The aim of the present study was to investigate whether normative variability in self-reported sleep quality, indexed by PSQI global sleep quality scores, moderated associations between threat-related amygdala reactivity and measures of negative affect and perceived stress. Consistent with our hypothesis, bilateral amygdala reactivity positively covaried with measures of depressive symptoms and perceived psychological stress in participants reporting poor overall sleep. In contrast, there was an absence of association between amygdala reactivity and our outcome measures among better sleepers, suggesting that sleep quality serves as an important behavioral modulator of the neural correlates of mood, affect, and stress sensitivity. Moreover, these relationships were specific to amygdala reactivity and did not generalize to the task-elicited response of other brain regions (i.e., visual cortex).
The present findings extend prior laboratory studies demonstrating the consequence of sleep restriction on neural emotion processing (21
) and stress sensitivity (17
). Indeed after a night of total sleep deprivation, participants report increased negative mood and have heightened pupillary dilation in response to negative emotional stimuli compared with non–sleep-deprived controls (18
). Unlike prior laboratory research, this is the first study to show that natural variation in a global measure of sleep quality modulates similar brain-behavior relationships. As noted, a score above 5 on the PSQI is indicative of a poor sleeper (50
). Intriguingly, our analyses demonstrated that significant associations between amygdala reactivity and our measures of negative affect emerged at PSQI scores ranging from 4.7 to 6.4 and higher, suggesting that sleep quality may serve as a tipping point in linking neural threat responsiveness and corresponding affective experience.
Although our primary analyses revealed that the modulatory effects of sleep were independent of sex, sex-specific analyses found that the influence of sleep on associations between amygdala reactivity and affective measures emerged in men but not in women. Such a sex disparity is in line with an emerging set of neuroimaging studies on emotion processing (26
); however, explanations for these differences are lacking. Prior research posits sex differences in emotion regulation processes (58
), neural lateralization and temporal processing characteristics in emotional responsiveness (59
), and sex-specific subjective reporting as potential pathways. Our findings raise the possibility that sleep, a health behavior rarely measured in neuroimaging research, may also help elucidate sex differences in future work.
How sleep influences the impact of amygdala reactivity on self-reported negative affect and perceived stress remains unclear. Zohar and colleagues (60
) propose a cognitive-energy model wherein disruptive or challenging circumstances require effortful self-regulation, leaving less energy available for behavioral regulation of emotional experience. This notion is supported by neuroimaging data showing that compared with nondeprived sleepers, participants under sleep deprivation conditions show a loss of functional connectivity between the amygdala and the medial prefrontal cortex (mPFC), which is critical for the effective regulation of amygdala reactivity and the translation of this reactivity into adaptive behavioral responses (61
). Interestingly, our analyses revealed that in men who are better sleepers, there is an inverse association between amygdala reactivity and negative affect. This further suggests that poor sleep may, in fact, gate the expression of amygdala reactivity to threat as greater or lesser negative affect. A recent study reported that greater rapid eye movement sleep, which is higher in better sleepers, predicted decreased subjective emotional responsiveness to negative stimuli and a decrease in amygdala reactivity as well as an increase in amygdala-mPFC connectivity over consecutive scans (62
). These authors speculate that the impact of rapid eye movement sleep on neural and behavioral responsiveness to negative emotion reflects the down-regulation of noradrenergic signaling, which is one modulator of corticolimbic circuit function, during this sleep stage. It will be interesting to explore the relationship between normative sleep quality and such amygdala habituation and amygdala-mPFC connectivity in shaping the expression of negative affect in future studies.
In addition to these potential biological and psychological mechanisms, unmeasured behavioral and social pathways may also clarify these findings. For instance, poorer sleep efficiency has been related to lower levels of perceived social support (63
). Recent evidence suggests that perceived social support moderates the link between threat-related amygdala reactivity and trait anxiety (64
). In addition, poor sleep may likely cluster with other negative health behaviors (e.g., physical inactivity and poor diet) that may potentiate the amygdala–negative affect relationship.
Two unique characteristics of our observations deserve specific consideration. First, the moderating role of sleep quality was unique to the relationship between amygdala reactivity to fear and measures of negative affect and perceived stress and did not extend to amygdala reactivity to anger. This likely reflects the implicit nature of threat conveyed by fearful facial expressions, which triggers a broad increase in behavioral and physiological arousal to facilitate exploration of the local environment for the source of the threat (40
). Such general changes in broad measures of arousal and negative affect are characteristic of poor sleep (65
). In contrast, amygdala reactivity to anger results in a more focused and directed response to the immediate threat present (i.e., the person displaying the angry expression) and has been mapped onto variability in aggression and not more general negative affect (46
Second, the moderating role of sleep quality was specific to the relationship between amygdala reactivity to fear and measures of depressive but not anxiety symptoms. It is unclear why we did not observe an association between amygdala reactivity and anxiety symptoms because prior studies have generally reported positive correlations (41
). In this sample, sleep quality was more strongly related to measures of depressive symptoms than anxiety. This pattern may reflect the relative variability reported across measures of state negative affect in our sample. Participants reported a larger range of scores related to depressive compared with anxiety symptoms, yielding greater variance to be possibly explained in depressive symptoms by the interaction between amygdala reactivity and sleep quality. Many prior studies reporting positive correlations between amygdala reactivity and anxiety assessed variability in trait and not state anxiety, as was done with the current measures. Thus, it is possible that amygdala reactivity is more strongly linked with measures of trait anxiety but state depression. Additional work, ideally with multiple measures of state and trait negative affect, may help resolve this unexpected finding.
In summary, our study provides novel evidence that normative variability in self-reported sleep quality moderates the link between neural threat processes, negative affect, and perceived stress, particularly among men. Although the implications of this work remain to be elucidated, these findings contribute to a growing literature linking sleep disturbance with poor mental and physical health, particularly in response to stress. For instance, a recent laboratory study demonstrated that poor sleep potentiated blood pressure reactivity to a social evaluative stressor (20
), which complements research linking blood pressure reactivity to heightened stress-induced activation of corticolimbic circuitry including the amygdala (72
). Poor sleep also predicts later stress-related psychopathology, particularly depression (11
), which is associated with exaggerated amygdala reactivity (74
). Thus, further research investigating the links between sleep quality, threat-related amygdala reactivity, negative affect, and perceived stress promises to advance opportunities for intervention to prevent the progression and/or incidence of physical and mental health disability associated with poor sleep.