Fearful Facial Expressions Research Articles

The effects of nalmefene on emotion processing in alcohol use disorder – A randomized, controlled fMRI study

Nalmefene is a µ- and δ-opioid receptor antagonist and a partial κ-opioid receptor agonist. The drug is suggested to reduce the craving for, and the consumption of alcohol effectively, also alleviating anxiety and anhedonia. The present fMRI study is the first to investigate the processing of emotions as a possible mechanism of action of nalmefene in humans. Fifteen non-treatment-seeking participants suffering from alcohol use disorder (AUD) (24–66 years; 5 females) finished this randomized, placebo controlled, double blind study. Following a cross over design, participants received either a single dose nalmefene or a placebo, with an interval of one week between sessions. Using fMRI, we investigated neural reactivity during the presentation of emotional faces picture sets. Additionally, we performed a visual dot-probe task to detect nalmefene's effects on attentional bias. We detected an increase in the response to emotional faces in the supramarginal gyrus, the angular gyrus as well as the putamen in the nalmefene vs. placebo condition. However, contradictory to our initial hypotheses, amygdala activation was not altered significantly in the placebo condition – a limitation, which might be associated with a lack of activation in the placebo condition maybe due to the small sample size. Attentional bias analyses revealed an interaction effect by trend, which was driven by a significant effect in a sub-analysis showing increased attentional shift towards happy compared to fearful facial expressions under nalmefene. Nalmefene increased brain activation in areas responsible for empathy, social cognition and behavior, which might help alleviating the reinforcing properties of alcohol.

No influence of eye gaze on emotional face processing in the absence of conscious awareness

The human brain has evolved specialised mechanisms to enable the rapid detection of threat cues, including emotional face expressions (e.g., fear and anger). However, contextual cues – such as gaze direction – influence the ability to recognise emotional expressions. For instance, anger paired with direct gaze, and fear paired with averted gaze are more accurately recognised compared to alternate conjunctions of these features. It is argued that this is because gaze direction conveys the relevance and locus of the threat to the observer. Here, we used continuous flash suppression (CFS) to assess whether the modulatory effect of gaze direction on emotional face processing occurs outside of conscious awareness. Previous research using CFS has demonstrated that fearful facial expressions are prioritised by the visual system and gain privileged access to awareness over other expressed emotions. We hypothesised that if the modulatory effects of gaze on emotional face processing occur also at this level, then the gaze-emotion conjunctions signalling self-relevant threat will reach awareness faster than those that do not. We report that fearful faces gain privileged access to awareness over angry faces, but that gaze direction does not modulate this effect. Thus, our findings suggest that previously reported effects of gaze direction on emotional face processing are likely to occur once the face is detected, where the self-relevance and locus of the threat can be consciously appraised.

Peripheral threat detection in facial expressions by younger and older adults

Everyday threat detection includes recognizing threat cues in facial expressions found in our peripheral visual field. The current study examined age differences in the detection of emotion in low and high intensity angry and fearful facial expressions presented in younger and older adults’ parafoveal (±5°) and peripheral visual field (±10°, ±15°). For both age groups, detection performance was better for higher than for lower intensity stimuli, and detection performance declined with greater peripheral distance. Although younger and older adults displayed a similar pattern of findings for angry facial expressions, younger adults appeared to be more sensitive to lower intensity fearful expressions across all viewing positions. These findings demonstrate that, although threat detection may be partly maintained into older age, neurophysiological changes may accompany aging that selectively reduce older adults’ sensitivity to peripheral facial cues of fear.

Facial Reactivity and Attentional Processing of Facial Expressions and Gaze Direction

Abstract. Patterns of facial reactivity and attentional allocation to emotional facial expressions, and how these are moderated by gaze direction, are not clearly established. Among a sample of undergraduate university students, aged between 17 and 22 years (76% female), corrugator and zygomatic reactivity, as measured by facial electromyography, and attention allocation, as measured by the startle reflex and startle-elicited N100, was examined while viewing happy, neutral, angry and fearful facial expressions, which were presented at either 0- or 30-degree gaze. Results indicated typically observed facial mimicry to happy faces but, unexpectedly, “smiling” facial responses to fearful, and to a lesser extent, angry faces. This facial reactivity was not influenced by gaze direction. Furthermore, emotional facial expressions did not elicit increased attentional allocation. Likewise, matched facial expressions did not elicit increased attentional allocation. Rather, happy and fearful faces with direct (0°) gaze elicited increased controlled attentional allocation, and averted (30°) gaze faces, regardless of emotional expression, elicited preferential, early cortical processing. These findings suggest typical facial mimicry to happy faces, but unexpected facial reactivity to angry and fearful faces, perhaps due to an attempt to regulate social bonds during threat perception. Findings also suggest a divergence in controlled versus preferential, early cortical attentional processing for direct compared to averted gaze faces. These findings relate to young, mostly female, adults attending university. The experiment should be repeated with a larger sample drawn from the general community, with a broader age range and gender balance, and with a stimulus set with validated subjective valence and arousal ratings. This can reduce Type II error and establish normative patterns of facial reactivity and attentional processing of emotional facial expressions with different gaze directions.

Amygdala responds to direct gaze in real but not in computer-generated faces

Computer-generated (CG) faces are an important visual interface for human-computer interaction in social contexts. Here we investigated whether the human brain processes emotion and gaze similarly in real and carefully matched CG faces. Real faces evoked greater responses in the fusiform face area than CG faces, particularly for fearful expressions. Emotional (angry and fearful) facial expressions evoked similar activations in the amygdala in real and CG faces. Direct as compared with averted gaze elicited greater fMRI responses in the amygdala regardless of facial expression but only for real and not for CG faces. We observed an interaction effect between gaze and emotion (i.e., the shared signal effect) in the right posterior temporal sulcus and other regions, but not in the amygdala, and we found no evidence for different shared signal effects in real and CG faces. Taken together, the present findings highlight similarities (emotional processing in the amygdala) and differences (overall processing in the fusiform face area, gaze processing in the amygdala) in the neural processing of real and CG faces.

Brain response to facial expressions in adults with adolescent ADHD

The symptoms of ADHD tend to have continuity to adulthood even though the diagnostic criteria were no longer fulfilled. The aim of our study was to find out possible differences in BOLD signal in the face-processing network between adults with previous ADHD (pADHD, n = 23) and controls (n = 29) from the same birth cohort when viewing dynamic facial expressions. The brain imaging was performed using a General Electric Signa 1.5 Tesla HDX. Dynamic facial expression stimuli included happy and fearful expressions. The pADHD group demonstrated elevated activity in the left parietal area during fearful facial expression. The Network Based Statistics including multiple areas demonstrated higher functional connectivity in attention related network during visual exposure to happy faces in the pADHD group. Conclusions: We found differences in brain responses to facial emotional expressions in individuals with previous ADHD compared to control group in a number of brain regions including areas linked to processing of facial emotional expressions and attention. This might indicate that although these individuals no longer fulfill the ADHD diagnosis, they exhibit overactive network properties affecting facial processing.

Development of Human Emotion Circuits Investigated Using a Big-Data Analytic Approach: Stability, Reliability, and Robustness.

Emotion perception is fundamental to affective and cognitive development and is thought to involve distributed brain circuits. Efforts to chart neurodevelopmental changes in emotion have been severely hampered by narrowly focused approaches centered on activation of individual brain regions and small sample sizes. Here we investigate the maturation of human functional brain circuits associated with identification of fearful, angry, sad, happy, and neutral faces using a large sample of 759 children, adolescents, and adults (ages 8-23; female/male = 419/340). Network analysis of emotion-related brain circuits revealed three functional modules, encompassing lateral frontoparietal, medial prefrontal-posterior cingulate, and subcortical-posterior insular cortices, with hubs in medial prefrontal, but not posterior cingulate, cortex. This overall network architecture was stable by age 8, and it anchored maturation of circuits important for salience detection and cognitive control, as well as dissociable circuit patterns across distinct emotion categories. Our findings point to similarities and differences in functional circuits associated with identification of fearful, angry, sad, happy, and neutral faces, and reveal aspects of brain circuit organization underlying emotion perception that are stable over development as well as features that change with age. Reliability analyses demonstrated the robustness of our findings and highlighted the importance of large samples for probing functional brain circuit development. Our study emphasizes a need to focus beyond amygdala circuits and provides a robust neurodevelopmental template for investigating emotion perception and identification in psychopathology.SIGNIFICANCE STATEMENT Emotion perception is fundamental to cognitive and affective development. However, efforts to chart neurodevelopmental changes in emotion perception have been hampered by narrowly focused approaches centered on the amygdala and prefrontal cortex and small sample sizes. Using a large sample of 759 children, adolescents, and adults and a multipronged analytical strategy, we investigated the development of brain network organization underlying identification and categorization of fearful, happy, angry, sad, and neutral facial expressions. Results revealed a developmentally stable modular architecture that anchored robust age-related and emotion category-related changes in brain connectivity across multiple brain systems that extend far beyond amygdala circuits and provide a new template for investigation of emotion processing in the developing brain.

A lack of differentiation in amygdala responses to fearful expression intensity in panic disorder patients

Patients with panic disorder show abnormalities in threat processing and regulation, both on a behavioural and neural level. Better understanding of the underlying mechanisms could help to develop new treatment strategies. In this study, we investigated brain region activation in 18 patients with untreated panic disorder (PD) and 17 healthy controls (HC) during the processing of emotional faces with fearful, happy and neutral expressions, using functional MRI. The intensity of the expressions was either prototypically high, medium or low. PD patients showed significantly increased activity in the dorso-medial prefrontal cortex (dmPFC) in response to faces in general and specifically for happy faces. While HC showed a decreased amygdala response to medium/low fearful versus high fearful faces, this effect was not present in PD: amygdala activation was stable across all fearful faces in this group. Psycho-physiological interaction analyses indicated more negative connectivity between the amygdala and prefrontal areas in the PD group during the task. Amygdala activation in panic patients appears to be less sensitive to decreasing intensities of fearful facial expressions and salience monitoring areas were less active during fearful faces in general in this group. This suggests PD patients might avoid more extensive processing of fearful faces.

Effects of low- and high-intensity exercise on emotional face processing: an fMRI face-matching study.

Physical exercise has positive effects on mood and it reduces clinical depression and states of anxiety. While previous work mostly used subjective measures to study the effect of exercise upon emotions, this study for the first time employed blood oxygen level dependent functional magnetic resonance imaging (fMRI) to unravel associated neuronal changes of the emotional face-processing network in response to acute exercise. A total of 25 male athletes underwent fitness assessments to define two standardized 30 min exercise interventions (low and high intensity). The Positive and Negative Affect Schedule (PANAS) was completed pre- and post-exercise and neuronal responses to neutral, happy and fearful facial expressions were determined using an fMRI-based face-matching paradigm. Complete data sets were acquired in 21 participants (mean age, 27.2 ± 4.2 years). Both exercise interventions induced significant increases of the PANAS positive affect scale. Modulations of brain activation patterns following acute exercise were found only for fearful facial stimuli vs forms: reduced brain activation in posterior cingulate cortex/precuneus for the low condition and reduced activity in caudate nucleus and ventral anterior putamen for the high condition. In conclusion, this study provides first in vivo evidence that acute strenuous exercise interferes with emotional face-processing brain regions in an emotion type-specific manner.

'Something in the way you move': Infants are sensitive to emotions conveyed in action kinematics.

Body movements, as well as faces, communicate emotions. Research in adults has shown that the perception of action kinematics has a crucial role in understanding others' emotional experiences. Still, little is known about infants' sensitivity to body emotional expressions, since most of the research in infancy focused on faces. While there is some first evidence that infants can recognize emotions conveyed in whole-body postures, it is still an open question whether they can extract emotional information from action kinematics. We measured electromyographic (EMG) activity over the muscles involved in happy (zygomaticus major, ZM), angry (corrugator supercilii, CS) and fearful (frontalis, F) facial expressions, while 11-month-old infants observed the same action performed with either happy or angry kinematics. Results demonstrate that infants responded to angry and happy kinematics with matching facial reactions. In particular, ZM activity increased while CS activity decreased in response to happy kinematics and vice versa for angry kinematics. Our results show for the first time that infants can rely on kinematic information to pick up on the emotional content of an action. Thus, from very early in life, action kinematics represent a fundamental and powerful source of information in revealing others' emotional state.

Electrophysiological Responses to Emotional Facial Expressions Following a Mild Traumatic Brain Injury.

The present study aimed to measure neural information processing underlying emotional recognition from facial expressions in adults having sustained a mild traumatic brain injury (mTBI) as compared to healthy individuals. We thus measured early (N1, N170) and later (N2) event-related potential (ERP) components during presentation of fearful, neutral, and happy facial expressions in 10 adults with mTBI and 11 control participants. Findings indicated significant differences between groups, irrespective of emotional expression, in the early attentional stage (N1), which was altered in mTBI. The two groups showed similar perceptual integration of facial features (N170), with greater amplitude for fearful facial expressions in the right hemisphere. At a higher-level emotional discrimination stage (N2), both groups demonstrated preferential processing for fear as compared to happiness and neutrality. These findings suggest a reduced early selective attentional processing following mTBI, but no impact on the perceptual and higher-level cognitive processes stages. This study contributes to further improving our comprehension of attentional versus emotional recognition following a mild TBI.

Rapid face processing for positive and negative emotions in 5-, 7-, and 12-month-old infants: An exploratory study.

Processing of positive and negative facial expressions in infancy follows a distinct course with a bias towards fearful facial expressions starting at 7months of age; however, little is known about the developmental trajectory of fear processing and other facial expressions, and if this bias is driven by specific regions of the face. This study used eye tracking to examine the processing of positive and negative emotional faces in independent groups of 5- (n=43), 7- (n=60), and 12-month-old infants (n=70). Methods: Infants were shown static images of female faces exhibiting happy, anger, and fear expressions, for one-second each. Total looking time and looking time for areas of interest (AOIs) including forehead and eyes (top), mouth and chin (bottom), and contour of each image were computed. Infants across all ages looked longer to fear faces than angry or happy faces. Negative emotions generally elicited greater looking times for the top of the face than did happy faces. In addition, we also found that at 12months of age infants looked longer for the bottom of the faces than did 5-month-olds. Our study suggests that the visual bias to attend longer to fearful faces may be in place by 5months of age, and between 5 and 12months of age, there seems to be a developmental shift towards looking more to the bottom of the faces. STATEMENT OF CONTRIBUTION: What is already known in this subject? Bias for fear face processing is present at 7months of age. Using older data collection systems, we have some idea about which facial features recruit infant attention. What the present study adds? Well-controlled paradigm that examines both positive and negative facial expressions, to different areas of interest in the face. Use of the same paradigm to test a cross-sectional sample of infants in distinct developmental stages - 5, 7, and 12months.

Brain Responses to Faces and Facial Expressions in 5-Month-Olds: An fNIRS Study.

Processing faces and understanding facial expressions are crucial skills for social communication. In adults, basic face processing and facial emotion processing rely on specific interacting brain networks. In infancy, however, little is known about when and how these networks develop. The current study uses functional near-infrared spectroscopy (fNIRS) to measure differences in 5-month-olds’ brain activity in response to fearful and happy facial expressions. Our results show that the right occipital region responds to faces, indicating that the face processing network is activated at 5 months. Yet sensitivity to facial emotions appears to be still immature at this age: explorative analyses suggest that if the facial emotion processing network was active this would be mainly visible in the temporal cortex. Together these results indicate that at 5 months, occipital areas already show sensitivity to face processing, while the facial emotion processing network seems not fully developed.

Adrenarcheal Timing Longitudinally Predicts Anxiety Symptoms via Amygdala Connectivity During Emotion Processing

This study aimed to examine longitudinally whether adrenarcheal timing (adrenarcheal hormone levels independent of age) and tempo (change in hormone levels over time) were associated with amygdala functional connectivity and how this in turn related to anxiety symptoms in the transition from childhood to adolescence. Participants were 64 children (34 girls) who completed the Spence Children's Anxiety Scale and saliva collections to measure levels of testosterone, dehydroepiandrosterone, and dehydroepiandrosterone sulfate at two time points (mean age 9.5 years at time 1 [T1], 12.2 years at time 2 [T2]). Participants also viewed fearful and calm facial expressions while undergoing functional magnetic resonance imaging scanning at both time points. Amygdala functional connectivity was assessed with psychophysiological interaction analysis and modeled longitudinally with the Multivariate and Repeated Measures MATLAB toolbox. Controlling for age, higher dehydroepiandrosterone sulfate at T1 was related to an increase in amygdala to inferior frontal gyrus connectivity over time (T1 to T2) in boys, but the opposite pattern was found in girls. Dehydroepiandrosterone at T1 showed a positive association with amygdala connectivity to several lateral prefrontal areas and the anterior cingulate across time. Higher dehydroepiandrosterone at T1 was indirectly related to more anxiety symptoms at T2, controlling for symptoms at T1, via more positive amygdala to inferior frontal gyrus connectivity. Changes in hormone levels did not relate to changes in amygdala connectivity (from T1 to T2). The results suggest that amygdala to prefrontal cortex connectivity may be a mechanism through which early adrenarcheal timing predicts the development of anxiety symptoms during adrenarche.

Emotional Tears Communicate Sadness but Not Excessive Emotions Without Other Contextual Knowledge.

Contexts of face perception are diverse. They range from the social environment to body postures, from the expresser’s gaze direction to the tone of voice. In extending the research on contexts of face perception, we investigated people’s perception of tears on a face. The act of shedding tears is often perceived as an expression of sad feelings aroused by experiencing loss, disappointment, or helplessness. Alternatively, tears may also represent the excessive intensity of any emotion, such as extreme fear during an unexpected encounter with a giant bear and extreme happiness when you win a competition. Investigating these competing interpretations of tears, we found that the addition of tears to different facial expressions made the expressions conceptually closer to sad expressions. In particular, the results of the similarity analysis showed that, after the addition of tears, patterns of ratings for anger, fear, disgust, and neutral facial expressions became more similar to those for sadness expressions. The effect of tears on the ratings of basic emotions and their patterns in facial expressions are discussed.

Memory facilitation for emotional faces: Visual working memory trade-offs resulting from attentional preference for emotional facial expressions.

Visual working memory (VWM) for faces is facilitated when they display negative facial expressions. The present study manipulated the emotional heterogeneity of the encoding display in a change detection task to examine whether VWM is enhanced by having a separate memory store or by a bias in the allocation of limited attentional resource. When the encoding display was emotionally heterogeneous, regardless of whether happy or fearful facial expressions were presented, memory for emotional faces increased while memory for neutral faces decreased, indicating a memory trade-off. To investigate whether this occurred as a result of preferential allocation of attentional resource towards emotional expressions over neutral ones, faces were shown sequentially in different quadrants of the display. The memory trade-off between happy and neutral faces disappeared but persisted between fearful and neutral faces at trailing serial positions. When blank intervals were inserted between faces to prevent fearful faces from having prolonged processing that consumes attentional resource that should be shared with neutral faces, the memory trade-off disappeared. Findings support the argument that emotional expressions facilitate VWM due to their bias in obtaining attentional resource but the exact mechanisms through which limited resource is allocated between happy and fearful expressions may differ.

Modulation of face- and emotion-selective ERPs by the three most common types of face image manipulations.

In neuroscientific studies, the naturalness of face presentation differs; a third of published studies makes use of close-up full coloured faces, a third uses close-up grey-scaled faces and another third employs cutout grey-scaled faces. Whether and how these methodological choices affect emotion-sensitive components of the event-related brain potentials (ERPs) is yet unclear. Therefore, this pre-registered study examined ERP modulations to close-up full-coloured and grey-scaled faces as well as cutout fearful and neutral facial expressions, while attention was directed to no-face oddballs. Results revealed no interaction of face naturalness and emotion for any ERP component, but showed, however, large main effects for both factors. Specifically, fearful faces and decreasing face naturalness elicited substantially enlarged N170 and early posterior negativity amplitudes and lower face naturalness also resulted in a larger P1.This pattern reversed for the LPP, showing linear increases in LPP amplitudes with increasing naturalness. We observed no interaction of emotion with face naturalness, which suggests that face naturalness and emotion are decoded in parallel at these early stages. Researchers interested in strong modulations of early components should make use of cutout grey-scaled faces, while those interested in a pronounced late positivity should use close-up coloured faces.

Implicitly and explicitly assessed anxiety: No relationships with recognition of and brain response to facial emotions

Trait anxiety, the disposition to experience anxiety, is known to facilitate perception of threats. Trait anxious individuals seem to identify threatening stimuli such as fearful facial expressions more accurately, especially when presented under temporal constraints. In past studies on anxiety and emotion face recognition, only self-report or explicit measures of anxiety have been administered. Implicit measures represent indirect tests allowing to circumvent problems associated with self-report. In our study, we made use of implicit in addition to explicit measures to investigate the relationships of trait anxiety with recognition of and brain response to emotional faces. 75 healthy young volunteers had to identify briefly presented (67 ms) fearful, angry, happy, and neutral facial expressions masked by neutral faces while undergoing functional magnetic resonance imaging. The Implicit Association Test, the State–Trait Anxiety Inventory and the Beck Anxiety Inventory were applied as implicit and explicit measures of trait anxiety. After corrections for multiple testing, neither implicitly nor explicitly measured anxiety correlated with recognition of emotional facial expressions. Moreover, implicitly and explicitly assessed anxiety was not linked to brain response to emotional faces. Our data suggest links between discrimination accuracy and brain response to facial emotions. Activation of the caudate nucleus seems be of particular importance for recognizing fear and happiness from facial expressions. Processes of somatosensory resonance appear to be involved in identifying fear from facial expressions. The present data indicate that, regardless of assessment method, trait anxiety does not affect the recognition of fear or other emotions as has been proposed previously.

Empathy in Facial Mimicry of Fear and Disgust: Simultaneous EMG-fMRI Recordings During Observation of Static and Dynamic Facial Expressions.

Real-life faces are dynamic by nature, particularly when expressing emotion. Increasing evidence suggests that the perception of dynamic displays enhances facial mimicry and induces activation in widespread brain structures considered to be part of the mirror neuron system, a neuronal network linked to empathy. The present study is the first to investigate the relations among facial muscle responses, brain activity, and empathy traits while participants observed static and dynamic (videos) facial expressions of fear and disgust. During display presentation, blood-oxygen level-dependent (BOLD) signal as well as muscle reactions of the corrugator supercilii and levator labii were recorded simultaneously from 46 healthy individuals (21 females). It was shown that both fear and disgust faces caused activity in the corrugator supercilii muscle, while perception of disgust produced facial activity additionally in the levator labii muscle, supporting a specific pattern of facial mimicry for these emotions. Moreover, individuals with higher, compared to individuals with lower, empathy traits showed greater activity in the corrugator supercilii and levator labii muscles; however, these responses were not differentiable between static and dynamic mode. Conversely, neuroimaging data revealed motion and emotional-related brain structures in response to dynamic rather than static stimuli among high empathy individuals. In line with this, there was a correlation between electromyography (EMG) responses and brain activity suggesting that the Mirror Neuron System, the anterior insula and the amygdala might constitute the neural correlates of automatic facial mimicry for fear and disgust. These results revealed that the dynamic property of (emotional) stimuli facilitates the emotional-related processing of facial expressions, especially among whose with high trait empathy.

Genetic Correlation between Child Callous-Unemotional Behaviors and Fear Recognition Deficit: Evidence for a Neurocognitive Endophenotype.

This study investigates emotion recognition deficits as candidate neurocognitive endophenotypes for callous-unemotional (CU) behaviors. Using a twin design, we tested genetic correlations between child CU behaviors and poor processing of fearful and sad facial expressions. Participants were 504 twin pairs (209 MZ pairs; 295 DZ pairs) from the Quebec Newborn Twin Study, a longitudinal study of a population-based sample of twins. Teachers in kindergarten and first grade rated children's CU behaviors and other behavior problems (attention deficit and hyperactivity symptoms, physical aggression, and depressive symptoms). In first grade (mean age 7years), the children completed the visual subtest of the Diagnostic Analysis of Nonverbal Accuracy Scale 2 (DANVA-II) to assess emotion recognition from facial stimuli. Using structural equation modeling, we examined the genetic-environmental etiology of the association between fear/sadness recognition and child CU behaviors, controlling for other behavior problems and recognition of other emotions. We found a significant genetic correlation between poor fear recognition and CU behaviors that was independent of other behavior problems. Poor recognition of sadness was not significantly associated with CU behaviors after taking into account other behavior problems. Our results suggest that CU behaviors and fear recognition have a partly shared genetic aetiology. This provides support for poor fear recognition as a key neurocognitive endophenotype for CU behaviors. Future research should test a hypothesized causal chain from specific genes, through amygdala functioning and fear recognition, to CU behaviors, and identify specific environmental factors (including intervention) that may disrupt this chain.