Common and distinct brain activation to threat and safety signals in social phobia

BACKGROUND: Little is known about the functional neuroanatomy underlying the processing of emotional stimuli in social phobia. OBJECTIVES: To investigate specific brain activation that is associated with the processing of threat and safety signals in social phobics. METHODS: Using functional magnetic resonance imaging, brain activation was measured in social phobic and nonphobic subjects during the presentation of angry, happy and neutral facial expressions under free viewing conditions. RESULTS: Compared to controls, phobics showed increased activation of extrastriate visual cortex regardless of facial expression. Angry, but not neutral or happy, faces elicited greater insula responses in phobics. In contrast, both angry and happy faces led to increased amygdala activation in phobics. CONCLUSIONS: The results support the hypothesis that the amygdala is involved in the processing of negative and positive stimuli. Furthermore, social phobics respond sensitively not only to threatening but also to accepting faces and common and distinct neural mechanisms appear to be associated with the processing of threat versus safety signals.     

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.     

Effect of task conditions on brain responses to threatening faces in social phobics: an event-related functional magnetic resonance imaging study.

BACKGROUND: The aim of this study was to identify brain activation to socially threatening stimuli in social phobic subjects during different experimental conditions. METHODS: With event-related functional magnetic resonance imaging, brain activation to photographs and schematic pictures depicting angry or neutral facial expressions was measured in social phobic subjects and healthy control subjects, while subjects assessed either emotional expression (angry vs. neutral; explicit task) or picture type (photographic vs. schematic; implicit task). RESULTS: Compared with control subjects, phobics showed greater responses to angry than to neutral photographic faces in the insula regardless of task, whereas amygdala, parahippocampal gyrus, and extrastriate visual cortex were more strongly activated only during the implicit task. Phobics, in contrast to control subjects, showed similar activation patterns during both tasks. For schematic angry versus neutral faces, activation of insula and extrastriate visual cortex was found in phobics, but not in control subjects, during both tasks. CONCLUSIONS: Differences between social phobics and control subjects in brain responses to socially threatening faces are most pronounced when facial expression is task-irrelevant. Phobics intensively process angry (photographic as well as schematic) facial expressions, regardless of whether this is required. The insula plays a unique role in the processing of threat signals by social phobics.     

Time-course of attention biases in social phobia

Theoretical models of social phobia implicate preferential attention to social threat in the maintenance of anxiety symptoms, though there has been limited work characterizing the nature of these biases over time. The current study utilized eye-movement data to examine the time-course of visual attention over 1500 ms trials of a probe detection task. Nineteen participants with a primary diagnosis of social phobia based on DSM-IV criteria and 20 non-clinical controls completed this task with angry, fearful, and happy face trials. Overt visual attention to the emotional and neutral faces was measured in 50 ms segments across the trial. Over time, participants with social phobia attend less to emotional faces and specifically less to happy faces compared to controls. Further, attention to emotional relative to neutral expressions did not vary notably by emotion for participants with social phobia, but control participants showed a pattern after 1000 ms in which over time they preferentially attended to happy expressions and avoided negative expressions. Findings highlight the importance of considering attention biases to positive stimuli as well as the pattern of attention between groups. These results suggest that attention “bias” in social phobia may be driven by a relative lack of the biases seen in non-anxious participants.     

Oxytocin increases recognition of masked emotional faces

The neuropeptide oxytocin has been shown to improve many aspects of social cognitive functioning, including facial emotion recognition, and to promote social approach behaviour. In the present study, we investigated the modulatory effects of oxytocin on the recognition of briefly presented facial expressions. In order to diversify the degree of visual awareness for the facial stimuli, presentation duration was systematically varied. Fifty-six participants were administered intranasal oxytocin or a placebo in a double-blind, randomized, between-subjects design. Participants viewed angry and happy target faces or neutral distractors for 18, 35, or 53 ms subsequently masked by neutral faces. Participants had to indicate the presence or absence of the briefly presented target face. Discrimination indices (d') showed that oxytocin generally enhanced detection accuracy of emotional stimuli. This effect was more pronounced for the recognition of happy faces. We provide evidence that a single dose of intranasally administered oxytocin enhances detection of briefly presented emotional stimuli. The possible role of stimulus valence and recognition difficulty is discussed.     

Perceptual bias of patients with schizophrenia in morphed facial expression

Limited research has specifically examined the nature of the dysfunction in emotion categorization representation in schizophrenia. The current study aimed to investigate the perception bias of morphed facial expression in subjects with schizophrenia and healthy controls in the emotion continua. Twenty-eight patients with schizophrenia and thirty-one 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 and approach to withdraw. Shift points, indicating the time point that the subjects’ emotion identification begins to change, and response slopes, indicating how rapidly these changes have happened at the shift points in the emotion continuum, were measured. Patients exhibited a significantly greater response slope (i.e., patients’ perception changed more rapidly) and greater shift point (i.e., patients still perceived mild expressions of anger as happy faces) with increasing emotion signal compared with healthy controls when the facial expression morphed from happy to angry. Furthermore, patients with schizophrenia still perceived mild expressions of fear as angry faces(a greater shift point) and were less discriminative from angry to fearful emotion(a flatter response slope). They were sensitive to sadness (a smaller shift point) and the perception changed rapidly (a sharper response slope) as compared with healthy controls in the emotion continuum of happy to sad. In conclusion, patients with schizophrenia demonstrated impaired categorical perception of facial expressions, with generally ‘rapid’ but ‘late’ discrimination towards social threat-related stimuli such as angry facial expression. Compared with healthy controls, these patients have a sharper discrimination perception pattern in the emotion continua from positive valence to negative valence.     

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.     

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.     

Emotional facial expressions capture attention

OBJECTIVE: To determine whether the emotional significance of stimuli can influence spatial attention. BACKGROUND: Motivational and emotional factors may affect attention toward stimuli. However, this has never been examined in brain-damaged patients who present with unilateral inattention due to left spatial neglect. METHODS: The authors studied three patients with chronic left neglect and visual extinction after right parietal stroke. Shapes or faces with neutral, happy, or angry expressions were briefly presented in the right, left, or both visual fields. On unilateral trials, the patients detected all stimuli equally on both sides. On bilateral trials, they extinguished faces in the contralesional field much less often than shapes, and faces with happy or angry facial expressions much less than faces with a neutral expression. CONCLUSION: Facial features and emotional expressions can be analyzed despite lying on the unattended side, and may influence the spatial distribution of attention. These findings support the view that attention is controlled by neural mechanisms involving not only frontoparietal areas but also limbic components in cingulate cortex and amygdala, which may interact with ventral visual areas in the temporal lobe to detect affective value and prioritize attention to salient stimuli.     

Enhanced amygdala responses to emotional versus neutral schematic facial expressions

Human facial emotional expressions are complex. This may confound studies examining brain responses to these stimuli in control and clinical populations. However, several lines of evidence suggest that a few elementary facial features convey the gist of emotional expressions. Using fMRI, we assessed brain responses to line drawings of emotionally valenced (i.e. angry and happy) and neutral faces in healthy human subjects. Significantly increased fMRI signal was found in the amygdala, hippocampus and prefrontal cortex in response to emotional vs neutral schematic faces. Although direct comparisons of schematic and human faces will be needed, these initial results suggest that schematic faces may be useful for studying brain responses to emotional stimuli because of their simplicity relative to human faces.     

Fear of negative evaluation and the hypervigilance-avoidance hypothesis: an eye-tracking study

The hypervigilance-avoidance hypothesis assumes that anxious individuals initially attend to and subsequently avoid threatening stimuli. In this study pairs of emotional (angry or happy) and neutral facial expressions were presented to students of high or low fear of negative evaluation (FNE) while their eye movements were recorded. High FNE participants initially looked more often at emotional compared to neutral faces, indicating an attentional bias for emotional facial expressions. This effect was further modulated by the sex of the face, as high FNE clearly showed a preference for happy female faces. Analysis of the time course of attention revealed that high FNE looked at the emotional faces longer during the first second of stimulus exposure, whereas they avoided these faces in the consecutive time interval from 1 to 1.5 s. These results partially support the hypervigilance-avoidance hypothesis and additionally indicate the relevance of happy faces for high FNE. Further research should clarify the meaning of happy facial expressions as well as the influence of the sex of the observed face in social anxiety.

Age determines memory for face identity and expression

Background: The recognition of facial expressions is an important component of emotion processing which contributes to interactional behavior. One of the factors highly associated with potential decline of ability in behavioral tasks is age. Methods: We have investigated age‐related changes in facial identity and expression memory of healthy subjects in three age groups: young adults (20–40 years), elderly adults (60–80 years) and, for the first time in the literature, very old adults (over 80 years of age). Using a picture test, photographs of faces with happy or angry expressions were presented to study participants during the encoding task, and the memory for identity and emotional facial expression was investigated in a subsequent recognition task showing emotionally neutral faces. Half of the faces presented in the recognition task were initially shown in the encoding task. Results: Age interacted with the memory process: the ability to recognize both facial identity and emotional expression declined with advanced age. Happy facial expressions were better recognized in all age groups. Although there was a continuous overall decrease in recognition of both happy and angry expressions with advanced age, the effect favoring happy facial expressions was stable also in very old adults. Other factors such as gender or educational level did not affect the memory process for facial expressions. Conclusions: Our findings suggest that age is a significant determinant of memory for facial identity and emotional expression, and that, similar to younger adults, the recognition process of the elderly favors happy emotional 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.     

Atypical spatiotemporal activation of cerebellar lobules during emotional face processing in adolescents with autism

Autism spectrum disorder (ASD) is characterized by social deficits and atypical facial processing of emotional expressions. The underlying neuropathology of these abnormalities is still unclear. Recent studies implicate cerebellum in emotional processing; other studies show cerebellar abnormalities in ASD. Here, we elucidate the spatiotemporal activation of cerebellar lobules in ASD during emotional processing of happy and angry faces in adolescents with ASD and typically developing (TD) controls. Using magnetoencephalography, we calculated dynamic statistical parametric maps across a period of 500 ms after emotional stimuli onset and determined differences between group activity to happy and angry emotions. Following happy face presentation, adolescents with ASD exhibited only left‐hemispheric cerebellar activation in a cluster extending from lobule VI to lobule V (compared to TD controls). Following angry face presentation, adolescents with ASD exhibited only midline cerebellar activation (posterior IX vermis). Our findings indicate an early (125–175 ms) overactivation in cerebellar activity only for happy faces and a later overactivation for both happy (250–450 ms) and angry (250–350 ms) faces in adolescents with ASD. The prioritized hemispheric activity (happy faces) could reflect the promotion of a more flexible and adaptive social behavior, while the latter midline activity (angry faces) may guide conforming behavior.     

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.     

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.     

Emotional facial expressions modulate pain-induced beta and gamma oscillations in sensorimotor cortex

Painful events in our environment are often accompanied by stimuli from other sensory modalities. These stimuli may influence the perception and processing of acute pain, in particular when they comprise emotional cues, like facial expressions of people surrounding us. In this whole-head magnetoencephalography (MEG) study, we examined the neuronal mechanisms underlying the influence of emotional (fearful, angry, or happy) compared to neutral facial expressions on the processing of pain in humans. Independent of their valence, subjective pain ratings for intracutaneous inputs were higher when pain stimuli were presented together with emotional facial expressions than when they were presented with a neutral facial expression. Source reconstruction using linear beamforming revealed pain-induced early (70-270 ms) oscillatory beta-band activity (BBA; 15-25 Hz) and gamma-band activity (GBA; 60-80 Hz) in the sensorimotor cortex. The presentation of faces with emotional expressions compared to faces with neutral expressions led to a stronger bilateral suppression of the pain-induced BBA, possibly reflecting enhanced response readiness of the sensorimotor system. Moreover, pain-induced GBA in the sensorimotor cortex was larger for faces expressing fear than for faces expressing anger, which might reflect the facilitation of avoidance-motivated behavior triggered by the concurrent presentation of faces with fearful expressions and painful stimuli. Thus, the presence of emotional cues, like facial expressions from people surrounding us, while receiving acute pain may facilitate neuronal processes involved in the preparation and execution of adequate protective motor responses.     

More excited for negative facial expressions in depression: Evidence from an event-related potential study

Objective

This study aims to investigate the intensity evaluation of social stimuli in depression.

Methods

Twenty-four never-disordered control participants (NC), 24 sub-clinically depressed individuals and 24 participants diagnosed with a current major depressive disorder (MDD) were recruited. All participants completed an emotional intensity evaluation task, in which they were required to judge the intensity of the facial expressions by pressing response keys, with the event-related potential (ERP) being recorded during the process.

Results

The MDD participants had higher intensity scores for sad faces compared with the NC group, longer reaction times (RTs) for all faces compared with other groups and higher P1 and P2 amplitude for sad faces compared with other faces. The sub-clinically depressed individuals had lower intensity scores for happy and neutral faces compared with other groups, longer RTs for happy faces compared with other faces and higher P1 and P2 amplitudes for happy faces compared with sad faces.

Conclusion

The findings suggest that the MDD participants are more excited for negative facial expressions, while the sub-clinically depressed individuals might have a disturbed perception for happy stimuli, which suggests a different cognitive pattern for facial expressions between MDD and sub-clinical depression. Moreover, the deep perception for sad faces is correlated with increased suicidal ideation.

Significance

The intensity effect of social stimuli (facial expressions) was observed in sub-clinically and clinically depressed (MDD) individuals simultaneously, which might suggest that the more excited perception for negative facial expressions is a stable cognitive vulnerability possibly associated with the occurrence or recurrence of depression.     

Impact of voice on emotional judgment of faces: an event-related fMRI study

Emotional information can be conveyed by various means of communication, such as propositional content, speech intonation, facial expression, and gestures. Prior studies have demonstrated that inputs from one modality can alter perception in another modality. To evaluate the impact of emotional intonation on ratings of emotional faces, a behavioral study first was carried out. Second, functional magnetic resonance (fMRI) was used to identify brain regions that mediate crossmodal effects of emotional prosody on judgments of facial expressions. In the behavioral study, subjects rated fearful and neutral facial expressions as being more fearful when accompanied by a fearful voice as compared to the same facial expressions without concomitant auditory stimulus, whereas no such influence on rating of faces was found for happy voices. In the fMRI experiment, this shift in rating of facial expressions in presence of a fearfully spoken sentence was correlated with the hemodynamic response in the left amygdala extending into the periamygdaloid cortex, which suggests that crossmodal effects on cognitive judgments of emotional information are mediated via these neuronal structures. Furthermore, significantly stronger activations were found in the mid-portion of the right fusiform gyrus during judgment of facial expressions in presence of fearful as compared to happy intonations, indicating that enhanced processing of faces within this region can be induced by the presence of threat-related information perceived via the auditory modality. Presumably, these increased extrastriate activations correspond to enhanced alertness, whereas responses within the left amygdala modulate cognitive evaluation of emotional facial expressions.     

Visual search for facial expressions of emotion is less affected in simultanagnosia

Evidence in healthy human subjects has suggested that angry faces may be enhanced during spatial processing, perhaps even "popping-out" of a crowd. These contentions have remained controversial, but two recent reports in patients suffering from unilateral spatial neglect have lent some support to these views, suggesting that emotional faces capture attention more efficiently than neutral stimuli in the neglected field. Here, we investigate this phenomenon in a patient suffering from severe Balint's syndrome and consequent simultanagnosia. Using a visual search paradigm, we studied differences in the detection of angry, happy and neutral faces, as well as non-emotional stimuli. Results revealed that emotionally expressive faces, in particular anger, were detected more efficiently than other stimuli. These findings corroborate claims that facial expressions of emotion constitute a specific category of stimuli that attract attention more effectively, and are processed prior to attentional engagement.