Sleep Deprivation Impairs the Accurate Recognition of Human Emotions

Study Objectives:

Investigate the impact of sleep deprivation on the ability to recognize the intensity of human facial emotions.

Design:

Randomized total sleep-deprivation or sleep-rested conditions, involving between-group and within-group repeated measures analysis.

Setting:

Experimental laboratory study.

Participants:

Thirty-seven healthy participants, (21 females) aged 18–25 y, were randomly assigned to the sleep control (SC: n = 17) or total sleep deprivation group (TSD: n = 20).

Interventions:

Participants performed an emotional face recognition task, in which they evaluated 3 different affective face categories: Sad, Happy, and Angry, each ranging in a gradient from neutral to increasingly emotional. In the TSD group, the task was performed once under conditions of sleep deprivation, and twice under sleep-rested conditions following different durations of sleep recovery. In the SC group, the task was performed twice under sleep-rested conditions, controlling for repeatability.

Measurements and Results:

In the TSD group, when sleep-deprived, there was a marked and significant blunting in the recognition of Angry and Happy affective expressions in the moderate (but not extreme) emotional intensity range; differences that were most reliable and significant in female participants. No change in the recognition of Sad expressions was observed. These recognition deficits were, however, ameliorated following one night of recovery sleep. No changes in task performance were observed in the SC group.

Conclusions:

Sleep deprivation selectively impairs the accurate judgment of human facial emotions, especially threat relevant (Anger) and reward relevant (Happy) categories, an effect observed most significantly in females. Such findings suggest that sleep loss impairs discrete affective neural systems, disrupting the identification of salient affective social cues.

Citation:

van der Helm E; Gujar N; Walker MP. Sleep deprivation impairs the accurate recognition of human emotions. SLEEP 2010;33(3):335-342.     

Effects of sleep loss on emotion recognition: a dissociation between face and word stimuli

Short-term sleep deprivation, or extended wakefulness, adversely affects cognitive functions and behavior. However, scarce research has addressed the effects of sleep deprivation (SD) on emotional processing. In this study, we investigated the impact of reduced vigilance due to moderate sleep deprivation on the ability to recognize emotional expressions of faces and emotional content of words. Participants remained awake for 24 h and performed the tasks in two sessions, one in which they were not affected by sleep loss (baseline; BSL), and other affected by SD, according to a counterbalanced sequence. Tasks were carried out twice at 10:00 and 4:00 am, or at 12:00 and 6:00 am. In both tasks, participants had to respond to the emotional valence of the target stimulus: negative, positive, or neutral. The results showed that in the word task, sleep deprivation impaired recognition irrespective of the emotional valence of words. However, sleep deprivation impaired recognition of emotional face expressions mainly when they showed a neutral expression. Emotional face expressions were less affected by the sleep loss, but positive faces were more resistant than negative faces to the detrimental effect of sleep deprivation. The differential effects of sleep deprivation on recognition of the different emotional stimuli are indicative of emotional facial expressions being stronger emotional stimuli than emotional laden words. This dissociation may be attributed to the more automatic sensory encoding of emotional facial content.     

Time course of implicit processing and explicit processing of emotional faces and emotional words

Facial expressions are important emotional stimuli during social interactions. Symbolic emotional cues, such as affective words, also convey information regarding emotions that is relevant for social communication. Various studies have demonstrated fast decoding of emotions from words, as was shown for faces, whereas others report a rather delayed decoding of information about emotions from words. Here, we introduced an implicit (color naming) and explicit task (emotion judgment) with facial expressions and words, both containing information about emotions, to directly compare the time course of emotion processing using event-related potentials (ERP). The data show that only negative faces affected task performance, resulting in increased error rates compared to neutral faces. Presentation of emotional faces resulted in a modulation of the N170, the EPN and the LPP components and these modulations were found during both the explicit and implicit tasks. Emotional words only affected the EPN during the explicit task, but a task-independent effect on the LPP was revealed. Finally, emotional faces modulated source activity in the extrastriate cortex underlying the generation of the N170, EPN and LPP components. Emotional words led to a modulation of source activity corresponding to the EPN and LPP, but they also affected the N170 source on the right hemisphere. These data show that facial expressions affect earlier stages of emotion processing compared to emotional words, but the emotional value of words may have been detected at early stages of emotional processing in the visual cortex, as was indicated by the extrastriate source activity.     

Shortened night sleep impairs facial responsiveness to emotional stimuli

Sleep deprivation deteriorates mood, impairs the recognition of facial expressions, and affects the ability to regulate emotions. The present study investigated the effect of partial sleep deprivation on facial responses to emotional stimuli.     

Emotional expressiveness in sleep-deprived healthy adults

The purpose of this study was to evaluate the influence of sleep deprivation on emotional expression and subjective emotional experience in a highly controlled, laboratory setting. Twenty-three healthy adult participants watched positive (amusing) and negative (sad) film clips before and after they were randomly assigned to a night of sleep deprivation or a normal sleep control condition. The intensity of their facial expressiveness while viewing the films was coded by human judges and compared to their subjective emotional responses. Relative to the control group, sleep-deprived participants demonstrated less expressiveness, especially in response to positive stimuli. Subjective responses were not significantly different between the sleep-deprived and control groups. These preliminary results suggest that sleep deprivation is associated with attenuated emotional expressiveness in healthy adults.     

Increased amygdala activation is related to heart rate during emotion processing in adolescent subjects

Emotions have been conceptualized as representations of bodily responses to a stimulus that critically involves the autonomic nervous system (ANS). An association between amygdala activation and ANS activity has been shown in adults. However, to date, no studies have demonstrated this association in adolescents. Examining the interaction between the ANS and amygdala in healthy adolescents may provide information about age-related changes in the association between amygdala activation and ANS measures. Therefore, the aim of this study was to examine the relationship between amygdala activation and heart rate in normal adolescents. Eighteen 12- to 17-year old adolescents participated. Heart rate data was collected during functional magnetic resonance imaging while subjects performed a facial expression matching task that reliably activates the amygdala. Adolescents showed significant amygdala activation for all facial expressions relative to the shape-matching, control task. Moreover, the degree of activation in the right amygdala for Fearful faces was significantly correlated with heart rate (Spearman's rho=0.55, p=0.018, two-tailed). This study shows that amygdala activity is related to heart rate in healthy adolescents. Thus, similar to adults, adolescents show a coupling between processing emotional events and adjusting the ANS accordingly. Furthermore, this study confirms previous adolescent studies showing amygdala activation to Fearful, Angry, and Happy faces. Finally, the results of the present study lay the foundation for future research to investigate whether adolescents with mood or anxiety disorders show an altered coupling between processing emotionally salient events and ANS activity.     

The role of encoding and attention in facial emotion memory: An EEG investigation

Facial expressions are encoded via sensory mechanisms, but meaning extraction and salience of these expressions involve cognitive functions. We investigated the time course of sensory encoding and subsequent maintenance in memory via EEG. Twenty-nine healthy participants completed a facial emotion delayed match-to-sample task. P100, N170 and N250 ERPs were measured in response to the first stimulus, and evoked theta power (4–7 Hz) was measured during the delay interval. Negative facial expressions produced larger N170 amplitudes and greater theta power early in the delay. N170 amplitude correlated with theta power, however larger N170 amplitude coupled with greater theta power only predicted behavioural performance for one emotion condition (very happy) out of six tested (see Supplemental Data). These findings indicate that the N170 ERP may be sensitive to emotional facial expressions when task demands require encoding and retention of this information. Furthermore, sustained theta activity may represent continued attentional processing that supports short-term memory, especially of negative facial stimuli. Further study is needed to investigate the potential influence of these measures, and their interaction, on behavioural performance.     

Is a neutral expression also a neutral stimulus? A study with functional magnetic resonance

Although neutral faces do not initially convey an explicit emotional message, it has been found that individuals tend to assign them an affective content. Moreover, previous research has shown that affective judgments are mediated by the task they have to perform. Using functional magnetic resonance imaging in 21 healthy participants, we focus this study on the cerebral activity patterns triggered by neutral and emotional faces in two different tasks (social or gender judgments). Results obtained, using conjunction analyses, indicated that viewing both emotional and neutral faces evokes activity in several similar brain areas indicating a common neural substrate. Moreover, neutral faces specifically elicit activation of cerebellum, frontal and temporal areas, while emotional faces involve the cuneus, anterior cingulated gyrus, medial orbitofrontal cortex, posterior superior temporal gyrus, precentral/postcentral gyrus and insula. The task selected was also found to influence brain activity, in that the social task recruited frontal areas while the gender task involved the posterior cingulated, inferior parietal lobule and middle temporal gyrus to a greater extent. Specifically, in the social task viewing neutral faces was associated with longer reaction times and increased activity of left dorsolateral frontal cortex compared with viewing facial expressions of emotions. In contrast, in the same task emotional expressions distinctively activated the left amygdale. The results are discussed taking into consideration the fact that, like other facial expressions, neutral expressions are usually assigned some emotional significance. However, neutral faces evoke a greater activation of circuits probably involved in more elaborate cognitive processing.     

Tonic pain grabs attention, but leaves the processing of facial expressions intact-evidence from event-related brain potentials

Emotion and attention are key players in the modulation of pain perception. However, much less is known about the reverse influence of pain on attentional and especially emotional processes. To this end, we employed painful vs. non-painful pressure stimulation to examine effects on the processing of simultaneously presented facial expressions (fearful, neutral, happy). Continuous EEG was recorded and participants had to rate each facial expression with regard to valence and arousal. Painful stimulation attenuated visual processing in general, as reduced P100 and late positive potential (LPP) amplitudes revealed, but did not interfere with structural encoding of faces (N170). In addition, early perceptual discrimination and sustained preferential processing of emotional facial expressions as well as affective ratings were not influenced by pain. Thus, tonic pain demonstrates strong attention-demanding properties, but this does not interfere with concurrently ongoing emotion discrimination processes. These effects point at partially independent effects of pain on emotion and attention, respectively.     

Dissociable effects of psychopathic traits on cortical and subcortical visual pathways during facial emotion processing: An ERP study on the N170

This study examined the relation between psychopathic traits and the brain response to facial emotion by analyzing the N170 component of the ERP. Fifty‐four healthy participants were assessed for psychopathic traits and exposed to images of emotional and neutral faces with varying spatial frequency content. The N170 was modulated by the emotional expressions, irrespective of psychopathic traits. Fearless dominance was associated with a reduced N170, driven by the low spatial frequency components of the stimuli, and dependent on the tectopulvinar visual pathway. Conversely, coldheartedness was related to overall enhanced N170, suggesting mediation by geniculostriate processing. Results suggest that different dimensions of psychopathy are related to distinct facial emotion processing mechanisms and support the existence of both amygdala deficits and compensatory engagement of cortical structures for emotional processing in psychopathy.     

Attention modulates emotional expression processing

To investigate the time course of emotional expression processing, we recorded ERPs to facial stimuli. The first task was to discriminate emotional expressions. Enhanced negativity of the face-specific N170 was elicited by emotional as opposed to neutral faces, followed by the occipital negativity (240-340 ms poststimulus). The second task was to classify face gender. Here, N170 was unaffected by the emotional expression. However, emotional expression effect was expressed in the anterior positivity (160-250 ms poststimulus) and subsequent occipital negativity (240-340 ms poststimulus). Results support the thesis that structural encoding relevant to gender recognition and simultaneous expression analysis are independent processes. Attention modulates facial emotion processing 140-185 ms poststimulus. Involuntary differentiation of facial expression was observed later (160-340 ms poststimulus), suggesting unintentional attention capture.     

Sodium valproate improves sensorimotor gating deficit induced by sleep deprivation at low doses

Background/aim Sleep deprivation disrupts prepulse inhibition of acoustic startle reflex and can be used to mimic psychosis in experimental animals. On the other hand, it is also a model for other disorders of sensory processing, including migraine. This study aims to assess the effects of sodium valproate, a drug that is used in a variety of neuropsychiatric disorders, on normal and disrupted sensorimotor gating in rats.Materials and methods Sixty-two Wistar albino rats were randomly distributed into 8 groups. Subchronic and intraperitoneal sodium valproate were administrated to the sleep-deprived and nonsleep-deprived rats by either 50–100 or 200 mg/kg/day. Prepulse inhibition test and locomotor activity test were performed. Sleep deprivation induced by the modified multiple platform method.Results Sleep deprivation impaired prepulse inhibition, decreased startle amplitude, and increased locomotor activity. Sodium valproate did not significantly alter prepulse inhibition and locomotor activity in nonsleep-deprived and sleep-deprived groups. On the other hand, all doses decreased locomotor activity in drug-treated groups, and low dose improved sensorimotor gating and startle amplitude after sleep deprivation.Conclusion Low-dose sodium valproate improves sleep deprivation-disrupted sensorimotor gating, and this finding may rationalize the use of sodium valproate in psychotic states and other sensory processing disorders. Dose-dependent effects of sodium valproate on sensorimotor gating should be investigated in detail.     

Emotion perception and interpersonal behavior in epilepsy patients after unilateral amygdalohippocampectomy

Aim of this study was to examine the relation between perception of facial expressions and interpersonal behavior in epilepsy patients after unilateral amygdalohippocampectomy (AH). Nine patients with unilateral amygdalohippocampectomy and 14 controls completed a forced-choice emotional recognition task, in which morphed facial emotional expressions were shown at different emotional intensities, and a self-report questionnaire of interpersonal behavior. Face perception and depressive symptoms were also taken into account. Compared to normal controls, patients were less sensitive in the recognition of fearful and disgusted facial expressions, in line with previous reports. These impairments were only minimally correlated with self-report interpersonal behavior. In all, unilateral damage to the amygdala and medial temporal lobe results in subtle emotion recognition impairments, but these deficits do not appear to extend to self-reported impairments in everyday interpersonal behavior. Further studies need to explore in more detail the effects of these subtle recognition problems on daily social intercourse.     

Interaction of facial expressions and familiarity: ERP evidence

There is mounting evidence that under some conditions the processing of facial identity and facial emotional expressions may not be independent; however, the nature of this interaction remains to be established. By using event-related brain potentials (ERP) we attempted to localize these interactions within the information processing system. During an expression discrimination task (Experiment 1) categorization was faster for portraits of personally familiar vs. unfamiliar persons displaying happiness. The peak latency of the P300 (trend) and the onset of the stimulus-locked LRP were shorter for familiar than unfamiliar faces. This implies a late perceptual but pre-motoric locus of the facilitating effect of familiarity on expression categorization. In Experiment 2 participants performed familiarity decisions about portraits expressing different emotions. Results revealed an advantage of happiness over disgust specifically for familiar faces. The facilitation was localized in the response selection stage as suggested by a shorter onset of the LRP. Both experiments indicate that familiarity and facial expression may not be independent processes. However, depending on the kind of decision different processing stages may be facilitated for happy familiar faces.     

Emotional content modulates response inhibition and perceptual processing

In this study, event‐related potentials were used to investigate the effect of emotion on response inhibition. Participants performed an emotional go/no‐go task that required responses to human faces associated with a “go” valence (i.e., emotional, neutral) and response inhibition to human faces associated with a “no‐go” valence. Emotional content impaired response inhibition, as evidenced by decreased response accuracy and N2 amplitudes in no‐go trials. More importantly, emotional expressions elicited larger N170 amplitudes than neutral expressions, and this effect was larger in no‐go than in go trials, indicating that the perceptual processing of emotional expression had priority in inhibitory trials. In no‐go trials, correlation analysis showed that increased N170 amplitudes were associated with decreased N2 amplitudes. Taken together, our findings suggest that emotional content impairs response inhibition due to the prioritization of emotional content processing.     

In the face of anger: Startle modulation to graded facial expressions

In the present study, the startle reflex was examined with respect to the degree of anger displayed in facial expressions. To this end, 52 participants viewed faces that were morphed to display 0, 20, 40, 60, 80, or 100% anger. As the percentage of anger in faces increased from 0 to 100%, faces were perceived as increasingly angry; however, relative to neutral facial expressions, startle amplitude was only potentiated to maximally angry faces. These data imply a non‐linear relationship between the intensity of angry faces and defensive physiological activity. This pattern of startle modulation suggests a categorical distinction between threatening (100% anger) and other facial expressions presented. These results are further discussed in terms of existing data, and how this paradigm might be utilized in psychopathology research.     

Effect of sleep deprivation on emotional working memory

The emotional dysregulation and impaired working memory found after sleep loss can have severe implications for our daily functioning. Considering the intertwined relationship between emotion and cognition in stimuli processing, there could be further implications of sleep deprivation in high‐complex emotional situations. Although studied separately, this interaction between emotion and cognitive processes has been neglected in sleep research. The aim of the present study was to investigate the effect of 1 night of sleep deprivation on emotional working memory. Sixty‐one healthy participants (mean age: 23.4 years) were either sleep deprived for 1 night (n = 30) or had a normal night’s sleep (n = 31). They performed an N‐back task with two levels of working memory load (1‐back and 3‐back) using positive, neutral and negative picture scenes. Sleep deprivation, compared with full night sleep, impaired emotional working memory accuracy, but not reaction times. The sleep‐deprived participants, but not the controls, responded faster to positive than to negative and neutral pictures. The effect of sleep deprivation was similar for both high and low working memory loads. The results showed that although detrimental in terms of accuracy, sleep deprivation did not impair working memory speed. In fact, our findings indicate that positive stimuli may facilitate working memory processing speed after sleep deprivation.     

A comparison of selective attention and facial processing biases in typically developing children who are high and low in self-reported trait anxiety

The relationship between children's anxiety and cognitive biases was examined in two tasks. A group of 50 children aged 10 to 11 years (mean = 11 years, SD = 3.71 months) was given two tasks. The first tested children's selective attention (SA) to threat in an emotional Stroop task. The second explored facial processing biases using morphed angry-neutral and happy-neutral emotional expressions that varied in intensity. Faces with varying levels of emotion (25% emotion-75% neutral, 50% emotion-50% neutral, 100% emotion-0% neutral [prototype] and 150% emotion-0% neutral [caricature]) were judged as being angry or happy. Results support previous work highlighting a link between anxiety and SA to threat. In addition, increased anxiety in late childhood is associated with decreased ability to discriminate facial expression. Finally, lack of discrimination in the emotional expression task was related to lack of inhibition to threat in the Stroop task.     

Modification of N170 by different emotional expression of schematic faces

The N170 is widely regarded as a face sensitive potential, having its maximum at occipito-temporal sites, with right-hemisphere dominance. However, it is debatable whether the N170 is modulated by different emotional expressions of a face. The aim of this study was to analyze the N170 elicited by schematic happy and angry faces when the emotional expression is semantically processed. To investigate the influence of different emotional expressions of schematic faces, we used a Prime-Probe procedure with the N400 effect as an indicator for a semantic processing. Eighteen subjects were presented the German word "happiness" or "anger" followed by happy and angry faces. The word-face pair could be congruent or incongruent in emotional meaning. Subjects were instructed to compare the emotional meaning of the words and faces and to count the congruent trials. Event-related potentials were recorded from 124 sites. Congruent faces elicited a smaller negativity in the N400 time range than incongruent faces, indicating that the facial emotional expression was cognitively processed. The face sensitive N170 was most pronounced at posterior and occipital sites, and N170 amplitudes were larger following the angry as compared to the happy faces. It is concluded that different emotional expressions of schematic faces can modulate the N170.     

Differential modulations of reward expectation on implicit facial emotion processing: ERP evidence

Implicit emotional processing refers to the preferential processing of emotional content even if it is task irrelevant. Given that motivation enhances executive control by biasing attentional resources toward target stimuli, here we investigated the effects of reward expectation on implicit facial emotional processing in two experiments using ERPs. A precue signaling additional monetary reward for fast and accurate response for the upcoming trial (incentive condition; relative to a cue indicating no such additional reward, i.e., nonincentive condition) was followed by the presentation of a happy, angry, or neutral face. Participants had to determine the gender of the face in Experiment 1 and decide whether a number superimposed on the face was even or odd in Experiment 2. In both experiments, incentive cues elicited larger P3 and contingent negative variation responses, and the targets following incentive cues elicited more positive‐going ERPs (200–700 ms), compared with the nonincentive condition. Importantly, the N2 responses (200–280 ms) to the target exhibited differential patterns of Reward × Emotion interaction: relative to the nonincentive condition, the N2 amplitude differences between emotional (i.e., happy and/or angry) and neutral faces increased in the incentive condition in Experiment 1, but diminished in Experiment 2. These results indicate that reward expectation can differentially modulate implicit processing of facial expressions, with increased sensitivity to emotions when the processing of whole faces is required, but with reduced sensitivity when the processing of faces is distractive. This study enriches the evidence for interactions between reward‐related executive control and implicit emotional processing.