Experimentally induced REM sleep fragmentation affects psychophysiological habituation to emotional stimuli

Rapid eye movement sleep is believed to reduce physiological reactivity to emotional experiences. While rapid eye movement 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 rapid eye movement 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 rapid eye movement sleep, a post-sleep emotional memory/reactivity reassessment, and a 48-h 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-heart rate deceleration). The stimulation procedure elicited cortical arousal during rapid eye movement sleep, increasing rapid eye movement sleep fragmentation without altering total sleep time, sleep efficiency, and wake after sleep onset. Stimulations reliably induced a distinct cortical arousal signature, characterized by increased higher EEG frequencies (alpha, sigma, beta, gamma). rapid eye movement sleep fragmentation compromised heart rate deceleration 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 rapid eye movement sleep continuity for proper psychophysiological habituation to emotional events, suggesting alpha intrusions as a potential cortical correlate of impaired habituation.