Opposite effect of motivated forgetting on sleep spindles during stage 2 and slow wave sleep

Abstract

Memories selectively benefit from sleep. In addition to the importance of the consolidation of relevant memories, the capacity to forget unwanted memories is also crucial. We investigated the effect of suppressing unwanted memories on electroencephalography activity of subsequent sleep using a motivated forgetting (MF) paradigm as compared with a control non-forgetting task. Subjects were randomly assigned to nap or no-nap groups. We used a modified version of the think/no-think paradigm with dominant number of no-think words cued to be forgotten and included only subjects capable of suppressing unwanted memories by performing an initial subject inclusion experiment. In both groups and conditions, the performance of the subjects in recalling the word pairs learned in the beginning of the day was evaluated in a final recall test. We found that both nap and no-nap groups recalled significantly less no-think words in the MF condition compared to the control condition. Moreover, for the nap group, in the MF compared to the control condition, spindle power and density increased during stage 2 (S2) whereas they decreased during slow wave sleep (SWS). Interestingly, recall performance of no-think words was negatively correlated with spindle power during S2 whereas it was positively correlated with spindle power during SWS. These results indicate that sleep spindles are sensitive to the previous MF experiences and suggest a differential role of sleep spindles during S2 and SWS in memory processing during sleep.

Manipulating neural activity and sleep-dependent memory consolidation

“…For example, when, after learning a list of word pairs, subjects are instructed to forget correspondingly cued words (motivated forgetting), the relation of post-task spindle density during light versus deep NREM sleep differed as compared to a control condition (Figure 2). We found higher spindle density in N2 during sleep subsequent to motivated forgetting leading to the notion that spindles during N2 enhance the erasure of unwanted memories (Dehnavi et al, 2019;Figure 2). Regardless of the specific function, it is well conceivable that stimulation during post-task N2 versus N3 would differentially affect the ongoing consolidation process.…”

“…The motivated forgetting task is associated with differential spindle density in light NREM sleep stage N2 and deep NREM sleep stage N3 as compared to sleep after a control condition. Thus, reflecting discrepant processing demands during both sleep states (control, gray; motivated forgetting, red; adapted from Dehnavi et al 2019). Stimulation procedures reveal often weak effect sizes: In addition to stimulation efficacy depending on parameters of the stimulation and neuroanatomical features, induced neural responses depend on interactions between interindividual factors and processing demands.…”

“…W, Wake. The asterisks indicate significant differences: *, p < 0.05; **p < 0.01. between learning and stimulation (Lu et al, 2018;Miyamoto et al, 2016), subjects' cognitive ability (Koo et al, 2018), different processing demands of the learning material, and/ or differences in NREM sleep stage composition at the time of stimulation (Dehnavi et al, 2019;Jiang et al, 2019;Lerner et al, 2019; Figure 2). For example, when, after learning a list of word pairs, subjects are instructed to forget correspondingly cued words (motivated forgetting), the relation of post-task spindle density during light versus deep NREM sleep differed as compared to a control condition (Figure 2).…”

Does sleep selectively strengthen certain memories over others? A critical review of the literature

“…In the Dehnavi et al (2019) study, there were several significant findings regarding differences between sleep after the T/NT task as compared to sleep after a control task that did not involve motivated forgetting. Such effects are, however, beyond the scope of this review, and there were no correlations between sleep variables specifically during post-learning sleep after the T/NT task and memory performance.…”

“…The SIF effects did not differ between the groups. In the Dehnavi et al (2019) study, there were no baseline items but instead only Think and No-Think items. Unlike other studies using this paradigm, this was also a within-subjects design, which means that participants could have been expecting the memory test.…”