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. 2010 Oct;33(10):1305-13.
doi: 10.1093/sleep/33.10.1305.

Sleep deprivation and interference by emotional distracters

Affiliations

Sleep deprivation and interference by emotional distracters

Lisa Y M Chuah et al. Sleep. 2010 Oct.

Abstract

Study objectives: We determined if sleep deprivation would amplify the effect of negative emotional distracters on working memory.

Design: A crossover design involving 2 functional neuroimaging scans conducted at least one week apart. One scan followed a normal night of sleep and the other followed 24 h of sleep deprivation. Scanning order was counterbalanced across subjects.

Setting: The study took place in a research laboratory.

Participants: 24 young, healthy volunteers with no history of any sleep, psychiatric, or neurologic disorders.

Interventions: N/A.

Measurements and results: Study participants were scanned while performing a delayed-response working memory task. Two distracters were presented during the maintenance phase, and these differed in content: highly arousing, negative emotional scenes; low-arousing, neutral scenes; and digitally scrambled versions of the pictures. Irrespective of whether volunteers were sleep deprived, negative emotional (relative to neutral) distracters elicited greater maintenance-related activity in the amygdala, ventrolateral prefrontal cortex, and fusiform gyri, while concurrently depressing activity in cognitive control regions. Individuals who maintained or increased distracter-related amygdala activation after sleep deprivation showed increased working memory disruptions by negative emotional distracters. These individuals also showed reduced functional connectivity between the amygdala and the ventromedial and dorsolateral prefrontal cortices, regions postulated to mediate cognitive control against emotional distraction.

Conclusions: Increased distraction by emotional stimuli following sleep deprivation is accompanied by increases in amygdala activation and reduced functional connectivity between the amygdala and prefrontal cognitive control regions. These findings shed light on the neural basis for interindividual variation in how negative emotional stimuli might distract sleep deprived persons.

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Figures

Figure 1
Figure 1
A schematic of the working memory task. Participants were instructed to view and remember the faces, view the distracters and to indicate if the probe face had been presented earlier. Distracters could be negative, neutral, or scrambled pictures.
Figure 2
Figure 2
Sleep deprivation impaired working memory. Corrected recognition was significantly lowered with emotional distracters and showed a trend for decline with neutral and scrambled pictures. Error bars indicate ± 1 SE. (RW: rested wakefulness; SD: sleep deprivation).
Figure 3
Figure 3
Dissociable effects of emotional distraction in dorsal and ventral neural systems at rested wakefulness (RW). There were dissociable patterns of activity during the maintenance phase in (A) lateral parietal cortex (LPC), (b) dorsolateral prefrontal cortex (dlPFC), (C) lateral occipital complex (LOC) and (D) ventrolateral PFC (vlPFC). Emotional distracters resulted in elevated activity in vlPFC and LOC while simultaneously reducing activity in the dlPFC and LPC to below prestimulus baseline levels. Error bars indicate ± 1 SE. (Scr: Scrambled; Neu: Neutral; Emo: Emotional).
Figure 4
Figure 4
Increased amygdala activity was associated with greater emotional distractibility following sleep deprivation (SD). Right amygdala activity (averaging the signal at time points 12, 14 and 16 s post trial onset) was elevated in response to emotional distracters relative to neutral distracters at rested wakefulness (RW). A State (rested wakefulness, sleep deprivation) by Condition (Neutral, Emotional) repeated-measures ANOVA conducted on averaged activation within this region of interest indicated decreases in amygdala activation following sleep deprivation, F1,23 = 5.44, P = 0.03, but this did not vary with condition, F1,23 = 0.17, P = 0.69. Critically, state-related change in amygdala activation correlated with the corresponding alteration of emotional distractibility (P = 0.01), while no parallel effect was present for neutral distracters. A similar effect was present for the left amygdala (Supplementary Figure 2). Error bars indicate ± 1 SE. (Neu: Neutral; Emo: Emotional).
Figure 5
Figure 5
Reduction in functional connectivity between the amygdala and brain regions known to mediate cognitive control, namely the dorsolateral prefrontal cortex (dlPFC) and ventromedial prefrontal cortex (vmPFC), was associated with greater distractibility by negative emotional stimuli during sleep deprivation. These correlations were computed following the removal of an influential outlier which inflated the correlations (N = 23). The region within the dorsolateral prefrontal cortex which showed a significant (P < 0.001, corrected) Condition by Time-on-trial interaction (Figure 3; Table 1) is shaded in blue. (RW: rested wakefulness; SD: sleep deprivation).

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