Experimentally induced REM sleep fragmentation affects psychophysiological habituation to emotional stimuli

Rapid eye movement (REM) sleep is believed to reduce physiological reactivity to emotional experiences. While REM sleep fragmentation has been associated with maladaptive emotional processing in clinical and animal models, its causal role has not been experimentally isolated in healthy humans. In this study, we tested whether selectively fragmenting REM sleep impairs overnight psychophysiological habituation in healthy individuals, aiming to identify the cortical dynamics involved. Seventeen participants (mean age±SD, 23.18±3.94, 14 females) completed two counterbalanced conditions (Fragmentation and Control) each encompassing a baseline assessment of emotional memory/reactivity, a nocturnal polysomnography with or without wrist-applied vibrotactile stimulation during REM sleep, a post-sleep emotional memory/reactivity reassessment, and a 48-hour follow-up evaluation. Emotional memory was evaluated using an old/new paradigm, while emotional reactivity was assessed through self-report and physiological measures (electrodermal activity and heart rate deceleration-HRD). The stimulation procedure elicited cortical arousal during REM sleep, increasing REM sleep fragmentation without altering total sleep time, sleep efficiency, and wake after sleep onset. Stimulations reliably induced a distinct cortical arousal signature, characterised by increased higher EEG frequencies (alpha, sigma, beta, gamma). REM sleep fragmentation compromised HRD habituation to emotional stimuli at both post-sleep assessments without impacting electrodermal response, self-report evaluation, and recognition memory. Crucially, the degree of impaired cardiac habituation at both timepoints was strongly predicted by the magnitude of stimulation-induced alpha power over parieto-occipital regions. These findings indicated the importance of unperturbed REM sleep continuity for proper psychophysiological habituation to emotional events, suggesting alpha intrusions as a potential cortical correlate of impaired habituation.