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Rapid Eye Movement (REM) sleep has been shown to modulate the consolidation of fear memories, a process that may contribute to the development of Post-Traumatic Stress Disorder (PTSD). However, contradictory findings have been reported regarding the direction of this modulation and its differential effects on recall versus generalization. In two complementary experiments, we addressed this by employing sleep deprivation protocols together with a novel fear-conditioning paradigm that required the discrimination between coexisting threat and safety signals. Using skin conductance responses and functional imaging (fMRI), we found two opposing effects of REM sleep: While REM impaired recall of the original threat memories, it improved the ability to generalize these memories to novel situations that emphasized the discrimination between threat and safety signals. These results, as well as previous findings in healthy participants and patients diagnosed with PTSD, could be explained by the degree to which the balance between threat and safety signals for a given stimulus was predictive of threat. We suggest that this account can be integrated with contemporary theories of sleep and fear learning, such as the REM recalibration hypothesis.

Sleep, and particularly rapid eye movement sleep (REM), has been implicated in the modulation of neural activity following fear conditioning and extinction in both human and animal studies. It has long been presumed that such effects play a role in the formation and persistence of posttraumatic stress disorder, of which sleep impairments are a core feature. However, to date, few studies have thoroughly examined the potential effects of sleep prior to conditioning on subsequent acquisition of fear learning in humans. Furthermore, these studies have been restricted to analyzing the effects of a single night of sleep—thus assuming a state-like relationship between the two. In the current study, we used long-term mobile sleep monitoring and functional neuroimaging (fMRI) to explore whether trait-like variations in sleep patterns, measured in advance in both male and female participants, predict subsequent patterns of neural activity during fear learning. Our results indicate that higher baseline levels of REM sleep predict reduced fear-related activity in, and connectivity between, the hippocampus, amygdala and ventromedial PFC during conditioning. Additionally, skin conductance responses (SCRs) were weakly correlated to the activity in the amygdala. Conversely, there was no direct correlation between REM sleep and SCRs, indicating that REM may only modulate fear acquisition indirectly. In a follow-up experiment, we show that these results are replicable, though to a lesser extent, when measuring sleep over a single night just before conditioning. As such, baseline sleep parameters may be able to serve as biomarkers for resilience, or lack thereof, to trauma.SIGNIFICANCE STATEMENTNumerous studies over the past two decades have established a clear role of sleep in fear-learning processes. However, previous work has focused on the effects of sleep following fear acquisition, thus neglecting the potential effects of baseline sleep levels on the acquisition itself. The current study provides the first evidence in humans of such an effect. Specifically, the results of this study suggest that baseline rapid eye movement (REM) sleep may serve a protective function against enhanced fear encoding through the modulation of connectivity between the hippocampus, amygdala, and the ventromedial PFC. Building on this finding, baseline REM measurements may serve as a noninvasive biomarker for resilience to trauma or, conversely, to the potential development of posttraumatic stress disorder following trauma.

Human studies of sleep and cognition have established thatdifferent sleep stages contribute to distinct aspects of cognitive and emotional processing. However, since the majority of these findings are based on single-night studies, it is difficult to determine whether such effects arise due to individual, between-subject differences in sleep patterns, or from within-subject variations in sleep over time. In the current study, weinvestigated the longitudinal relationship between sleep patterns and cognitive performance by monitoring both in parallel, daily, for a week. Using two cognitive tasks - one assessing emotional reactivity to facial expressions and the other evaluating learning abilities in a probabilistic categorization task - we found that between-subjectdifferences in the average time spent in particular sleep stages predicted performance in these tasks far more than within-subject daily variations. Specifically, the typical time individualsspent in Rapid-Eye Movement (REM) sleep and Slow-Wave Sleep (SWS) was correlated to their characteristic measures of emotional reactivity, whereas the typical time spent in SWS and non-REM stages 1 and 2 was correlated to their success in category learning. These effects were maintained even when sleep properties werebased onbaseline measures taken prior to the experimental week. In contrast, within-subject daily variations in sleep patterns only contributed to overnight difference in one particular measure of emotional reactivity. Thus, we conclude that the effects of natural sleep onemotional cognition and categorylearning are more trait-dependent than state-dependent, and suggest ways to reconcile these results with previous findings in the literature.