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In economic decision-making individuals choose between items on the basis of their perceived value. For both humans and nonhuman primates, these decisions are often carried out while shifting gaze between the available options. Recent studies in humans suggest that these shifts in gaze actively influence choice, manifesting as a bias in favor of the items that are viewed first, viewed last, or viewed for the overall longest duration in a given trial. This suggests the existence of a mechanism that links gaze behavior to the neural computations underlying value-based choices. In order to identify this mechanism, it is first necessary to develop and validate a suitable animal model of this behavior. To this end, we have created a novel value-based choice task for macaque monkeys that captures the essential features of the human paradigms in which gaze biases have been observed. Using this task, we identified gaze biases in the monkeys that were both qualitatively and quantitatively similar to those in humans. In addition, the monkeys’ gaze biases were well-explained using a sequential sampling model framework previously used to describe gaze biases in humans—the first time this framework has been used to explore value-based choice mechanisms in nonhuman primates. Together, these findings suggest a common mechanism that can explain gaze-related choice biases across species, and open the way for mechanistic studies to identify the neural origins of this behavior.

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.