: (A) In the time-locked group, a higher theta power (5 Hz) was observed for theta-Hits (compared to theta-Misses) 550–800 ms after stimulus onset (p = 0.044). The dashed box indicates the time (550–800 ms)-frequency (5–5.5 Hz) area used to illustrate the topographical distribution shown in subfigure (B). Significant electrodes are represented in filled black dots. (C) This cluster was found neither in the control-tACS of the time-locked group nor in the continuous group in both (D) the theta-tACS condition and (E) the control condition. (E) Control-Hits vs. control-Misses in the continuous group: there was a statistical trend for a lower theta power for Hits, 1.92–2.26 s after cue onset in the control-tACS condition, in the frontal region (p = 0.079). (F) Theta-Hits vs. theta-Misses in the time-locked group, in the frontal right region: the cluster shown in (A) was observed specifically in the frontal right region (F4, F8, FC6; p = 0.012) of the theta-tACS condition in the time-locked group. (G) Mean theta power from the cluster shown in (F): exploratory t-tests on the extracted mean theta power in this time window in the right frontal region revealed that theta power was indeed higher for Hits compared to Misses in the theta-tACS condition of the time-locked group (t14 = −2.71, p = 0.017, d = 0.70), but not in the continuous group, nor in the control-tACS condition (all p-value > 0.284). (H) Correlation between theta power difference between Hits and Misses in the frontal right region and memory performance, both groups and stimulation conditions together: no correlation was found. The shaded area represents 95% confidence interval. *: p < 0.05.
Figure 4
Figure 4
Theta mean power during reactivation (TMR blocks without stimulation), 3–5 s after cue onset: In the frontal left (A) and frontal right (B) regions, theta mean power was significantly higher in the time-locked group compared to the continuous group (left: p = 0.011; right: p = 0.001). Neither main effect of the stimulation condition nor interaction were observed. Comparison of the theta mean power in TMR-only vs. TMR + tACS blocks in the time-locked group: in the time-locked group only, an analysis was performed to compare the theta mean power in TMR blocks without stimulation (TMR-only) and TMR blocks coupled with stimulation (TMR + tACS), 3–5 s after cue onset. In the frontal left (C) and frontal right (D) regions, theta mean power in the time-locked group was higher in the blocks without stimulation compared to the blocks coupled with tACS (left: p = 0.057; right: p = 0.008). Neither main effect of the stimulation condition nor interaction were observed. +: p ≤ 0.06, *: p < 0.05, **: 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. Paller K.A., Creery J.D., Schechtman E. Memory and Sleep: How Sleep Cognition Can Change the Waking Mind for the Better. Annu. Rev. Psychol. 2021;72:123–150. doi: 10.1146/annurev-psych-010419-050815. - DOI - PMC - 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. Maingret N., Girardeau G., Todorova R., Goutierre M., Zugaro M. Hippocampo-cortical coupling mediates memory consolidation during sleep. Nat. Neurosci. 2016;19:959–964. doi: 10.1038/nn.4304. - DOI - PubMed
    1. Ólafsdóttir H.F., Bush D., Barry C. The Role of Hippocampal Replay in Memory and Planning. Curr. Biol. 2018;28:R37–R50. doi: 10.1016/j.cub.2017.10.073. - DOI - PMC - PubMed

LinkOut - more resources