Understanding the role of REM sleep fragmentation on emotional memory and emotional reactivity through a new methodological approach

Sleep is fundamental to allow proper memory and emotional processing. In particular, rapid eye movement (REM) sleep duration and continuity are supposed to be crucial for ensuring adequate encoding and consolidation of emotional events. However, how REM sleep acts on the emotional reactivity associated with the emotional information needs to be clarified. Different methodological limitations affect the studies in this field. Recently, studies on clinical populations highlighted that REM sleep fragmentation (manifested in cortical arousals and stage transitions that disrupt the continuity of REM periods) negatively interferes with emotional processing that is assumed to occur during REM sleep. Therefore, experimentally induced REM sleep fragmentation in healthy participants could be adopted as an alternative paradigm to investigate REM sleep's effects on emotional memory and emotional reactivity, overcoming existing methodological limitations. In this view, we aim to investigate the role of REM sleep in consolidating emotional memory and modulating emotional reactivity by inducing REM sleep fragmentation through cortical arousals elicited via a wristband delivering vibrotactile stimulations. Recruited participants underwent two experimental conditions (Fragmentation and Control) in a counterbalanced order. In each condition, the participants took part in: i) a baseline assessment of emotional reactivity followed by a stimulus encoding phase and a baseline assessment of emotional memory in the afternoon (at 18:00); ii) a nocturnal polysomnographic recording with 64-channel high-density EEG of the nocturnal sleep with (Fragmentation) or without (Control) vibrotactile stimulation; iii) a post-sleep emotional memory and emotional reactivity assessment one hour after the final awakening, (iv) and a follow-up assessment of emotional reactivity and emotional memory after 48 hours. The effects of the experimental manipulation of REM sleep continuity on emotional memory and emotional reactivity for negative and neutral stimuli were evaluated by collecting behavioural (old/new paradigm), self-report (self-assessment manikin scale), and physiological (skin conductance responses and heart rate deceleration) measurements. We demonstrated that experimentally induced REM sleep fragmentation led to a lack of psychophysiological habituation to previously encountered emotional stimuli in healthy participants without affecting their subjective emotional reactivity ratings and emotional memory consolidation. Moreover, we revealed that re-exposing participants to emotional stimuli after a night of experimental REM sleep fragmentation did not allow this information to be correctly processed during two subsequent nights of regular sleep. Finally, we proved that our new methodological approach of experimentally induced REM sleep fragmentation is able to hinder REM sleep continuity, minimising macrostructural sleep alteration. Altogether, our data support the importance of unperturbed REM sleep continuity in promoting a proper psychophysiological reaction to known emotional events.