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The role of sleep deprivation in aggressive behavior has not been systematically investigated, despite a great deal of evidence to suggest a relationship. We investigated the impact of 33 h of sleep loss on endocrine function and reactive aggression using the Point Subtraction Aggression Paradigm (PSAP) task. PSAP performance was assessed in 24 young men and 25 women who were randomly assigned to a sleep deprivation or control condition. Sleep deprivation lowered reactive aggression and testosterone (but not cortisol) in men, and disrupted the positive relationship between a pre-post PSAP increase in testosterone and aggression that was evident in rested control men. While women increased aggression following provocation as expected, no influence of sleep deprivation was found. This is the first experimental study to demonstrate that sleep deprivation lowers reactive aggression in men. Testosterone, but not cortisol, played a role in the relationship between sleep and reactive aggression in men.

Human sleep deprivation leads to decreased arousal, reduced visual and motor acuity, and cognitive deficits including slower and more variable response time, impaired memory and attention (Bonnet, 2011). Imaging and behavioral data illustrate that sleep loss impairs pre-frontal cortex (PFC) function in particular (Drummond and Brown, 2001 and Harrison and Horne, 2000). Since the earliest report of human sleep deprivation (Patrick and Gilbert, 1896), one of the most reliable findings has been changes to mood. In support of this, a meta-analysis reported that the negative effects on mood were greater than those on cognitive functioning (Pilcher and Huffcutt, 1996). Despite this robust finding of changes to subjective mood following sleep loss, researchers have only recently begun to investigate the impact of sleep loss on objective measures of emotion regulation and processing such as reactivity to stimuli. Behavioral response data to emotional stimuli as a result of sleep deprivation are mixed; compared to rested controls, researchers have reported that sleep deprivation leads to lower accuracy for happy and angry faces (Van der Helm et al., 2010), and less facial expressiveness to both positive and negative emotional video clips (Minkel et al., 2011), yet increased hit rate and response time to negative stimuli in a go-no-go task using emotional words (Anderson and Platten, 2011), and a tendency to rate neutral pictures as more negative (Tempesta et al., 2010). Franzen et al. (2009) showed that sleep deprived participants had greater autonomic reactivity in pupil diameter compared to controls to blocks of negative emotional stimuli, but not positive or neutral stimuli from the International Affective Picture Set (IAPS). Using fMRI, Yoo et al. (2007) examined brain activation to emotionally neutral and negative pictures from the IAPS. Sleep deprived participants showed greater amygdala activation to negative pictures, and less connectivity between the amygdala and the medial prefrontal cortex (mPFC), compared to controls. Subsequently, Gujar et al. (2011) demonstrated that sleep deprived participants showed greater activation in brain regions involved in reward and less connectivity to frontal brain regions compared to rested controls when presented with emotionally positive pictures from the IAPS; these data show that sleep deprivation leads to an affective imbalance, where there is greater reactivity to pleasure evoking or rewarding stimuli as well as emotionally negative or threatening stimuli. Together, these data indicate that sleep deprived participants are highly reactive to emotional stimuli; thus, they may also be more prone to reactive aggression. In a recent review, Kamphuis et al. (2012) demonstrated that there is a great deal of anecdotal evidence for a relationship between sleep deprivation and aggression in particular, yet few systematic studies. In children, better sleep quality was associated with better control over aggressive behaviors (Meijer et al., 2000); poor sleep has been associated with more conduct problems in a number of studies (Kamphuis et al., 2012). Other correlative evidence exists including associations between sleep duration or quality and negative mood in adults, and the presence of sleep disruption in various groups who often display aggression (e.g., people with psychiatric and personality disorders) (Kamphuis et al., 2012). There is some experimental evidence to support the association between sleep and aggression. Early animal research showed that sleep deprived, especially REM deprived, rats engaged in more aggressive behavior (e.g., Hicks et al., 1978), although the possibility that factors other than sleep were at play prohibits drawing causal inferences (Kamphuis et al., 2012). One experimental study has shown an impact of sleep loss on aggressive behavior in humans. Using a projective type of test, Kahn-Greene et al. (2006) examined the impact of 55 h of wakefulness on subjective responses to cartoons depicting a frustrating situation. Sleep deprived individuals were more likely to provide aggressive responses and were also more likely to blame others when presented with frustrating scenarios. The authors suggested that sleep deprivation alters the ability to inhibit aggressive behavior due to decreased PFC function. Another experimental study by Vohs et al. (2011) examined the effects of 24 h sleep deprivation and self-regulation on aggressive responding using a computer game where the level of volume chosen to blast one's opponent following a win was considered an index of retaliatory aggression. The authors found no effect of sleep deprivation using this measure of aggression. In the current study, we investigated the effects of sleep deprivation on aggressive behavior using the Point Subtraction Aggression Paradigm (PSAP), a well-validated laboratory measure of reactive aggression (Cherek, 1981, Cherek et al., 1996, Zhou et al., 2006, Kivisto et al., 2009 and New et al., 2009). Although there is evidence for a relationship between baseline testosterone and measures of behavioral aggression (reviewed in Archer, 2006), including increased aggression on the PSAP after administration of testosterone (Pope et al., 2000), there may be stronger relationships between dynamic endocrine function and aggression (Carré et al., 2009 and Geniole et al., 2011). Specifically, we have found that changes from baseline in salivary testosterone and salivary cortisol are positively correlated with increased aggression on the PSAP (e.g., Carré and McCormick, 2008 and Geniole et al., 2011). These relationships, however, depended on situational factors (e.g., win/loss, Carré et al., 2009; social exclusion, Geniole et al., 2011), and may therefore be influenced by sleep deprivation. Very few systematic investigations have been carried out to examine the impact of sleep deprivation on aggression in humans despite a great deal of evidence to suggest a relationship exists. Moreover, the mechanisms underlying this relationship have not been investigated; Kamphuis et al. (2012) suggest PFC and hypothalamic–pituitary–adrenal (HPA) axis function as potential mechanisms of the role of sleep loss in increased aggression. It is important to understand the role of sleep in emotion regulation and aggressive behavior in particular, given our society is increasingly sleep deprived and because many psychiatric disorders are co-morbid with sleep disturbances (Walker, 2009). In the present study, we investigated the impact of 33-h of total sleep deprivation on reactive aggression using the PSAP task and the role of hormones. Because sleep deprivation impairs PFC function (Drummond and Brown, 2001 and Harrison and Horne, 2000), and based on the literature showing sleep loss leads to mood changes (Pilcher and Huffcutt, 1996), increased emotional reactivity (Yoo et al., 2007, Franzen et al., 2009 and Gujar et al., 2011), and increased aggressive responding and blame to frustrating scenarios (Kahn-Greene et al., 2006), we hypothesized that sleep deprivation would increase aggressive behavior upon provocation in the PSAP task. We also sought to investigate how sleep deprivation altered the endocrine-aggression relationship. There is evidence that sleep deprivation alters endocrine function (e.g., increased cortisol, Redwine et al., 2000 and Spiegel et al., 1999, and decreased testosterone, Anderson and Platten, 2011, Leproult and Van Cauter, 2011 and Wu et al., 2011), which may in turn influence endocrine reactivity and relationships with aggressive behavior; thus, we collected morning and evening saliva samples before and after sleep deprivation, and before and after the PSAP task. Given the fundamental sex differences in hormonal factors, we carried out analyses separately in men and women. We expected sleep deprivation would increase aggressive behavior in both men and women, and be related to baseline levels of and task-related changes in testosterone and estradiol respectively. Lastly, cortisol was measured to investigate the role of stress in the relationship between sleepiness and aggressive behavior.

Sleep efficiency (the percent time spent asleep of time in bed) was high for the control group on both the baseline (M = 93.07%, SD = 5.12) and experimental nights (M = 94.96%, SD = 2.51), and for the sleep deprivation group on the baseline night (M = 93.40%, SD = 4.20); groups did not differ on sleep efficiency on the baseline night. Compared to the control group, sleep deprived participants reported greater subjective sleepiness, and less positive mood and more negative mood on the PANAS at various times throughout the experimental day (see Table 1).