Selective suppression of rapid eye movement sleep increases next-day negative affect and amygdala responses to social exclusion

Abstract

Healthy sleep, positive general affect, and the ability to regulate emotional experiences are fundamental for well-being. In contrast, various mental disorders are associated with altered rapid eye movement (REM) sleep, negative affect, and diminished emotion regulation abilities. However, the neural processes mediating the relationship between these different phenomena are still not fully understood. In the present study of 42 healthy volunteers, we investigated the effects of selective REM sleep suppression (REMS) on general affect, as well as on feelings of social exclusion, cognitive reappraisal (CRA) of emotions, and their neural underpinnings. Using functional magnetic resonance imaging we show that, on the morning following sleep suppression, REMS increases general negative affect, enhances amygdala responses and alters its functional connectivity with anterior cingulate cortex during passively experienced experimental social exclusion. However, we did not find effects of REMS on subjective emotional ratings in response to social exclusion, their regulation using CRA, nor on functional amygdala connectivity while participants employed CRA. Our study supports the notion that REM sleep is important for affective processes, but emphasizes the need for future research to systematically investigate how REMS impacts different domains of affective experience and their neural correlates, in both healthy and (sub-)clinical populations.

Figure 1

Summary of the experimental procedure. Three groups of subjects spent two consecutive nights in the sleep laboratory. During both nights, polysomnography was recorded. In the second night, two groups were woken up as soon as they entered REM sleep or SWS (groups REMS and SWSS, respectively), while the control group was not woken up (CTL). The grey arrows indicate onsets of REM sleep and SWS upon which the respective groups were awakened. After waking up on the second morning, all subjects performed two sessions of the Cyberball game while inside the fMRI scanner. The game included a total of eight blocks, with four inclusion (INC) and four exclusion (EXC) blocks. During inclusion, subjects received the ball continuously throughout the block, while during exclusion, the other two players stopped throwing the ball to the participant soon after the beginning of the block, effectively excluding the participant from the game. Additionally, during the first four blocks (half INC, half EXC), subjects simply performed the task (VIEW), while during the second four blocks (half INC, half EXC) they were instructed to use cognitive reappraisal (CRA) to regulate their emotions.

Figure 2

Selective sleep suppression and general affect. (a) REM sleep was significantly more reduced in the REMS group than in the other two groups, whereas SWS suppression was significantly stronger in the SWSS group than in the other two groups. Suppression scores for REM (SWS) sleep are the difference of percentage REM (SWS) of TST between the habituation night minus the experimental night. (b) Ratings of general positive and negative affect, measured with the Positive And Negative Affect Scale (PANAS) on the mornings after the habituation night and after the experimental night, separately for the three groups. (c) Changes in negative (right) but not positive affect (left) from the habituation night to the experimental night correlate significantly with REM sleep suppression scores across all groups. Shaded areas represent 95% confidence intervals for simple bivariate regression. Error bars represent standard error of the mean. n.s. not significant.

Figure 3

Neural responses to ostracism are altered by selective REM sleep suppression. Left Neural responses for the contrast [EXC/VIEW > INC/VIEW] > [EXC/CRA > INC/CRA] differed significantly between the REMS group and the other two groups in the right amygdala, (peak MNI-coordinates: x = 26, y = − 2, z = − 28, surviving FWE-correction at p < 0.05 inside the a priori mask). Displayed at p < 0.005, uncorrected, for visualization purposes. Right Parameter estimates for the contrast EXC > INC in the VIEW session were positive in the REMS group, but did not deviate from 0 in the other two groups, nor in the CRA session for any of the three groups. In addition, parameter estimates for EXC > INC were significantly more positive in the REMS group during VIEW than during CRA, while sessions did not differ in the other two groups. See main text for details. ***p < 0.001. Error bars represent standard error of the mean.