Sex differences in neural activation to facial expressions denoting contempt and disgust

The facial expression of contempt has been regarded to communicate feelings of moral superiority. Contempt is an emotion that is closely related to disgust, but in contrast to disgust, contempt is inherently interpersonal and hierarchical. The aim of this study was twofold. First, to investigate the hypothesis of preferential amygdala responses to contempt expressions versus disgust. Second, to investigate whether, at a neural level, men would respond stronger to biological signals of interpersonal superiority (e.g., contempt) than women. We performed an experiment using functional magnetic resonance imaging (fMRI), in which participants watched facial expressions of contempt and disgust in addition to neutral expressions. The faces were presented as distractors in an oddball task in which participants had to react to one target face. Facial expressions of contempt and disgust activated a network of brain regions, including prefrontal areas (superior, middle and medial prefrontal gyrus), anterior cingulate, insula, amygdala, parietal cortex, fusiform gyrus, occipital cortex, putamen and thalamus. Contemptuous faces did not elicit stronger amygdala activation than did disgusted expressions. To limit the number of statistical comparisons, we confined our analyses of sex differences to the frontal and temporal lobes. Men displayed stronger brain activation than women to facial expressions of contempt in the medial frontal gyrus, inferior frontal gyrus, and superior temporal gyrus. Conversely, women showed stronger neural responses than men to facial expressions of disgust. In addition, the effect of stimulus sex differed for men versus women. Specifically, women showed stronger responses to male contemptuous faces (as compared to female expressions), in the insula and middle frontal gyrus. Contempt has been conceptualized as signaling perceived moral violations of social hierarchy, whereas disgust would signal violations of physical purity. Thus, our results suggest a neural basis for sex differences in moral sensitivity regarding hierarchy on the one hand and physical purity on the other.     

Neural structures associated with recognition of facial expressions of basic emotions.

People with Huntington''s disease and people suffering from obsessive compulsive disorder show severe deficits in recognizing facial expressions of disgust, whereas people with lesions restricted to the amygdala are especially impaired in recognizing facial expressions of fear. This double dissociation implies that recognition of certain basic emotions may be associated with distinct and non-overlapping neural substrates. Some authors, however, emphasize the general importance of the ventral parts of the frontal cortex in emotion recognition, regardless of the emotion being recognized. In this study, we used functional magnetic resonance imaging to locate neural structures that are critical for recognition of facial expressions of basic emotions by investigating cerebral activation of six healthy adults performing a gender discrimination task on images of faces expressing disgust, fear and anger. Activation in response to these faces was compared with that for faces showing neutral expressions. Disgusted facial expressions activated the right putamen and the left insula cortex, whereas enhanced activity in the posterior part of the right gyrus cinguli and the medial temporal gyrus of the left hemisphere was observed during processing of angry faces. Fearful expressions activated the right fusiform gyrus and the left dorsolateral frontal cortex. For all three emotions investigated, we also found activation of the inferior part of the left frontal cortex (Brodmann area 47). These results support the hypotheses derived from neuropsychological findings, that (i) recognition of disgust, fear and anger is based on separate neural systems, and that (ii) the output of these systems converges on frontal regions for further information processing.     

Developmental and Individual Differences in the Neural Processing of Dynamic Expressions of Pain and Anger

We examined the processing of facial expressions of pain and anger in 8-month-old infants and adults by measuring event-related brain potentials (ERPs) and frontal EEG alpha asymmetry. The ERP results revealed that while adults showed a late positive potential (LPP) to emotional expressions that was enhanced to pain expressions, reflecting increased evaluation and emotional arousal to pain expressions, infants showed a negative component (Nc) to emotional expressions that was enhanced to angry expressions, reflecting increased allocation of attention to angry faces. Moreover, infants and adults showed opposite patterns in their frontal asymmetry responses to pain and anger, suggesting developmental differences in the motivational processes engendered by these facial expressions. These findings are discussed in the light of associated individual differences in infant temperament and adult dispositional empathy.     

Emotional intelligence and oscillatory responses to emotional facial expressions

Emotional intelligence-related differences in oscillatory responses to emotional facial expressions were investigated in 48 subjects (26 men and 22 women), age 18–30 years. Participants were instructed to evaluate emotional expression (angry, happy, and neutral) of each presented face on an analog scale ranging from ?100 (very hostile) to + 100 (very friendly). High emotional intelligence (EI) participants were found to be more sensitive to the emotional content of the stimuli. It showed up both in their subjective evaluation of the stimuli and in a stronger EEG theta synchronization at an earlier (between 100 and 500 ms after face presentation) processing stage. Source localization using sLORETA showed that this effect was localized in the fusiform gyrus upon the presentation of angry faces and in the posterior cingulate gyrus upon the presentation of happy faces. At a later processing stage (500–870 ms), event-related theta synchronization in high emotional intelligence subjects was higher in the left prefrontal cortex upon the presentation of happy faces, but it was lower in the anterior cingulate cortex upon the presentation of angry faces. This suggests the existence of a mechanism that can selectively increase the positive emotions and reduce negative emotions.     

Neural responses to facial and vocal expressions of fear and disgust.

Neuropsychological studies report more impaired responses to facial expressions of fear than disgust in people with amygdala lesions, and vice versa in people with Huntington''s disease. Experiments using functional magnetic resonance imaging (fMRI) have confirmed the role of the amygdala in the response to fearful faces and have implicated the anterior insula in the response to facial expressions of disgust. We used fMRI to extend these studies to the perception of fear and disgust from both facial and vocal expressions. Consistent with neuropsychological findings, both types of fearful stimuli activated the amygdala. Facial expressions of disgust activated the anterior insula and the caudate-putamen; vocal expressions of disgust did not significantly activate either of these regions. All four types of stimuli activated the superior temporal gyrus. Our findings therefore (i) support the differential localization of the neural substrates of fear and disgust; (ii) confirm the involvement of the amygdala in the emotion of fear, whether evoked by facial or vocal expressions; (iii) confirm the involvement of the anterior insula and the striatum in reactions to facial expressions of disgust; and (iv) suggest a possible general role for the perception of emotional expressions for the superior temporal gyrus.     

Neural correlates of perceiving emotional faces and bodies in developmental prosopagnosia: an event-related fMRI-study

Many people experience transient difficulties in recognizing faces but only a small number of them cannot recognize their family members when meeting them unexpectedly. Such face blindness is associated with serious problems in everyday life. A better understanding of the neuro-functional basis of impaired face recognition may be achieved by a careful comparison with an equally unique object category and by a adding a more realistic setting involving neutral faces as well facial expressions. We used event-related functional magnetic resonance imaging (fMRI) to investigate the neuro-functional basis of perceiving faces and bodies in three developmental prosopagnosics (DP) and matched healthy controls. Our approach involved materials consisting of neutral faces and bodies as well as faces and bodies expressing fear or happiness. The first main result is that the presence of emotional information has a different effect in the patient vs. the control group in the fusiform face area (FFA). Neutral faces trigger lower activation in the DP group, compared to the control group, while activation for facial expressions is the same in both groups. The second main result is that compared to controls, DPs have increased activation for bodies in the inferior occipital gyrus (IOG) and for neutral faces in the extrastriate body area (EBA), indicating that body and face sensitive processes are less categorically segregated in DP. Taken together our study shows the importance of using naturalistic emotional stimuli for a better understanding of developmental face deficits.     

Different Timing Features in Brain Processing of Core and Moral Disgust Pictures: An Event-Related Potentials Study

Disgust, an emotion motivating withdrawal from offensive stimuli, protects us from the risk of biological pathogens and sociomoral violations. Homogeneity of its two types, namely, core and moral disgust has been under intensive debate. To examine the dynamic relationship between them, we recorded event-related potentials (ERPs) for core disgust, moral disgust and neutral pictures while participants performed a modified oddball task. ERP analysis revealed that N1 and P2 amplitudes were largest for the core disgust pictures, indicating automatic processing of the core disgust-evoking pictures. N2 amplitudes were higher for pictures evoking moral disgust relative to core disgust and neutral pictures, reflecting a violation of social norms. The core disgust pictures elicited larger P3 and late positive potential (LPP) amplitudes in comparison with the moral disgust pictures which, in turn, elicited larger P3 and LPP amplitudes when compared to the neutral pictures. Taken together, these findings indicated that core and moral disgust pictures elicited different neural activities at various stages of information processing, which provided supporting evidence for the heterogeneity of disgust.     

Event-related Potential Study of the Effects of Emotional Facial Expressions on Task Performance in Euthymic Bipolar Patients

There appears to be a significant disconnect between symptomatic and functional recovery in bipolar disorder (BD). Some evidence points to interepisode cognitive dysfunction. We tested the hypothesis that some of this dysfunction was related to emotional reactivity in euthymic bipolar subjects may effect cognitive processing. A modification of emotional gender categorization oddball task was used. The target was gender (probability 25%) of faces with negative, positive, and neutral emotional expression. The experiment had 720 trials (3 blocks × 240 trials each). Each stimulus was presented for 150 ms, and the EEG/ERP responses were recorded for 1,000 ms. The inter-trial interval was varied in 1,100–1,500 ms range to avoid expectancy effects. Task took about 35 min to complete. There were 9 BD and 9 control subjects matched for age and gender. Reaction time (RT) was globally slower in BD subjects. The centro-parietal amplitudes at N170 and N200, and P200 and P300 were generally smaller in the BD group compared to controls. Latency was shorter to neutral and negative targets in BD. Frontal P200 amplitude was higher to emotional negative facial non-targets in BD subjects. The frontal N200 in response to positive facial emotion was less negative in BD subjects. The frontal P300 of BD subjects was lower to emotionally neutral targets. ERP responses to facial emotion in BD subjects varied significantly from normal controls. These variations are consistent with the common depressive symptomology seen in long term studies of bipolar subjects.     

Effect of empathy trait on attention to various facial expressions: evidence from N170 and late positive potential (LPP)

Background

The present study sought to clarify the relationship between empathy trait and attention responses to happy, angry, surprised, afraid, and sad facial expressions. As indices of attention, we recorded event-related potentials (ERP) and focused on N170 and late positive potential (LPP) components.

Methods

Twenty-two participants (12 males, 10 females) discriminated facial expressions (happy, angry, surprised, afraid, and sad) from emotionally neutral faces under an oddball paradigm. The empathy trait of participants was measured using the Interpersonal Reactivity Index (IRI, J Pers Soc Psychol 44:113–126, 1983).

Results

Participants with higher IRI scores showed: 1) more negative amplitude of N170 (140 to 200 ms) in the right posterior temporal area elicited by happy, angry, surprised, and afraid faces; 2) more positive amplitude of early LPP (300 to 600 ms) in the parietal area elicited in response to angry and afraid faces; and 3) more positive amplitude of late LPP (600 to 800 ms) in the frontal area elicited in response to happy, angry, surprised, afraid, and sad faces, compared to participants with lower IRI scores.

Conclusions

These results suggest that individuals with high empathy pay attention to various facial expressions more than those with low empathy, from very-early stage (reflected in N170) to late-stage (reflected in LPP) processing of faces.     

Seeing fearful body expressions activates the fusiform cortex and amygdala

Darwin's evolutionary approach to organisms' emotional states attributes a prominent role to expressions of emotion in whole-body actions. Researchers in social psychology [1,2] and human development [3] have long emphasized the fact that emotional states are expressed through body movement, but cognitive neuroscientists have almost exclusively considered isolated facial expressions (for review, see [4]). Here we used high-field fMRI to determine the underlying neural mechanisms of perception of body expression of emotion. Subjects were presented with short blocks of body expressions of fear alternating with short blocks of emotionally neutral meaningful body gestures. All images had internal facial features blurred out to avoid confounds due to a face or facial expression. We show that exposure to body expressions of fear, as opposed to neutral body postures, activates the fusiform gyrus and the amygdala. The fact that these two areas have previously been associated with the processing of faces and facial expressions [5-8] suggests synergies between facial and body-action expressions of emotion. Our findings open a new area of investigation of the role of body expressions of emotion in adaptive behavior as well as the relation between processes of emotion recognition in the face and in the body.     

Neural Processing of Emotional Facial and Semantic Expressions in Euthymic Bipolar Disorder (BD) and Its Association with Theory of Mind (ToM)

Background

Adults with bipolar disorder (BD) have cognitive impairments that affect face processing and social cognition. However, it remains unknown whether these deficits in euthymic BD have impaired brain markers of emotional processing.

Methodology/Principal Findings

We recruited twenty six participants, 13 controls subjects with an equal number of euthymic BD participants. We used an event-related potential (ERP) assessment of a dual valence task (DVT), in which faces (angry and happy), words (pleasant and unpleasant), and face-word simultaneous combinations are presented to test the effects of the stimulus type (face vs word) and valence (positive vs. negative). All participants received clinical, neuropsychological and social cognition evaluations. ERP analysis revealed that both groups showed N170 modulation of stimulus type effects (face > word). BD patients exhibited reduced and enhanced N170 to facial and semantic valence, respectively. The neural source estimation of N170 was a posterior section of the fusiform gyrus (FG), including the face fusiform area (FFA). Neural generators of N170 for faces (FG and FFA) were reduced in BD. In these patients, N170 modulation was associated with social cognition (theory of mind).

Conclusions/Significance

This is the first report of euthymic BD exhibiting abnormal N170 emotional discrimination associated with theory of mind impairments.     

形状识别的功能定位和时间过程:功能磁共振与脑电结合的研究

通过结合具有高空间分辨率的功能磁共振成像（fMRI）和具有高时间分辨率的128导脑电事件相关电位（ERP）两项技术,测量了视皮层腹侧区域对图形形状识别任务反应的空间定位和时间过程。fMRI的实验结果表明,图形的形状和觉引起了腹测GTi／GF皮层区域的兴奋。进一步,基于fMRI兴奋区域的种子偶极子模型拟合的的ERP动态定位分析的结果和自由运动的偶极子模型拟合的ERP定位分析结果表明：GTi／GF区域活动的时间发生在刺激呈现之后132－176ms时间段,峰值150ms左右,相应于ERP的N1成分。这些结果在人类大脑皮层上同时确定了视觉通路中涉及图形形状识别的兴奋区域和兴奋的时间过程。     

Time Perception and Dynamics of Facial Expressions of Emotions

Two experiments were run to examine the effects of dynamic displays of facial expressions of emotions on time judgments. The participants were given a temporal bisection task with emotional facial expressions presented in a dynamic or a static display. Two emotional facial expressions and a neutral expression were tested and compared. Each of the emotional expressions had the same affective valence (unpleasant), but one was high-arousing (expressing anger) and the other low-arousing (expressing sadness). Our results showed that time judgments are highly sensitive to movements in facial expressions and the emotions expressed. Indeed, longer perceived durations were found in response to the dynamic faces and the high-arousing emotional expressions compared to the static faces and low-arousing expressions. In addition, the facial movements amplified the effect of emotions on time perception. Dynamic facial expressions are thus interesting tools for examining variations in temporal judgments in different social contexts.     

Hemispheric asymmetry of visual evoked potentials during human recognition of facial emotional expressions

Visual evoked potentials (VEP) in standard 16 EEG derivations were recorded in 26 young men and 20 women during recognition of facial emotional expressions and geometric figures. The stimuli were presented on a computer screen in the center of the visual field or randomly in the right or left vision hemifields. Peak VEP latency and mean amplitude in 50-ms epochs were measured; spatiotemporal VEP dynamics was analyzed in a series of topographic maps. The right hemisphere was shown to be more important in processing emotional faces. The character of the asymmetry was dynamic: at earlier stages of emotion processing the electrical activity was higher in the right inferior temporal region compared to the left symmetrical site. Later on the activity was higher in the right frontal and central areas. The dynamic mapping of "face-selective" component N180 of VEPs revealed the onset of activation over the right frontal areas that was followed by the fast activation of symmetrical left zones. Notably, this dynamics didn't correlate with the hemifield of stimuli exposition. The degree of asymmetry was lower during presentation of figures, especially in the inferior temporal and frontal regions. The prominent asymmetry of information processes in the inferior temporal and frontal areas was suggested to be specific for recognition of facial expression.     

Effects of low-spatial frequency components of fearful faces on fusiform cortex activity

Emotive faces elicit neural responses even when they are not consciously perceived. We used faces hybridized from spatial frequency-filtered individual stimuli to study processing of facial emotion. Employing event-related functional magnetic resonance imaging (fMRI), we show enhanced fusiform cortex responses to hybrid faces containing fearful expressions when such emotional cues are present in the low-spatial frequency (LSF) range. Critically, this effect is independent of whether subjects use LSF or high-spatial frequency (HSF) information to make gender judgments on the hybridized faces. The magnitude of this fusiform enhancement predicts behavioral slowing in response times when participants report HSF information of the hybrid stimulus in the presence of fear in the unreported LSF components. Thus, emotional modulation of a face-responsive region of fusiform is driven by the low-frequency components of the stimulus, an effect independent of subjects' reported perception but evident in an incidental measure of behavioral performance.     

Effects of AKAP5 Pro100Leu Genotype on Working Memory for Emotional Stimuli

Recent investigations addressing the role of the synaptic multiadaptor molecule AKAP5 in human emotion and behavior suggest that the AKAP5 Pro100Leu polymorphism (rs2230491) contributes to individual differences in affective control. Carriers of the less common Leu allele show a higher control of anger as indicated by behavioral measures and dACC brain response on emotional distracters when compared to Pro homozygotes. In the current fMRI study we used an emotional working memory task according to the n-back scheme with neutral and negative emotional faces as target stimuli. Pro homozygotes showed a performance advantage at the behavioral level and exhibited enhanced activation of the amygdala and fusiform face area during working memory for emotional faces. On the other hand, Leu carriers exhibited increased activation of the dACC during performance of the 2-back condition. Our results suggest that AKAP5 Pro100Leu effects on emotion processing might be task-dependent with Pro homozygotes showing lower control of emotional interference, but more efficient processing of task-relevant emotional stimuli.     

Positive Facial Affect – An fMRI Study on the Involvement of Insula and Amygdala

Imitation of facial expressions engages the putative human mirror neuron system as well as the insula and the amygdala as part of the limbic system. The specific function of the latter two regions during emotional actions is still under debate. The current study investigated brain responses during imitation of positive in comparison to non-emotional facial expressions. Differences in brain activation of the amygdala and insula were additionally examined during observation and execution of facial expressions. Participants imitated, executed and observed happy and non-emotional facial expressions, as well as neutral faces. During imitation, higher right hemispheric activation emerged in the happy compared to the non-emotional condition in the right anterior insula and the right amygdala, in addition to the pre-supplementary motor area, middle temporal gyrus and the inferior frontal gyrus. Region-of-interest analyses revealed that the right insula was more strongly recruited by (i) imitation and execution than by observation of facial expressions, that (ii) the insula was significantly stronger activated by happy than by non-emotional facial expressions during observation and imitation and that (iii) the activation differences in the right amygdala between happy and non-emotional facial expressions were increased during imitation and execution, in comparison to sole observation. We suggest that the insula and the amygdala contribute specifically to the happy emotional connotation of the facial expressions depending on the task. The pattern of the insula activity might reflect increased bodily awareness during active execution compared to passive observation and during visual processing of the happy compared to non-emotional facial expressions. The activation specific for the happy facial expression of the amygdala during motor tasks, but not in the observation condition, might reflect increased autonomic activity or feedback from facial muscles to the amygdala.     

Influence of Repressive Coping Style on Cortical Activation during Encoding of Angry Faces

Background

Coping plays an important role for emotion regulation in threatening situations. The model of coping modes designates repression and sensitization as two independent coping styles. Repression consists of strategies that shield the individual from arousal. Sensitization indicates increased analysis of the environment in order to reduce uncertainty. According to the discontinuity hypothesis, repressors are sensitive to threat in the early stages of information processing. While repressors do not exhibit memory disturbances early on, they manifest weak memory for these stimuli later. This study investigates the discontinuity hypothesis using functional magnetic resonance imaging (fMRI).

Methods

Healthy volunteers (20 repressors and 20 sensitizers) were selected from a sample of 150 students on the basis of the Mainz Coping Inventory. During the fMRI experiment, subjects evaluated and memorized emotional and neutral faces. Subjects performed two sessions of face recognition: immediately after the fMRI session and three days later.

Results

Repressors exhibited greater activation of frontal, parietal and temporal areas during encoding of angry faces compared to sensitizers. There were no differences in recognition of facial emotions between groups neither immediately after exposure nor after three days.

Conclusions

The fMRI findings suggest that repressors manifest an enhanced neural processing of directly threatening facial expression which confirms the assumption of hyper-responsivity to threatening information in repression in an early processing stage. A discrepancy was observed between high neural activation in encoding-relevant brain areas in response to angry faces in repressors and no advantage in subsequent memory for these faces compared to sensitizers.     

Emotional expectations influence neural sensitivity to fearful faces in humans: An event-related potential study

The present study tested whether neural sensitivity to salient emotional facial expressions was influenced by emotional expectations induced by a cue that validly predicted the expression of a subsequently presented target face. Event-related potentials (ERPs) elicited by fearful and neutral faces were recorded while participants performed a gender discrimination task under cued (‘expected’) and uncued (‘unexpected’) conditions. The behavioral results revealed that accuracy was lower for fearful compared with neutral faces in the unexpected condition, while accuracy was similar for fearful and neutral faces in the expected condition. ERP data revealed increased amplitudes in the P2 component and 200–250 ms interval for unexpected fearful versus neutral faces. By contrast, ERP responses were similar for fearful and neutral faces in the expected condition. These findings indicate that human neural sensitivity to fearful faces is modulated by emotional expectations. Although the neural system is sensitive to unpredictable emotionally salient stimuli, sensitivity to salient stimuli is reduced when these stimuli are predictable.     

Neurophysiological correlates of induced discrete emotions in humans: an individual analysis

The present study addressed EEG pattering during experimentally manipulated emotion. Film clips previously shown to induce happiness,joy, anger, disgust, fear/anxiety, sadness, as well as neutral control films, were presented to 30 university students while a 62-channel EEG was recorded, and a self-reported effect was described. Analyses revealed both emotion-specific and emotion-unspecific EEG pattering for the emotions under study. Induced positive and negative emotions were accompanied by hemispheric activation asymmetries in theta-2, alpha-2, and beta-1 EEG frequency bands. Emotions of joy and disgust induced lateralized a theta-2 power increase in anterior-temporal and frontal regions of the left hemisphere reflecting involvement of cognitive mechanisms in the emotional processing. Negative emotions of disgust and fear/anxiety were characterized by alpha-2 and beta-1 desynchronization of the right temporal-parietal cortex, suggesting its involvement in modulation of the emotion-related arousal.