Sleepiness induced by sleep-debt enhanced amygdala activity for subliminal signals of fear

Abstract

BackgroundEmotional information is frequently processed below the level of consciousness, where subcortical regions of the brain are thought to play an important role. In the absence of conscious visual experience, patients with visual cortex damage discriminate the valence of emotional expression. Even in healthy individuals, a subliminal mechanism can be utilized to compensate for a functional decline in visual cognition of various causes such as strong sleepiness. In this study, sleep deprivation was simulated in healthy individuals to investigate functional alterations in the subliminal processing of emotional information caused by reduced conscious visual cognition and attention due to an increase in subjective sleepiness. Fourteen healthy adult men participated in a within-subject crossover study consisting of a 5-day session of sleep debt (SD, 4-h sleep) and a 5-day session of sleep control (SC, 8-h sleep). On the last day of each session, participants performed an emotional face-viewing task that included backward masking of nonconscious presentations during magnetic resonance scanning.ResultsFinally, data from eleven participants who were unaware of nonconscious face presentations were analyzed. In fear contrasts, subjective sleepiness was significantly positively correlated with activity in the amygdala, ventromedial prefrontal cortex, hippocampus, and insular cortex, and was significantly negatively correlated with the secondary and tertiary visual areas and the fusiform face area. In fear-neutral contrasts, subjective sleepiness was significantly positively correlated with activity of the bilateral amygdala. Further, changes in subjective sleepiness (the difference between the SC and SD sessions) were correlated with both changes in amygdala activity and functional connectivity between the amygdala and superior colliculus in response to subliminal fearful faces.ConclusionSleepiness induced functional decline in the brain areas involved in conscious visual cognition of facial expressions, but also enhanced subliminal emotional processing via superior colliculus as represented by activity in the amygdala. These findings suggest that an evolutionally old and auxiliary subliminal hazard perception system is activated as a compensatory mechanism when conscious visual cognition is impaired. In addition, enhancement of subliminal emotional processing might cause involuntary emotional instability during sleep debt through changes in emotional response to or emotional evaluation of external stimuli.

Personal sleep debt and daytime sleepiness mediate the relationship between sleep and mental health outcomes in young adults

“…Consistent with this view, we estimated less mediation for the quadratic effect of sleep duration on depression and anxiety risk in the university sample, suggesting the mediation effect in students is stronger for short sleep duration compared to long sleep. Sleep debt and daytime sleepiness can decrease certain behaviors (e.g., physical activity, leisure activities) (McAllister et al., ; McClain, Lewin, Laposky, Kahle, & Berrigan, ) and alter neurochemical (e.g., serotonin and norepinephrine) (Chellappa, Schroder, & Cajochen, ; Walker & van der Helm, ) and neuroanatomical processes (e.g., amygdala activity) (Motomura et al., , ) that accentuate negative emotions and increase psychopathology risk. Further research is needed to better understand the physiological and behavioral mechanisms underlying the interactions between sleep and mental health in different populations of young adults and other high‐risk groups (e.g., emergency personnel).…”

“…Consistent with this view, we estimated less mediation for the quadratic effect of sleep duration on depression and anxiety risk in the university sample, suggesting the mediation effect in students is stronger for short sleep duration compared to long sleep. Sleep debt and daytime sleepiness can decrease certain behaviors (e.g., physical activity, leisure activities) (McAllister et al, 2009;McClain, Lewin, Laposky, Kahle, & Berrigan, 2014) and alter neurochemical (e.g., serotonin and norepinephrine) (Chellappa, Schroder, & Cajochen, 2009;Walker & van der Helm, 2009) and neuroanatomical processes (e.g., amygdala activity) (Motomura et al, 2013(Motomura et al, , 2014 Table S5 and Table S6). Social activity can also influence chronotype (Leonhard & Randler, 2009), and growing research suggests that the contribution of social relative to biological (circadian and sleep) factors on eveningness may vary in different social contexts (Natale, Adan, & Fabbri, 2009;Randler, Faßl, & Kalb, 2017).…”

Sleep restriction caused impaired emotional regulation without detectable brain activation changes – a functional magnetic resonance imaging study

“…The main aim of the study was to investigate the effects of sleep restriction on emotion regulation. It has previously been proposed that sleep deprivation causes increased amygdala activation in response to negative stimuli (6,40) and that the mechanism behind this phenomenon is a prefrontal-amygdala disconnect (6,41,42). We found no effect of sleep restriction on amygdala activity nor connectivity to negative stimuli for passive viewing.…”

Effects of sleep on memory for conditioned fear and fear extinction.

“…A recent fMRI study has further shown that the sleep debt accrued by prolonged sleep restriction can produce a similar hyper-responsivity of the amygdala to emotional faces as well as reduce its functional connectivity with the vmPFC (ventral anterior cingulate) (Motomura et al, 2013). Additionally, these same investigators showed that sleep-debt induced amygdala hyperactivity also extends to subliminally presented (backward masked) emotional-face stimuli (Motomura et al, 2014). In addition to increased reactivity of neural structures to negative stimuli, TSD has also been shown to increase the reactivity of the mesolimbic reward system to positive stimuli as well as decrease its functional connectivity with regulatory prefrontal regions suggesting that the emotional regulatory function of sleep may be important in a bivalent manner (Gujar, Yoo, Hu, & Walker, 2011).…”