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. 2021 Sep 2;16(9):e0256983.
doi: 10.1371/journal.pone.0256983. eCollection 2021.

Total sleep deprivation reduces top-down regulation of emotion without altering bottom-up affective processing

Anthony R Stenson  1 , Courtney A Kurinec  1 , John M Hinson  1   2 , Paul Whitney  1   2 , Hans P A Van Dongen  2   3
Affiliations

Total sleep deprivation reduces top-down regulation of emotion without altering bottom-up affective processing

Anthony R Stenson et al. PLoS One. .

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.

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Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Study design for the total sleep deprivation condition (top) and well-rested control condition (bottom).
Open symbols represent task administrations not used in analysis.
Fig 2
Fig 2
Positive affect (PA) and negative affect (NA) ratings on the PANAS (mean ± SE) for subjects in the TSD (red) and WR (blue) conditions. Grey bar represents sleep opportunity for WR condition and time awake for TSD condition.
Fig 3
Fig 3
Number of lapses (mean ± SE) on the affective PVT for each category of valenced word stimuli for the TSD (red) and WR (blue) conditions. Grey bar represents sleep opportunity for WR condition and time awake for TSD condition.
Fig 4
Fig 4. Accuracy (mean ± SE) on the 1- and 2-back blocks of the N-back task, for both positive and negative stimuli, in the TSD (red) and WR (blue) conditions (left).
Response time for accurate trials (mean ± SE) on the 1- and 2-back blocks of the N-back task, for both positive and negative stimuli, in the TSD and WR conditions (right).
Fig 5
Fig 5
Valence ratings (mean ± SE) on the affective categorization task for each stimulus type, in the WR and TSD conditions (left). Response times (mean ± SE) on the affective categorization task for each stimulus type, in the WR and TSD conditions (right).
Fig 6
Fig 6. Negativity ratings (mean ± SE) during attend/negative trials (left) and decrease/negative trials (right) of the emotion regulation task, in the TSD (red) and WR (blue) conditions.
Fig 7
Fig 7. Subjective sleepiness ratings (mean ± SE) on the KSS for the TSD (red) and WR (blue) conditions.
Grey bar represents sleep opportunity for WR condition and time awake for TSD condition.
See this image and copyright information in PMC

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