Children's processing of emotions expressed by peers and adults: An fMRI study

The recognition of emotional expressions is an important skill and relates to social functioning and adjustment in childhood. The current functional MRI study investigated the neural processing of angry and happy facial expressions in 5- to 6-year-old children and in adults. Participants were presented happy and angry faces of adults and children while they performed a non-emotion-related task with low cognitive load. Very similar neural networks were involved in the processing of angry and happy faces in adults and children, including the amygdala and prefrontal areas. In general, children showed heightened amygdala activation in response to emotional faces relative to adults. While children showed stronger amygdala activation in response to angry adult compared to angry child faces, adults showed stronger amygdala activation for angry child faces. In both age groups enhanced amygdala involvement was found for happy peer faces relative to happy non-peer faces, though this effect was only a tendency in adults. The findings are discussed in the context of the development of the social brain network.     

Post-learning intranasal oxytocin modulates human memory for facial identity

The nanopeptide oxytocin has physiological functions during labour and lactation. In addition, oxytocin is known to modulate aggression, anxiety, social behaviour and cognition. Little is known about its effects on memory for emotional stimuli. In the present single-blind, placebo-controlled, randomised study we have investigated the short- and long-term effects of a single post-learning dose (20 IU) of intranasal oxytocin on memory for facial identity and expression in 36 healthy young females and males using a face portrait recognition test. In the acquisition phase of the test, 60 different male faces with happy, angry or neutral expressions were presented to the volunteers. Thirty minutes and 24h after oxytocin administration, recognition memory tests were performed using portraits with neutral facial expressions, only. Oxytocin improved identity recognition memory independently of participant's gender, for neutral and angry faces, whereas this effect was not present for happy faces. Oxytocin-treated subjects had a lower bias to judge not previously seen faces as being previously seen. Oxytocin had no effect on facial expression memory. In conclusion, oxytocin has distinct effects on memory performance for facial identity and may contribute to the modulation of social behaviour.     

The changing face of emotion: age-related patterns of amygdala activation to salient faces

The present study investigated age-related differences in the amygdala and other nodes of face-processing networks in response to facial expression and familiarity. fMRI data were analyzed from 31 children (3.5–8.5 years) and 14 young adults (18–33 years) who viewed pictures of familiar (mothers) and unfamiliar emotional faces. Results showed that amygdala activation for faces over a scrambled image baseline increased with age. Children, but not adults, showed greater amygdala activation to happy than angry faces; in addition, amygdala activation for angry faces increased with age. In keeping with growing evidence of a positivity bias in young children, our data suggest that children find happy faces to be more salient or meaningful than angry faces. Both children and adults showed preferential activation to mothers’ over strangers’ faces in a region of rostral anterior cingulate cortex associated with self-evaluation, suggesting that some nodes in frontal evaluative networks are active early in development. This study presents novel data on neural correlates of face processing in childhood and indicates that preferential amygdala activation for emotional expressions changes with age.     

Emotional face processing deficit in schizophrenia: A replication study in a South African Xhosa population

Schizophrenia is associated with a deficit in the recognition of negative emotions from facial expressions. The present study examined the universality of this finding by studying facial expression recognition in African Xhosa population. Forty-four Xhosa patients with schizophrenia and forty healthy controls were tested with a computerized task requiring rapid perceptual discrimination of matched positive (i.e. happy), negative (i.e. angry), and neutral faces. Patients were equally accurate as controls in recognizing happy faces but showed a marked impairment in recognition of angry faces. The impairment was particularly pronounced for high-intensity (open-mouth) angry faces. Patients also exhibited more false happy and angry responses to neutral faces than controls. No correlation between level of education or illness duration and emotion recognition was found but the deficit in the recognition of negative emotions was more pronounced in familial compared to non-familial cases of schizophrenia. These findings suggest that the deficit in the recognition of negative facial expressions may constitute a universal neurocognitive marker of schizophrenia.     

Electrophysiological correlates of improved short-term memory for emotional faces

Long-term memory (LTM) is enhanced for emotional information, but the influence of stimulus emotionality on short-term memory (STM) is less clear. We examined the electrophysiological correlates of improved visual STM for emotional face identity, focusing on the P1, N170, P3b and N250r event-related potential (ERP) components. These correlates are taken to indicate which memory processing stages and cognitive processes contribute to the improved STM for emotional face identity. In the encoding phase, one or three angry, happy or neutral faces were presented for 2 s, resulting in a memory load of one or three. The subsequent 1-s retention phase was followed by a 2-s retrieval phase, in which participants indicated whether a probe face had been present or not during encoding. Memory performance was superior for angry and happy faces over neutral faces at load three. None of the ERP components during encoding were affected by facial expression. During retrieval, the early P3b was decreased for emotional compared to neutral faces, which presumably reflects greater resource allocation to the maintenance of the emotional faces. Furthermore, the N250r during retrieval was increased for emotional compared to neutral faces, reflecting an enhanced repetition effect for emotional faces. These findings suggest that enhanced visual STM for emotional faces arises from improved maintenance and from improved detection of face repetition at retrieval.     

The effects of angry and happy expressions on recognition memory for unfamiliar faces in delusion-prone individuals

Numerous studies suggest a cognitive bias for threat-related material in delusional ideation. However, few studies have examined this bias using a memory task. We investigated the influence of delusion-proneness on identity and expression memory for angry and happy faces. Participants high and low in delusion-proneness were presented with happy and angry faces and were later asked to recognise the same faces displaying a neutral expression. They also had to remember what the initial expressions of the faces had been. Remember/know/guess judgments were asked for both identity and expression memory. Results showed that delusion-prone participants better recognised the identity of angry faces compared to non-delusional participants. Also, this difference between the two groups was mainly due to a greater number of remember responses in delusion-prone participants. These findings extend previous studies by showing that delusions are associated with a memory bias for threat-related stimuli.     

Age‐related changes in amygdala–frontal connectivity during emotional face processing from childhood into young adulthood

The ability to process and respond to emotional facial expressions is a critical skill for healthy social and emotional development. There has been growing interest in understanding the neural circuitry underlying development of emotional processing, with previous research implicating functional connectivity between amygdala and frontal regions. However, existing work has focused on threatening emotional faces, raising questions regarding the extent to which these developmental patterns are specific to threat or to emotional face processing more broadly. In the current study, we examined age‐related changes in brain activity and amygdala functional connectivity during an fMRI emotional face matching task (including angry, fearful, and happy faces) in 61 healthy subjects aged 7–25 years. We found age‐related decreases in ventral medial prefrontal cortex activity in response to happy faces but not to angry or fearful faces, and an age‐related change (shifting from positive to negative correlation) in amygdala–anterior cingulate cortex/medial prefrontal cortex (ACC/mPFC) functional connectivity to all emotional faces. Specifically, positive correlations between amygdala and ACC/mPFC in children changed to negative correlations in adults, which may suggest early emergence of bottom‐up amygdala excitatory signaling to ACC/mPFC in children and later development of top‐down inhibitory control of ACC/mPFC over amygdala in adults. Age‐related changes in amygdala–ACC/mPFC connectivity did not vary for processing of different facial emotions, suggesting changes in amygdala–ACC/mPFC connectivity may underlie development of broad emotional processing, rather than threat‐specific processing. Hum Brain Mapp 37:1684–1695, 2016. © 2016 Wiley Periodicals, Inc .     

Age and cortisol levels modulate judgment of positive and negative facial expressions

There is some evidence that older adults respond to emotional stimuli differently to young adults, and that they may exhibit better performance on measures of memory and attention when stimuli are positive rather than negative in valence. A relation between cortisol levels and attention/memory for emotional stimuli in young adults has also been reported. The relationship between cortisol levels and the judgment of facial expressions of emotion in aging, however, has yet to be explored. The aim of this study was to investigate performance on a simple emotional face judgment task in young (N=37) and middle-aged (N=37) adults in association with salivary cortisol levels. Middle-aged participants were slower in responding to stimuli than younger participants. Cortisol levels were found to be associated with shorter response latencies to categorise emotional but not neutral faces, and with a greater tendency to judge neutral faces as being emotional. An interaction between age and cortisol levels emerged in response to angry faces; such that higher cortisol levels predicted significantly shorter reaction times to angry faces in young adults, but not in middle-aged adults. Thus, cortisol may be differently related to the processing of emotional facial expressions, particularly of anger, in middle-aged and young individuals. The findings are discussed in relation to the hypothesised changes in emotion regulation with aging.     

Neural responses to happy,fearful and angry faces of varying identities in 5- and 7-month-old infants

The processing of facial emotion is an important social skill that develops throughout infancy and early childhood. Here we investigate the neural underpinnings of the ability to process facial emotion across changes in facial identity in cross-sectional groups of 5- and 7-month-old infants. We simultaneously measured neural metabolic, behavioral, and autonomic responses to happy, fearful, and angry faces of different female models using functional near-infrared spectroscopy (fNIRS), eye-tracking, and heart rate measures. We observed significant neural activation to these facial emotions in a distributed set of frontal and temporal brain regions, and longer looking to the mouth region of angry faces compared to happy and fearful faces. No differences in looking behavior or neural activations were observed between 5- and 7-month-olds, although several exploratory, age-independent associations between neural activations and looking behavior were noted. Overall, these findings suggest more developmental stability than previously thought in responses to emotional facial expressions of varying identities between 5- and 7-months of age.     

Exogenous cortisol shifts a motivated bias from fear to anger in spatial working memory for facial expressions

Studies assessing processing of facial expressions have established that cortisol levels, emotional traits, and affective disorders predict selective responding to these motivationally relevant stimuli in expression specific manners. For instance, increased attentional processing of fearful faces (attentional bias for fearful faces) is associated with fear and anxiety and diminishes after administration of the anxiolytic hormone testosterone. Conversely, attentional bias for angry faces has been associated with higher levels of approach motivation (e.g. anger) and testosterone, but lower levels of cortisol. This negative relation between cortisol levels and bias for angry faces was also seen in a test of biased working memory performance. However, previous research suggests that exogenous glucocorticoids acutely decrease fearful and inhibited behavior and increase aggressiveness. Hypothesizing from these findings, the present study tested this spatial working memory for faces of various emotional expressions (neutral, happy, fearful, and angry) after double-blind, placebo-controlled administration of 40 mg cortisol in 18 healthy young men. It was predicted that cortisol would acutely attenuate memory bias for fearful expressions while increasing memory bias for angry expressions, in effect creating a shift in biased motivated memory from fear to anger. Results largely confirmed the hypotheses. This is the first causal evidence that cortisol differentially regulates spatial working memory for different facial expressions. Possible biological mechanisms are discussed.     

Attentionally modulated effects of cortisol and mood on memory for emotional faces in healthy young males

Heightened cortisol levels due to stress or acute administration seem to enhance memory for emotional material, independently of emotional valence. An arousal-driven neurobiological mechanism involving the amygdala has been proposed. The relation between pre-task salivary measures of cortisol (by convention named 'basal levels') and emotionally modulated memory has not been investigated yet. Given the association between higher basal levels of cortisol and indices of low mood, valence-specific effects on emotionally modulated memory could be expected (e.g. mood-congruent or stimulus-specific forms of processing). This study was designed to investigate the relationship between basal levels of salivary cortisol, self-reported mood and spatial memory for neutral, happy and angry facial expressions in healthy young volunteers (N=31). Memory performance was indexed using a modified version of a computerized object-relocation task, using emotional facial expressions as stimuli. Results showed a significant relation between cortisol and depressive mood. More importantly, both the levels of cortisol and depressive mood were inversely related to the memory performance for the happy facial expressions, while a similar relationship between cortisol and memory performance on angry faces neared significance. An explanation in terms of the down-regulation of social behavior by elevated basal cortisol levels is postulated.     

Simultaneous recording of EEG and facial muscle reactions during spontaneous emotional mimicry

The perception of emotional facial expressions induces covert imitation in emotion-specific muscles of the perceiver's face. Neural processes involved in these spontaneous facial reactions remain largely unknown. Here we concurrently recorded EEG and facial EMG in 15 participants watching short movie clips displaying either happy or angry facial expressions. EMG activity was recorded for the zygomaticus major (ZM) that elevates the lips during a smile, and the corrugator supercillii (CS) that knits the eyebrows during a frown. We found increased EMG activity of CS in response to angry expressions, and enhanced EMG activity of ZM for happy expressions, replicating earlier EMG studies. More importantly, we found that the amplitude of an early visual evoked potential (right P1) was larger when ZM activity to happy faces was high, and when CS activity to angry faces was high, as compared to when muscle reactions were low. Conversely, the amplitude of right N170 component was smaller when the intensity of facial imitation was high. These combined EEG-EMG results suggest that early visual processing of face expression may determine the magnitude of subsequent facial imitation, with dissociable effects for P1 and N170. These findings are discussed against the classical dual-route model of face recognition.     

Facial-affect recognition in normal preschool children and in senile elderly persons

The performance of senile elderly persons and of young children was compared on an identical facial affect recognition test. The senile persons were disoriented with impaired recent memory. However, their neurological functioning in visual, perceptual, verbal, and motor processing required for the testing was intact. The children were divided into age groups of 3, 3 1/2, 4, 4 1/2, and 5. Pictures of happy, sad, and angry faces were shown and the subjects were tested for their ability to discriminate between the emotions by the use of prompting and oddity procedures. The very young children (ages 3 and 3 1/2) were found to be at a deficit in recognizing facial expressions, particularly with regard to the recognition of sad faces. The children's recognition level improved as a function of age. The senile persons were found to be significantly more impaired than even the youngest group of children, particularly with regard to the recognition of angry faces. While the children attempted to distinguish between the stimuli on the basis of affect, the seniles tended to "feature-detect", because their facial feature recognition ability remained relatively intact. Thus the impairment of facial affect recognition in senility was quite unlike that of younger children. The extensive deterioration of senile patients in facial affect recognition ability is remarkable and has important therapeutic implications. Since these patients still maintain high level of verbal comprehension, clear verbal expression of our feelings toward them is essential.     

Recognition advantage of happy faces: Tracing the neurocognitive processes

The present study aimed to identify the brain processes—and their time course—underlying the typical behavioral recognition advantage of happy facial expressions. To this end, we recorded EEG activity during an expression categorization task for happy, angry, fearful, sad, and neutral faces, and the correlation between event-related-potential (ERP) patterns and recognition performance was assessed. N170 (150–180 ms) was enhanced for angry, fearful and sad faces; N2 was reduced and early posterior negativity (EPN; both, 200–320 ms) was enhanced for happy and angry faces; P3b (350–450 ms) was reduced for happy and neutral faces; and slow positive wave (SPW; 700–800 ms) was reduced for happy faces. This reveals (a) an early processing (N170) of negative affective valence (i.e., angry, fearful, and sad), (b) discrimination (N2 and EPN) of affective intensity or arousal (i.e., angry and happy), and (c) facilitated categorization (P3b) and decision (SPW) due to expressive distinctiveness (i.e., happy). In addition, N2, EPN, P3b, and SPW were related to categorization accuracy and speed. This suggests that conscious expression recognition and the typical happy face advantage depend on encoding of expressive intensity and, especially, on later response selection, rather than on the early processing of affective valence.     

Effects of alcohol on ratings of emotional facial expressions in social phobics

Social phobics have an increased risk of alcoholism. The mechanism behind this co-morbidity is not well understood. According to the appraisal-disruption model [Sayette, M. A. (1993). An appraisal-disruption model of alcohol's effects on stress responses in social drinkers. Psychological Bulletin, 114, 459-476], alcohol disrupts appraisal of threat stimuli unless the stimuli are easy to process. We investigated whether alcohol alters the judgment of emotional facial expressions in social phobics and controls. We also tested the judgment of emotionally ambiguous faces which should be more difficult to process. Forty social phobics and controls rated faces depicting five emotional expressions on an animosity rating scale. For two ambiguous facial expressions, angry, respectively, happy faces were blended with neutral faces. Half of the participants consumed alcohol. Socially phobic participants rated neutral and happy facial expressions as less friendly than controls, irrespective of alcohol consumption. In both groups, consuming alcohol reduced the perceived rejection of angry faces. In line with current theories of social phobia, patients interpreted neutral facial expressions as more rejecting than controls. The rejection perceived in explicitly angry facial expressions was less after drinking alcohol. This reduction of the adversity of socially threatening stimuli by alcohol might act as negative reinforcement and thus contributes to alcohol problems.     

Neural activation during encoding of emotional faces in pediatric bipolar disorder

OBJECTIVE: Neurobiological understanding of bipolar disorder (BD) is limited by a paucity of functional magnetic resonance imaging (fMRI) research examining correlates of psychological processes. To begin to address these limitations, the current study tests the hypothesis that pediatric BD (PBD) subjects exhibit altered neural activation during encoding of emotional faces compared to typically developing controls. METHODS: Pediatric BD subjects (n=23; mean age=14.2+/-3.1 years) and controls (n=22; mean age=14.7+/-2.3 years) were matched on age, gender, and IQ. In this event-related fMRI study, subjects were scanned while viewing emotional faces and given a surprise recognition memory test 30 min postscan. Our main outcome measure was between-group differences in neural activation during successful versus unsuccessful face encoding. RESULTS: Pediatric BD youth exhibited reduced memory for emotional faces, relative to healthy comparisons, particularly on fearful faces. Event-related fMRI analyses controlling for this behavioral difference showed that PBD subjects, compared to controls, had increased neural activation in the striatum and anterior cingulate cortex when successfully encoding happy faces and in the orbitofrontal cortex when successfully encoding angry faces. There were no between-group differences in neural activation during fearful face encoding. CONCLUSIONS: Our results extend what is known about memory and face emotion processing impairments in PBD subjects by showing increased fronto-striatal activation during encoding of emotional faces. Further work is required to determine the impact of mood state, medication, and comorbid illnesses on these findings.     

Facial perception bias in patients with major depression

This study used a morphed categorical perception facial expression task to evaluate whether patients with depression demonstrated deficits in distinguishing boundaries between emotions. Forty-one patients with depression and 41 healthy controls took part in this study. They were administered a standardized set of morphed photographs of facial expressions with varying emotional intensities between 0% and 100% of the emotion, in 10% increments to provide a range of intensities from pleasant to unpleasant(e.g. happy to sad, happy to angry) and approach-avoidance (e.g. angry to fearful). Compared with healthy controls, the patients with depression demonstrated a rapid perception of sad expressions in happy-sad emotional continuum and demonstrated a rapid perception of angry expressions in angry-fearful emotional continuum. In addition, when facial expressions shifted from happy to angry, the depressed patients had a clear demarcation for the happy-angry continuum. Depressed patients had a perceptual bias towards unpleasant versus pleasant expressions and the hypersensitivity to angry facial signals might influence the interaction behaviors between depressed patients and others.     

Visual and auditory affect recognition in senile and normal elderly persons

Senile patients were compared to normal elderly people for visual and auditory affect recognition. The study consisted of eight conditions, with the subjects prompted verbally to point to happy, sad and angry pictures in the first five. The pictures consisted of expressive faces, expressive postures with blank faces and matching facial and postural expressions in Conditions 1-3, respectively. The facial and postural expressions conflicted in Conditions 4 and 5, with the facial expressions redundant in Condition 4 and the postures redundant in Condition 5. Conditions 6 and 7 were the same as the first two, except that the subjects were prompted by use of taped, affective voice intonations. In Condition 8, the subjects were requested to identify each of the affectively intoned prompts. The findings revealed a consistent level difference between the groups, with the senile elderly demonstrating both visual and auditory affective agnosia. These impairments in emotional recognition were affect-specific and they tended to confound one another. Finally, there was a subgroup of normals that was somewhat deficient in visual and auditory affect recognition.     

Psychophysiological correlates of face processing in social phobia

Social phobia has been associated with abnormal processing of angry faces, which directly signal disapproval--a situation that social phobics fear. This study investigated the electrophysiological correlates of emotional face processing in socially phobic and non-phobic individuals. Subjects identified either the gender (modified emotional Stroop task) or the expression of angry, happy, or neutral faces. Social phobics showed no deviations from controls in reaction times, heart rates, P1, or P2 amplitudes in response to angry faces, although elevated FSS scores were associated with higher P1 amplitudes in social phobic persons. In addition, social phobic persons showed enhanced right temporo-parietal N170 amplitudes in response to angry faces in the emotion identification task. Furthermore, higher scores on the Social Phobia and Anxiety Inventory (SPAI) were associated as a trend with larger N170 amplitudes in response to angry faces in the emotion identification task. Thus, the present results suggest that social phobics show abnormalities in the early visual processing of angry faces, as reflected by the enhanced right-hemispheric N170 when the emotion of the angry face was the focus of attention, while behavioral responses and heart rates showed no evidence for preferred processing of angry facial expressions.     

Functional brain networks involved in gaze and emotional processing

Eye‐gaze direction plays a fundamental role in the perception of facial features and particularly the processing of emotional facial expressions. Yet, the neural underpinnings of the integration of eye gaze and emotional facial cues are not well understood. The primary aim of this study was to delineate the functional networks that subserve the recognition of emotional expressions as a function of eye gaze. Participants were asked to identify happy, angry, or neutral faces, displayed with direct or averted gaze, while their neural responses were measured with fMRI. The results showed that recognition of happy expressions, irrespective of eye‐gaze direction, engaged the critical nodes of the default mode network. Recognition of angry faces, on the other hand, was gaze‐dependent, engaging the critical nodes of the salience network when presented with direct gaze, but fronto‐parietal areas when presented with averted gaze. Functional connectivity analysis further showed gaze‐dependent engagement of a large‐scale network connected to bilateral amygdala during the recognition of angry expressions. This study provides important insights into the functional connectivity between the amygdala and other critical social‐cognitive brain nodes, which are essential in processing of ambiguous, potentially threatening social signals. These findings have implications for psychiatric disorders, such as post‐traumatic stress disorder, which are characterized by aberrant limbic connectivity.