Total sleep deprivation reduces top-down regulation of emotion without altering bottom-up affective processing.
ABSTRACT: Sleep loss is reported to influence affective processing, causing changes in overall mood and altering emotion regulation. These aspects of affective processing are seldom investigated together, making it difficult to determine whether total sleep deprivation has a global effect on how affective stimuli and emotions are processed, or whether specific components of affective processing are affected selectively. Sixty healthy adults were recruited for an in-laboratory study and, after a monitored night of sleep and laboratory acclimation, randomly assigned to either a total sleep deprivation condition (n = 40) or a rested control condition (n = 20). Measurements of mood, vigilant attention to affective stimuli, affective working memory, affective categorization, and emotion regulation were taken for both groups. With one exception, measures of interest were administered twice: once at baseline and again 24 hours later, after the sleep deprived group had spent a night awake (working memory was assessed only after total sleep deprivation). Sleep deprived individuals experienced an overall reduction in positive affect with no significant change in negative affect. Despite the substantial decline in positive affect, there was no evidence that processing affectively valenced information was biased under total sleep deprivation. Sleep deprived subjects did not rate affective stimuli differently from rested subjects, nor did they show sleep deprivation-specific effects of affect type on vigilant attention, working memory, and categorization tasks. However, sleep deprived subjects showed less effective regulation of negative emotion. Overall, we found no evidence that total sleep deprivation biased the processing of affective stimuli in general. By contrast, total sleep deprivation appeared to reduce controlled processing required for emotion regulation.
Project description:Appropriate interpretation of pleasurable, rewarding experiences favors decisions that enhance survival. Conversely, dysfunctional affective brain processing can lead to life-threatening risk behaviors (e.g., addiction) and emotion imbalance (e.g., mood disorders). The state of sleep deprivation continues to be associated with maladaptive emotional regulation, leading to exaggerated neural and behavioral reactivity to negative, aversive experiences. However, such detrimental consequences are paradoxically aligned with the perplexing antidepressant benefit of sleep deprivation, elevating mood in a proportion of patients with major depression. Nevertheless, it remains unknown how sleep loss alters the dynamics of brain and behavioral reactivity to rewarding, positive emotional experiences. Using functional magnetic resonance imaging (fMRI), here we demonstrate that sleep deprivation amplifies reactivity throughout human mesolimbic reward brain networks in response to pleasure-evoking stimuli. In addition, this amplified reactivity was associated with enhanced connectivity in early primary visual processing pathways and extended limbic regions, yet with a reduction in coupling with medial frontal and orbitofrontal regions. These neural changes were accompanied by a biased increase in the number of emotional stimuli judged as pleasant in the sleep-deprived group, the extent of which exclusively correlated with activity in mesolimbic regions. Together, these data support a view that sleep deprivation not only is associated with enhanced reactivity toward negative stimuli, but imposes a bidirectional nature of affective imbalance, associated with amplified reward-relevant reactivity toward pleasure-evoking stimuli also. Such findings may offer a neural foundation on which to consider interactions between sleep loss and emotional reactivity in a variety of clinical mood disorders.
Project description:<h4>Study objectives</h4>To better understand the sometimes catastrophic effects of sleep loss on naturalistic decision making, we investigated effects of sleep deprivation on decision making in a reversal learning paradigm requiring acquisition and updating of information based on outcome feedback.<h4>Design</h4>Subjects were randomized to a sleep deprivation or control condition, with performance testing at baseline, after 2 nights of total sleep deprivation (or rested control), and following 2 nights of recovery sleep. Subjects performed a decision task involving initial learning of go and no go response sets followed by unannounced reversal of contingencies, requiring use of outcome feedback for decisions. A working memory scanning task and psychomotor vigilance test were also administered.<h4>Setting</h4>Six consecutive days and nights in a controlled laboratory environment with continuous behavioral monitoring.<h4>Subjects</h4>Twenty-six subjects (22-40 y of age; 10 women).<h4>Interventions</h4>Thirteen subjects were randomized to a 62-h total sleep deprivation condition; the others were controls.<h4>Measurements and results</h4>Unlike controls, sleep deprived subjects had difficulty with initial learning of go and no go stimuli sets and had profound impairment adapting to reversal. Skin conductance responses to outcome feedback were diminished, indicating blunted affective reactions to feedback accompanying sleep deprivation. Working memory scanning performance was not significantly affected by sleep deprivation. And although sleep deprived subjects showed expected attentional lapses, these could not account for impairments in reversal learning decision making.<h4>Conclusions</h4>Sleep deprivation is particularly problematic for decision making involving uncertainty and unexpected change. Blunted reactions to feedback while sleep deprived underlie failures to adapt to uncertainty and changing contingencies. Thus, an error may register, but with diminished effect because of reduced affective valence of the feedback or because the feedback is not cognitively bound with the choice. This has important implications for understanding and managing sleep loss-induced cognitive impairment in emergency response, disaster management, military operations, and other dynamic real-world settings with uncertain outcomes and imperfect information.
Project description:The emotional dysregulation and impaired working memory found after sleep loss can have severe implications for our daily functioning. Considering the intertwined relationship between emotion and cognition in stimuli processing, there could be further implications of sleep deprivation in high-complex emotional situations. Although studied separately, this interaction between emotion and cognitive processes has been neglected in sleep research. The aim of the present study was to investigate the effect of 1?night of sleep deprivation on emotional working memory. Sixty-one healthy participants (mean age: 23.4?years) were either sleep deprived for 1?night (n?=?30) or had a normal night's sleep (n?=?31). They performed an N-back task with two levels of working memory load (1-back and 3-back) using positive, neutral and negative picture scenes. Sleep deprivation, compared with full night sleep, impaired emotional working memory accuracy, but not reaction times. The sleep-deprived participants, but not the controls, responded faster to positive than to negative and neutral pictures. The effect of sleep deprivation was similar for both high and low working memory loads. The results showed that although detrimental in terms of accuracy, sleep deprivation did not impair working memory speed. In fact, our findings indicate that positive stimuli may facilitate working memory processing speed after sleep deprivation.
Project description:<h4>Study objectives</h4>Total sleep deprivation is known to have significant detrimental effects on cognitive and socio-emotional functioning. Nonetheless, the mechanisms by which total sleep loss disturbs decision-making in social contexts are poorly understood. Here, we investigated the impact of total sleep deprivation on approach/avoidance decisions when faced with threatening individuals, as well as the potential moderating role of sleep-related mood changes.<h4>Methods</h4>Participants (n = 34) made spontaneous approach/avoidance decisions in the presence of task-irrelevant angry or fearful individuals, while rested or totally sleep deprived (27 h of continuous wakefulness). Sleep-related changes in mood and sustained attention were assessed using the Positive and Negative Affective Scale and the psychomotor vigilance task, respectively.<h4>Results</h4>Rested participants avoided both fearful and angry individuals, with stronger avoidance for angry individuals, in line with previous results. On the contrary, totally sleep deprived participants favored neither approach nor avoidance of fearful individuals, while they still comparably avoided angry individuals. Drift-diffusion models showed that this effect was accounted for by the fact that total sleep deprivation reduced value-based evidence accumulation toward avoidance during decision making. Finally, the reduction of positive mood after total sleep deprivation positively correlated with the reduction of fearful display avoidance. Importantly, this correlation was not mediated by a sleep-related reduction in sustained attention.<h4>Conclusions</h4>All together, these findings support the underestimated role of positive mood-state alterations caused by total sleep loss on approach/avoidance decisions when facing ambiguous socio-emotional displays, such as fear.
Project description:Unwanted memories often enter conscious awareness when individuals confront reminders. People vary widely in their talents at suppressing such memory intrusions; however, the factors that govern suppression ability are poorly understood. We tested the hypothesis that successful memory control requires sleep. Following overnight sleep or total sleep deprivation, participants attempted to suppress intrusions of emotionally negative and neutral scenes when confronted with reminders. The sleep-deprived group experienced significantly more intrusions (unsuccessful suppressions) than the sleep group. Deficient control over intrusive thoughts had consequences: Whereas in rested participants suppression reduced behavioral and psychophysiological indices of negative affect for aversive memories, it had no such salutary effect for sleep-deprived participants. Our findings raise the possibility that sleep deprivation disrupts prefrontal control over medial temporal lobe structures that support memory and emotion. These data point to an important role of sleep disturbance in maintaining and exacerbating psychiatric conditions characterized by persistent, unwanted thoughts.
Project description:<h4>Study objectives</h4>Eyelid closures in fatigued individuals signify task disengagement in attention-demanding visual tasks. Here, we studied how varying degrees of eyelid closure predict responses to auditory stimuli depending on whether a participant is well rested or sleep deprived. We also examined time-on-task effects and how more and less vulnerable individuals differed in frequency of eye closures and lapses.<h4>Design</h4>Six repetitions of an auditory vigilance task were performed in each of two sessions: rested wakefulness (RW) and total sleep deprivation (TSD) (order counterbalanced).<h4>Setting</h4>Sleep laboratory.<h4>Participants</h4>Nineteen healthy young adults (mean age: 22 ± 2.8 y; 11 males).<h4>Intervention</h4>Approximately 24 h of TSD.<h4>Measurements and results</h4>Eyelid closure was rated on a 9-point scale (1 = fully closed to 9 = fully opened) using video segments time-locked to the auditory event. Eyes-open trials predominated during RW, but different degrees of eye closure were uniformly distributed during TSD. The frequency of lapses (response time > 800 ms or nonresponses) to auditory stimuli increased dramatically with greater degrees of eye closure, but the association was strong only during TSD. There were significant within-run time-on-task effects on eye closure and auditory lapses that were exacerbated by TSD. Participants who had more auditory lapses during TSD (more vulnerable) had greater variability in their eyelid closures.<h4>Conclusions</h4>Eyelid closures are a strong predictor of auditory task disengagement in the sleep-deprived state but are less relevant during rested wakefulness. Individuals relatively more impaired in this auditory vigilance task during total sleep deprivation display oculomotor evidence for greater state instability.
Project description:A night without sleep is followed by enhanced sleepiness, increased low-frequency activity in the waking EEG, and reduced vigilant attention. The magnitude of these changes is highly variable among healthy individuals. Findings in young men of low and high subjective caffeine sensitivity suggest that adenosinergic mechanisms contribute to inter-individual differences in sleep deprivation-induced changes in EEG theta activity, as well as optimal performance on the psychomotor vigilance task (PVT). In comparison to young subjects, healthy adults of older age typically feel less sleepy after sleep deprivation, and show fewer response lapses, and faster reaction times on the PVT, especially in the morning after the night without sleep. We hypothesized that age-related changes in adenosine signal transmission underlie reduced vulnerability to sleep deprivation in older individuals. To test this hypothesis, the combined effects of prolonged wakefulness and the adenosine receptor antagonist, caffeine, on an antero-posterior power gradient in EEG theta activity and PVT performance were analyzed in healthy older and caffeine-insensitive and -sensitive young men. The results show that age-related differences in sleep loss-induced changes in brain rhythmic activity and neurobehavioral functions are mirrored in young individuals of low and high sensitivity to the stimulant effects of caffeine. Moreover, the effects of sleep deprivation and caffeine on regional theta power and vigilant attention are inversely correlated across older and young age groups. Genetic variants of the adenosine A(2A) receptor gene contribute to individual differences in neurobehavioral performance in rested and sleep deprived state, and modulate the actions of caffeine in wakefulness and sleep. Based upon this evidence, we propose that age-related differences in A(2A) receptor-mediated signal transduction could be involved in age-related changes in the vulnerability to acute sleep deprivation.
Project description:Judgements and decisions in many political, economic or medical contexts are often made while sleep deprived. Furthermore, in such contexts individuals are required to integrate information provided by - more or less qualified - advisors. We asked if sleep deprivation affects advice taking. We conducted a 2 (sleep deprivation: yes vs. no) ×2 (competency of advisor: medium vs. high) experimental study to examine the effects of sleep deprivation on advice taking in an estimation task. We compared participants with one night of total sleep deprivation to participants with a night of regular sleep. Competency of advisor was manipulated within subjects. We found that sleep deprived participants show increased advice taking. An interaction of condition and competency of advisor and further post-hoc analyses revealed that this effect was more pronounced for the medium competency advisor compared to the high competency advisor. Furthermore, sleep deprived participants benefited more from an advisor of high competency in terms of stronger improvement in judgmental accuracy than well-rested participants.
Project description:Prolonged wakefulness impairs sustained vigilant attention, measured with the psychomotor vigilance task (PVT), and induces a compensatory increase in sleep intensity in recovery sleep, quantified by slow-wave activity (SWA) in the sleep electroencephalogram (EEG). These effects of sleep deprivation are counteracted by the adenosine receptor antagonist caffeine, implying involvement of the adenosine neuromodulator/receptor system. To examine a role for adenosine A(2A) receptors, we investigated whether variation of the A(2A) receptor gene (ADORA2A) modified effects of caffeine on PVT and SWA after sleep deprivation.A haplotype analysis of eight single-nucleotide polymorphisms of ADORA2A was performed in 82 volunteers. In 45 young men carrying five different allele combinations, we investigated the effects of prolonged waking and 2 × 200 mg caffeine or 2 × 100 mg modafinil on psychomotor vigilance, sleepiness, and the waking and sleep EEG.Throughout extended wakefulness, the carriers of haplotype HT4 performed faster on the PVT than carriers of non-HT4 haplotype alleles. In haplotype HT4, caffeine failed to counteract the waking-induced impairment of PVT performance and the rebound of SWA in recovery sleep. However, caffeine was effective in non-HT4 allele carriers, and modafinil reduced the consequences of prolonged waking, independently of ADORA2A haplotype.Common genetic variation of ADORA2A is an important determinant of psychomotor vigilance in rested and sleep-deprived state. It also modulates individual responses to caffeine after sleep deprivation. These findings demonstrate a role for adenosine A(2A) receptors in the effects of prolonged wakefulness on vigilant attention and the sleep EEG.
Project description:There is growing evidence that sleep plays a pivotal role on health, cognition and emotional regulation. However, the interplay between sleep and social cognition remains an uncharted research area. In particular, little is known about the impact of sleep deprivation on sarcasm detection, an ability which, once altered, may hamper everyday social interactions. The aim of this study is to determine whether sleep-deprived participants are as able as sleep-rested participants to adopt another perspective in gauging sarcastic statements. At 9am, after a whole night of sleep (n = 15) or a sleep deprivation night (n = 15), participants had to read the description of an event happening to a group of friends. An ambiguous voicemail message left by one of the friends on another's phone was then presented, and participants had to decide whether the recipient would perceive the message as sincere or as sarcastic. Messages were uttered with a neutral intonation and were either: (1) sarcastic from both the participant's and the addressee's perspectives (i.e. both had access to the relevant background knowledge to gauge the message as sarcastic), (2) sarcastic from the participant's but not from the addressee's perspective (i.e. the addressee lacked context knowledge to detect sarcasm) or (3) sincere. A fourth category consisted in messages sarcastic from both the participant's and from the addressee's perspective, uttered with a sarcastic tone. Although sleep-deprived participants were as accurate as sleep-rested participants in interpreting the voice message, they were also slower. Blunted reaction time was not fully explained by generalized cognitive slowing after sleep deprivation; rather, it could reflect a compensatory mechanism supporting normative accuracy level in sarcasm understanding. Introducing prosodic cues compensated for increased processing difficulties in sarcasm detection after sleep deprivation. Our findings support the hypothesis that sleep deprivation might damage the flow of social interactions by slowing perspective-taking processes.