Research report
Lack of sleep affects the evaluation of emotional stimuli

https://doi.org/10.1016/j.brainresbull.2010.01.014Get rights and content

Abstract

Sleep deprivation (SD) negatively affects various cognitive performances, but surprisingly evidence about a specific impact of sleep loss on subjective evaluation of emotional stimuli remains sparse. In the present study, we assessed the effect of SD on the emotional rating of standardized visual stimuli selected from the International Affective Picture System.

Forty university students were assigned to the sleep group (n = 20), tested before and after one night of undisturbed sleep at home, or to the deprivation group, tested before and after one night of total SD. One-hundred and eighty pictures (90 test, 90 retest) were selected and categorized as pleasant, neutral and unpleasant. Participants were asked to judge their emotional reactions while viewing pictures by means of the Self-Assessment Manikin. Subjective mood ratings were also obtained by means of Visual Analog Scales.

No significant effect of SD was observed on the evaluation of pleasant and unpleasant stimuli. On the contrary, SD subjects perceived the neutral pictures more negatively and showed an increase of negative mood and a decrease of subjective alertness compared to non-deprived subjects. Finally, an analysis of covariance on mean valence ratings of neutral pictures using negative mood as covariate confirmed the effect of SD.

Our results indicate that sleep is involved in regulating emotional evaluation. The emotional labeling of neutral stimuli biased toward negative responses was not mediated by the increase of negative mood. This effect can be interpreted as an adaptive reaction supporting the “better safe than sorry” principle. It may also have applied implications for healthcare workers, military and law-enforcement personnel.

Introduction

The effects of sleep deprivation on neurocognitive processes are well documented [2]. Several studies have shown that the prefrontal cortex (PFC) is particularly sensitive to sleep loss [10], [25], [4] and that only one night of acute total sleep deprivation reduces performance on neuropsychological tasks such as those investigating working memory, decision making, task switching and attention [26], [19], [9], [7]. All these skills are subserved by the PFC. Moreover, neuroimaging studies have found that 24 h of continuous wakefulness are associated with significant reductions in metabolic activity within the prefrontal cortex, and, as a consequence, the PFC tasks performance is impaired (e.g., [25]).

The frontal lobes subserve not only the higher order cognitive abilities, but also emotion reactivity and behavioral inhibition (e.g., [18]). Amplified irritability and affective volatility are common complaints following sleepless nights [29], [24]. During prolonged sleep deprivation there is an increase in self-reported feelings of depressed mood, anger, frustration, tension and anxiety [6], [17]. In fact, a meta-analysis of consequences of sleep deprivation [23] showed that mood is more affected than performance measures following sleep deprivation.

While the effects of sleep loss on mood are well documented, on the other hand its specific impact on subjective reactivity to emotional stimuli has been surprisingly little studied. Without adequate sleep, negative reactions to adverse experiences appear to be significantly magnified, while positive reactions to pleasant events are often subdued. These effects on emotional reactivity can lead to negative consequences in real-word settings. As an example, it has been reported that sleep loss amplifies the negative emotive effects of disruptive daytime work events in medical residents [29].

Nevertheless, little is known about the specific effects of sleep loss on the subjective evaluation of emotional stimuli. It has been recently shown that sleep deprivation leads to a dysfunctionality of the MPFC–amygdala circuitry, accompanied by an increased negative evaluation of the emotional stimuli selected from the International Affective Picture System [28]. However, those pictures ranged from emotionally neutral to increasingly aversive (i.e., the pleasant pictures were discarded). Moreover, a dichotomic (unpleasant/neutral) emotionality rating was requested, instead of the typical valence rating on a continuous 1–9 scale [5].

In the present study we assessed the impact of one night of sleep deprivation on the emotional rating of a battery of affective visual stimuli selected from the International Affective Picture System (IAPS) [20], a set of static images based on a dimensional model of emotion. We hypothesized that, whether sleep deprivation causes an imbalance of the prefrontal–limbic circuitry, sleep-deprived and well-rested subjects should diverge in their evaluations of the affective stimuli. Given that judgments of emotional stimuli are not carried out in a dichotomous way, but continuously along the two dimensions of valence and arousal [5], we asked subjects to rate the pictures in terms of their ability to induce valence (unpleasant/pleasant) and arousal (calm/excited) changes.

Section snippets

Participants

Forty university students participated in this study (all females; mean age ± S.D.: 24.2 ± 4.2 years; range: 20–36 years).

None of the subjects had a history of medical, neurological or psychiatric disorders, neither of medication or drug intake. Moreover, each participant filled out the Toronto Alexithymia Scale (TAS-20) [1], to exclude alexithymic subjects (TAS-20 scores ≥61) and the Center for Epidemiological Studies Depression rating Scale (CES-D) [12] to exclude subjects with depression (CES-D

Subjective mood and alertness measures

ANOVA on Negative Mood Index (NMI) scores showed a significant main effect for Session (F1,38 = 5.73; p < 0.05), while the effect of Group only approached to significance (F1,38 = 3.41; p = 0.07). However, the Group × Session interaction was significant (F1,38 = 7.75; p < 0.01). Post hoc comparisons indicated that after one night of sleep deprivation subjects report a more negative mood than the non-deprived subjects (p < 0.01), while mood remains unchanged after a sleep night (see Fig. 1 panel A).

ANOVA on

Discussion

The purpose of this study was to investigate the effects of one night of sleep deprivation on the emotional valence and arousal subjective ratings of pleasant, neutral and unpleasant pictures in healthy humans. Different patterns of changes were observed for ratings of valence and arousal, in keeping with the view that these two dimensions reflect different aspects of emotional appraisal. Moreover, the analyses showed that valence rating was highest for unpleasant, intermediate for neutral and

Conflict of interest

The authors declare that they have no competing financial interests.

Acknowledgments

This study was supported in part by a MiUR grant to M. Ferrara (PRIN: n. 2007BNRWLP-003), and by a grant from the University of L’Aquila (Ricerche di Ateneo ex 60%).

References (29)

  • M.W. Chee et al.

    Functional neuroimaging and behavioral correlates of capacity decline in visual short-term memory following sleep deprivation

    Proc. Natl. Acad. Sci. U.S.A.

    (2007)
  • A. Couyoumdjian et al.

    The effects of sleep and sleep deprivation on task switching performance

    J. Sleep Res.

    (2009)
  • S.P. Drummond et al.

    Sleep deprivation-induced reduction in cortical functional response to serial subtraction

    Neuroreport

    (1999)
  • J.S. Durmer et al.

    Neurocognitive consequences of sleep deprivation

    Semin. Neurol.

    (2005)
  • Cited by (162)

    • An experimental test of the effects of acute sleep deprivation on affect and avoidance

      2022, Journal of Behavior Therapy and Experimental Psychiatry
    • Sleep and affect: A conceptual review

      2022, Sleep Medicine Reviews
      Citation Excerpt :

      For short-term behavioral/physiological measures of duration, we found a possible null association with self-reported negative valence [49,70,76†,77†,79–82†,86†,89–92] (46% of studies involved sleep deprivation) but a negative association with behavioral/physiological measures of negative valence [49,76†,77†,90] (50% of studies involved sleep deprivation). Likewise, different findings depending on methods also emerged for arousal, where we found a possible null association with self-reported arousal [49,76†,80†,83,90,93] (33% of studies involved sleep deprivation) but a negative association with behavioral/physiological measures of arousal [76†,90,92,93] (25% of studies involved sleep deprivation). Sensitivity analyses for results pertaining to behavioral/physiological signals of sleep duration revealed that excluding studies involving partial or total sleep deprivation only changed the conclusions for the association between short-term duration and short-term behavioral/physiological signals of negative valence; specifically, after excluding sleep studies involving manipulation of sleep duration, there were not enough remaining studies to draw conclusions.

    View all citing articles on Scopus
    View full text