Targeted memory reactivation during REM sleep may selectively enhance the late positive potential amplitude in previously encountered negative images: preliminary findings

Abstract

The function of rapid eye movement (REM) sleep in consolidating emotional memories and reducing emotional charge has been studied, but evidence remains conflicting. Our study employed the targeted memory reactivation (TMR) technique, which posits that specific sleep memories can be reactivated through sensory stimuli during sleep. Additionally, the late positive potential (LPP), a component of event-related brain potentials, was measured while participants (N = 16, 22.5 ± 1.2 years) viewed negative, neutral, or positive images (old images) paired with an odor stimulus. During subsequent REM sleep, the same odor was presented in the TMR condition, while an odorless stimulus was presented in the control condition. Upon awakening, participants performed the same task as before sleep, with new images added to test memory. The results demonstrated that TMR increased the LPP amplitude between 500 and 800 ms after image onset following sleep for negative old images; however, no changes were observed in the LPP in the same range for negative new images and neutral or positive images. TMR during REM sleep did not influence performance on the memory task, nor did it affect levels of arousal or emotional valence immediately after viewing the emotional images. These preliminary findings from our pilot study suggest that either the presentation of phenylethyl alcohol itself or the reprocessing induced by TMR during REM sleep selectively enhances the LPP in emotional processing of previously encountered negative stimuli. Due to the small sample size of this study, further investigation is warranted to evaluate the robustness of the results.

Keywords: REM sleep; emotion; late positive potential; olfactory stimulation; targeted memory reactivation.

Figure 1.

Experimental design and experimental day schedule. (A) After the participants had passed the screening online, an adaptation night was conducted for participants who had slept in the laboratory for the first time. After the adaptation night, the participants underwent a 1-week lifestyle control period to adjust their sleep–wake rhythms. Each participant spent one night in the experimental condition and another in the control condition. (B) Participants arrived at the laboratory at 20:00, where they applied the electroencephalogram electrodes. After undergoing the psychomotor vigilance test and completing a questionnaire, the emotional picture task was performed twice (pre-sleep 1 and pre-sleep 2) starting at 22:20. The participants went to bed at 24:00 and woke up at 08:00 the next day. When the experimenter detected REM sleep, odor or odorless stimuli were presented. After the participants woke up at 8:00 the next day, participants underwent psychomotor vigilance test at 08:30 and completed the questionnaire. Participants performed the emotional picture task (Post) starting at 8:50; electroencephalogram was recorded.

Figure 2.

Emotional picture task. After cross fixation first appeared randomly (2.0–2.5 seconds) (1), negative, neutral, or positive images were presented (1.5 seconds) (2). Participants were required to rate their valence (3) and arousal (4) using a self-assessment manikin. At the post-task, participants completed a memory test in addition to the pre-sleep procedure. Participants were asked to discriminate whether the presented picture was old or new in this test (5). Images were retrieved from Openverse ("SNAKE COILED ON LOG - CROOKED RIVER NATIONAL GRASSLAND" by the Forest Service Pacific, Northwest Region, available under Public Domain Mark 1.0 at https://wordpress.org/openverse/image/43b00faa-f58b-4e3d-822b-cfb5ae28f269) and the Self-Assessment Manikin as described previously [42].

Figure 3.

Sleepiness and mood before bedtime (Pre) and after waking (Post). (A) Mean reciprocal response time (1/s) in the psychomotor vigilance test, (B) Karolinska Sleepiness Scale, (C) FI in profile of mood states second edition-adult short. No significant differences existed between the odor and control conditions regarding sleepiness and fatigue before the emotional picture task. (D) DD. (E) TA. (F) Total Mood State in profile of mood states 2. The odor condition during REM sleep decreases next-day depression and the overall negative affect. Red boxes represent the odor condition, and blue boxes represent the control condition. Tukey plots illustrate the box plots, which show the median (central line), 25th percentile, and 75th percentile (lower and upper box limits). Tukey error bars indicate 1.5 times the 25th and 75th percentiles or maximum and minimum values. *:p < .05 with Bonferroni correction, **:p < .01 with Bonferroni correction

Figure 4.

Affective rating after sleep. Valence (a–c) and arousal (d–f) of the new and old images. Negative (a, d), neutral (b, e), positive (c, f). No differences in the valence and arousal were found between the conditions after waking. Red boxes represent the odor condition, and blue boxes represent the control condition. Tukey error bars indicate 1.5 times the 25th and 75th percentiles or maximum and minimum values.

Figure 5.

Averaged event-related potential (μV) recorded from Fz, Cz, Pz of the new (A, C, E) and old images (B, D, F) after waking up for negative (A, B), neutral (C, D), and positive (E, F) images. Red lines indicate the odor stimulation condition, and blue lines indicate the control condition. Shaded areas represent the standard error of the mean.

Figure 6.

Late positive potential (LPP) amplitudes averaged over 10 electrodes on the scalp at 300–500 ms (A–C) and 500–800 ms (D–F) after sleep. The LPP amplitude in 300–500 ms was larger in the odor condition than in the control condition. After odor stimulation during REM sleep, the LPP amplitude in 500–800 ms increased only for old negative images. Tukey error bars indicate 1.5 times the 25th and 75th percentiles or maximum and minimum values. *:p < .05 with Bonferroni correction.

Figure 7.

Event-related potentials elicited by negative (A, B), neutral (C, D), and positive (E, F) images during the pre-sleep 1 (A, C, E) and pre-sleep 2 (B, D, F) sessions. Red lines indicate the odor stimulation condition, and blue lines indicate the control condition. Shaded areas represent the standard error of the mean.

Figure 8.

The influence of odor condition on the memories. (A) Hit rate. (B) d’. There were no differences in memory accuracy between conditions. Red boxes represent the odor condition, and blue boxes represent the control condition. Tukey error bars indicate 1.5 times the 25th and 75th percentiles or maximum and minimum values. *:p < .05 with Bonferroni correction, **:p < .01 with Bonferroni correction.