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

Robert W Glosemeyer,Ulrich Koehler,Laura Müller-Pinzler,David S Stolz,Ines Wilhelm,Stefan Westermann,Werner Cassel,Stefan Borgwardt,Sören Krach,Frieder M Paulus,Karl Kesper,Susanne Diekelmann,Armin Steffen

doi:10.1038/s41598-020-74169-8

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.

Highlights

IntroductionPositive general affect, and the ability to regulate emotional experiences are fundamental for well-being
Healthy sleep, positive general affect, and the ability to regulate emotional experiences are fundamental for well-being
The REMS and SWSS groups were experimentally disturbed often in the experimental night (REMS: M = 15.29, SD = 5.25; SWSS: M = 15.70, SD = 8.71; t(25) = 0.15, p = 0.881), and the SWSS and control group with regular sleep (CTL) groups were similar with regard to the amount of rapid eye movement (REM) sleep suppression (t(22) = 0.52, two-sided p = 0.608; see Table 1 and Fig. 2a for details)

Summary

Introduction

Positive general affect, and the ability to regulate emotional experiences are fundamental for well-being. 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. The existing literature suggests that the selective deprivation of REM sleep mainly disturbs the consolidation of emotional memories[28,29,30], whereas the selective suppression of SWS mainly impairs emotionally-neutral declarative memory encoding and c onsolidation[31,32]. These experimental findings are in line with clinical observations suggesting that REM sleep in particular is closely tied with emotional functioning[19]. Following a night of sleep, a low amount of REM sleep was associated with a decline in anterior cingulate cortex (ACC)-amygdala c onnectivity[18], possibly reflecting a specific effect of REM sleep on cognitive control of emotions[42]

Objectives

Methods

Results

Conclusion