Facial Emotion Recognition after Bilateral Amygdala Damage: Differentially Severe Impairment of Fear

Although the amygdala is widely believed to have a role in the recognition of emotion, a central issue concerns whether it is involved in the recognition of all emotions or whether it is more important to some emotions than to others. We describe studies of two people, DR and SE, with impaired recognition of facial expressions in the context of bilateral amygdala damage. When tested with photographs showing facial expressions of emotion from the Ekman and Friesen (1976) series, both DR and SE showed deficits in the recognition of fear. Problems in recognising fear were also found using photographic quality images interpolated (“morphed”) between prototypes of the six emotions in the Ekman and Friesen (1976) series to create a hexagonal continuum (running from happiness to surprise to fear to sadness to disgust to anger to happiness). Control subjects identified these morphed images as belonging to distinct regions of the continuum, corresponding to the nearest prototype expression. However, DR and SE were impaired on this task, with problems again being most clearly apparent in the region of the fear prototype. An equivalent test of recognition of morphed identities of six famous faces was performed normally by DR, confirming the dissociability of impairments affecting the recognition of identity and expression from the face. Further two-way forced-choice tests showed that DR was unable to tell fear from anger, but could tell happiness from sadness without difficulty. The finding that the recognition of fear can be differentially severely affected by brain injury is consistent with reports of the effects of bilateral amygdala damage in another case (Adolphs, Tranel, Damasio, & Damasio, 1994, 1995). The recognition of facial expressions of basic emotions may therefore be linked, to some extent, to specific neural substrates.     

Emotion recognition: facial components associated with various emotions

This study examined the effect of the changes in facial expressions in different parts of the face on emotion recognition. Fifty-two university students participated in the study. Seven emotions were selected as being the most suitable for categorization and expression: namely, anger, fear, surprise, disgust, sadness, happiness, and neutrality. Picture of these emotions were used to create stimulus materials, composed facial expressions were created by combining the upper and the lower parts of the pictures expressing different emotions. The participants were asked to categorize the type of emotion represented by each picture. The results showed that the upper area of the face was more often associated with anger, fear, surprise, and sadness. On the contrary, the lower area was more often associated with disgust and happiness. There were no significant differences between parts of the face associated with neutral emotions. Based on these results, we conclude that affected areas of the face differed as a function of emotion being experienced. Finally, the relationship of our results with Yamada's model (1993) was discussed.     

Concordance of facial reactions to facial expressions

Participants watching a facial expression of emotion tend to respond with the same facial expression. This facial concordance is well known for happiness, but not for other emotions. The present study investigated whether facial expressions of basic six emotions induce facial concordance in participants by average-face method. Facial reactions of 20 subjects were videotaped while watching a facial expression of six emotions performed by amateur actors in a computer display. The six average faces were made from corresponding facial expression of emotions in the display. Newly chosen 62 subjects were asked to classify those average faces into six categories of emotion. The facial concordance was found for happiness and surprise, but not for disgust and fear. However, for average face of anger and that of sadness, classifications were divided into a few categories. This result suggests a possibility that an average faces might have included ambiguous or different faces. It may be necessary to conduct re-classification not with the average-face but with individual faces.     

Discrimination thresholds for recognizing facial emotions: mostly higher among the elderly

Elderly people have lower ability for recognizing facial emotions than younger people. Previous studies showed that older adults had difficulty in recognizing anger, sadness and fear, but there were no consistent results for happiness, surprise and disgust. Most of these studies used a small number of stimuli, and tabulated the number of correct responses for facial expressions. These characteristics of the task might be the source of the discrepancy in the findings. The present study used a task which measures participants' discrimination thresholds for six basic emotions using psychophysical measurement methods. The results showed that the thresholds for elderly participants (74.8 +/- 6.5 yrs) were significantly higher than for younger participants (20.1 +/- 1.6 yrs) for sadness, surprise, anger, disgust and fear. There was no significant difference for happiness. Since the task that we developed was sufficiently sensitive, it is a useful tool for assessing individuals' ability to perceive emotion.     

A generalised deficit can account for problems in facial emotion recognition in schizophrenia.

Neuroimaging research has shown localised brain activation to different facial expressions. This, along with the finding that schizophrenia patients perform poorly in their recognition of negative emotions, has raised the suggestion that patients display an emotion specific impairment. We propose that this asymmetry in performance reflects task difficulty gradations, rather than aberrant processing in neural pathways subserving recognition of specific emotions. A neural network model is presented, which classifies facial expressions on the basis of measurements derived from human faces. After training, the network showed an accuracy pattern closely resembling that of healthy subjects. Lesioning of the network led to an overall decrease in the network's discriminant capacity, with the greatest accuracy decrease to fear, disgust and anger stimuli. This implies that the differential pattern of impairment in schizophrenia patients can be explained without having to postulate impairment of specific processing modules for negative emotion recognition.     

Reduced sensitivity in the recognition of anger and disgust in social anxiety disorder

Introduction. The aim of this study was to investigate the recognition of facial expressions in patients with a generalised social anxiety disorder. It is well documented that in different psychiatric disorders (e.g., depression, schizophrenia) patients may show an altered processing of emotions. However, in generalised social anxiety, emotion recognition has not been studied.

Methods. 24 Patients with generalised social anxiety disorder and 26 healthy controls, matched on age, education, and sex were included. The task entailed the emotional labelling of faces with different facial expressions (happiness, fear, disgust, sadness, surprise, anger) presented in different intensities. Subjects were asked to make a forced‐choice response.

Results. These revealed that patients with a generalised social anxiety disorder were less sensitive for the negative facial expressions of anger and disgust compared to the control group.

Conclusions. This deficit could play a role in the development and/or the maintaining of the social anxiety. Both explanations are discussed.     

Brain oscillations and BIS/BAS (behavioral inhibition/activation system) effects on processing masked emotional cues.: ERS/ERD and coherence measures of alpha band

Alpha brain oscillation modulation was analyzed in response to masked emotional facial expressions. In addition, behavioural activation (BAS) and behavioural inhibition systems (BIS) were considered as an explicative factor to verify the effect of motivational significance on cortical activity. Nineteen subjects were submitted to an ample range of facial expressions of emotions (anger, fear, surprise, disgust, happiness, sadness, and neutral). The results demonstrated that anterior frontal sites were more active than central and posterior sites in response to facial stimuli. Moreover, right-side responses varied as a function of emotional types, with an increased right-frontal activity for negative emotions. Finally, whereas higher BIS subjects generated a more right hemisphere activation for some negative emotions (such as fear, anger, and surprise), Reward-BAS subjects were more responsive to positive emotion (happiness) within the left hemisphere. Valence and potential threatening power of facial expressions were considered to elucidate these cortical differences.     

Voluntary Facial Action Generates Emotion-Specific Autonomic Nervous System Activity

Four experiments were conducted to determine whether voluntarily produced emotional facial configurations are associated with differentiated patterns of autonomic activity, and if so, how this might be mediated. Subjects received muscle-by-muscle instructions and coaching to produce facial configurations for anger, disgust, fear, happiness, sadness, and surprise while heart rate, skin conductance, finger temperature, and somatic activity were monitored. Results indicated that voluntary facial activity produced significant levels of subjective experience of the associated emotion, and that autonomic distinctions among emotions: (a) were found both between negative and positive emotions and among negative emotions, (b) were consistent between group and individual subjects' data, (c) were found in both male and female subjects, (d) were found in both specialized (actors, scientists) and nonspecialized populations, (e) were stronger when the voluntary facial configurations most closely resembled actual emotional expressions, and (f) were stronger when experience of the associated emotion was reported. The capacity of voluntary facial activity to generate emotion-specific autonomic activity: (a) did not require subjects to see facial expressions (either in a mirror or on an experimenter's face), and (b) could not be explained by differences in the difficulty of making the expressions or by differences in concomitant somatic activity.     

Effects of believes and expectations about self and others on emotional recognition of facial expressions: from the perspective of adult attachment

This study aimed at examining how adult attachment styles as believes and expectations about self and others affected emotional recognition of facial expressions. In this study, hypotheses were framed based on the perspective of attachment dimensions. One hundred and sixty one undergraduates observed positive, negative, and neutral facial expressions as stimulus, and rated the extent to which each stimuli expressed several kinds of emotion. The main results were as follows. Generally, either anxious or avoidant individuals were less likely to perceive positive emotion (happy) from facial expressions, and anxious and less avoidant individuals perceived other-oriented negative emotions (anger, disgust, and contempt). In addition, avoidant individuals were less likely to perceive positive emotion from positive facial expressions. On the other hand, from negative facial expressions, anxious and less avoidant individuals were more likely to perceive other-oriented negative emotions, and anxious individuals were less likely to perceive positive emotion. The results were discussed from the perspective of adult attachment theory.     

Impaired recognition of fear in a Chinese man with bilateral cingulate and unilateral amygdala damage

LJM, a 41-year-old schizophrenic Chinese man with bilateral anterior cingulate gyrus (Brodmann's area 24) lesions and also a small lesion in right amygdala after an operation, was compared with normal as well as brain-damaged and schizophrenic controls in identification of morphed facial expressions of six basic emotions. In repeated administrations of the test for recognition of facial emotions, over a 1- year period, LJM performed significantly worse for expressions of fear compared with the three groups of controls. Recognition of other emotions was not significantly different from that of the controls, except that his recognition of disgust during the first session (but not in two subsequent sessions) was worse than normal and brain-damaged controls but not worse than schizophrenic controls. The dissociation between recognition of fear and other emotions supported the view that the brain has separable networks for processing different emotions, and that the right amygdala as well as the anterior part of bilateral cingulate gyrus are possible substrates involved in the special network for perception of fear. The results from the various groups of Chinese subjects indicate that they perceive emotions in a categorical manner, and that the six basic emotions are likely to be cross-cultural universals.     

Face emotion labeling deficits in children with bipolar disorder and severe mood dysregulation

Children with narrow phenotype bipolar disorder (NP-BD; i.e., history of at least one hypomanic or manic episode with euphoric mood) are deficient when labeling face emotions. It is unknown if this deficit is specific to particular emotions, or if it extends to children with severe mood dysregulation (SMD; i.e., chronic irritability and hyperarousal without episodes of mania). Thirty-nine NP-BD, 31 SMD, and 36 control subjects completed the emotional expression multimorph task, which presents gradations of facial emotions from 100% neutrality to 100% emotional expression (happiness, surprise, fear, sadness, anger, and disgust). Groups were compared in terms of intensity of emotion required before identification occurred and accuracy. Both NP-BD and SMD youth required significantly more morphs than controls to label correctly disgusted, surprised, fearful, and happy faces. Impaired face labeling correlated with deficient social reciprocity skills in NP-BD youth and dysfunctional family relationships in SMD youth. Compared to controls, patients with NP-BD or SMD require significantly more intense facial emotion before they are able to label the emotion correctly. These deficits are associated with psychosocial impairments. Understanding the neural circuitry associated with face-labeling deficits has the potential to clarify the pathophysiology of these disorders.     

Facial mimicry and emotional contagion to dynamic emotional facial expressions and their influence on decoding accuracy.

The present study had the goal to assess whether individuals mimic and show emotional contagion in response to relatively weak and idiosyncratic dynamic facial expressions of emotions similar to those encountered in everyday life. Furthermore, the question of whether mimicry leads to emotional contagion and in turn facilitates emotion recognition was addressed. Forty-one female participants rated a series of short video clips of stimulus persons expressing anger, sadness, disgust, and happiness regarding the emotions expressed. An unobtrusive measure of emotional contagion was taken. Evidence for mimicry was found for all types of expressions. Furthermore, evidence for emotional contagion of happiness and sadness was found. Mediational analyses could not confirm any relation between mimicry and emotional contagion nor between mimicry and emotion recognition.     

Basic and complex emotions in depression and anxiety

The current study was designed to assess the emotion states that occur across the clinical disorders of depression, anxiety and mixed anxiety depression. The emotion states were assessed using the Basic Emotions Scale, which includes a set of simple and complex emotions rationally derived from the basic emotions of sadness, anger, fear, disgust and happiness. The profiles of emotion states across the clinical disorders and across a matched healthy control group supported an analysis in which emotions related to sadness and disgust were elevated in the depressed and mixed disorders, whereas increased levels of anger and fear, and decreased levels of happiness did not distinguish between clinical groups but were found in all disorders in comparison to healthy controls. Further factor analyses gave support for the proposed basic emotions model and did not support alternative models such as the Positive Affect‐Negative Affect model. The findings demonstrate how a theoretically based emotion analysis can provide a useful foundation from which to explore the emotional disorders. Copyright © 2007 John Wiley & Sons, Ltd.     

FACIAL EXPRESSION RECOGNITION BY PEOPLE WITH MÖBIUS SYNDROME

We present an investigation of facial expression recognition by three people (BC, LP, and NC) with Mobius syndrome, a congenital disorder producing facial paralysis. The participants were asked to identify the emotion displayed in 10 examples of facial expressions associated with each of 6 basic emotions from the Ekman and Friesen (1976) series. None of the three people with Möbius syndrome was significantly impaired on this task. On a second test of facial expression recognition using computer-morphed facial expressions, NC showed a statistically significant impairment, BC a borderline deficit, and LP was unimpaired. However, even when impairments were found, people with Möbius syndrome still recognised many of the facial expressions shown to them. The recognition of facial expressions by people who have never been able to produce such signals on their own faces demonstrates that the ability to produce facial expressions is not a necessary prerequisite of their recognition.     

Facial expression recognition by people with mobius syndrome

We present an investigation of facial expression recognition by three people (BC, LP, and NC) with Mobius syndrome, a congenital disorder producing facial paralysis. The participants were asked to identify the emotion displayed in 10 examples of facial expressions associated with each of 6 basic emotions from the Ekman and Friesen (1976) series. None of the three people with Mobius syndrome was significantly impaired on this task. On a second test of facial expression recognition using computer-morphed facial expressions, NC showed a statistically significant impairment, BC a borderline deficit, and LP was unimpaired. However, even when impairments were found, people with Mobius syndrome still recognised many of the facial expressions shown to them. The recognition of facial expressions by people who have never been able to produce such signals on their own faces demonstrates that the ability to produce facial expressions is not a necessary prerequisite of their recognition.     

Common and specific brain responses to scenic emotional stimuli

Processing of emotions has been an enduring topic of interest in neuroimaging research, but studies have mostly used facial emotional stimuli. The aim of this study was to determine neural networks involved in emotion processing using scenic emotional visual stimuli. One hundred and twenty photographs from the International Affective Picture System (IAPS), including ecological scenes of disgust, fear, happiness, and sadness, were presented to 40 healthy participants while they underwent functional magnetic imaging resonance (fMRI). Afterwards they evaluated the emotional content of the pictures in an offline task. The occipito-temporal cortex and the amygdala–hippocampal complex showed a non-specific emotion-related activation, which was more marked in response to negative emotions than to happiness. The temporo-parietal cortex and the ventral anterior cingulate gyrus showed deactivation, with the former being marked for all emotions except fear and the latter being most marked for disgust. The fusiform gyrus showed activation in response to disgust and deactivation in response to happiness or sadness. Brain regions involved in processing of scenic emotion therefore resemble those reported for facial expressions of emotion in that they respond to a range of different emotions, although there appears to be specificity in the intensity and direction of the response.     

Decreased P3 amplitudes elicited by negative facial emotion in manic patients: Selective deficits in emotional processing

Manic patients have impairments in recognizing negative emotional stimuli. However, there have been few studies on manic patients’ neurophysiological responses to facial emotions. We measured the P3 event-related potentials using facial emotional stimuli to investigate whether the impairment in recognition of negative emotions is greater in maniac patients. We recruited twenty manic patients and twenty controls. A visual oddball paradigm was used with facial pictures: happy, neutral, sad, fear, and disgust emotions. While P3 amplitudes of emotional stimuli were significantly larger than those of neutral stimuli in controls, the amplitudes were not significantly different from those for neutral pictures in manic patients. Repeated-measures analysis of variance on P3 amplitudes revealed significant interaction effects of paired emotions as sad-neutral, disgust-neutral, fear-neutral, but not in the happy-neutral emotion pairs. These differential P3 responses suggest that manic patients may have abnormal neurophysiological activity when evaluating negative facial emotions. Thus, these findings may give the evidence for reduced negative emotion recognition of manic patients.     

Decline or improvement?: Age-related differences in facial expression recognition

We examined age-related differences in facial expression recognition in association with potentially interfering variables such as general cognitive ability (verbal and visuospatial abilities), face recognition ability, and the experiences of positive and negative emotions. Participants comprised 34 older (aged 62-81 years) and 34 younger (aged 18-25 years) healthy Japanese adults. The results showed not only age-related decline in sadness recognition but also age-related improvement in disgust recognition. Among other variables, visuospatial ability was moderately related to facial expression recognition in general, and the experience of negative emotions was related to sadness recognition. Consequently, age-related decline in sadness recognition was statistically explained by age-related decrease in the experience of negative emotions. On the other hand, age-related improvement in disgust recognition was not explained by the interfering variables, and it reflected a higher tendency in the younger participants to mistake disgust for anger. Possible mechanisms are discussed in terms of neurobiological and socio-environmental factors.     

Voluntary facial expression and hemispheric asymmetry over the frontal cortex

Brain activity was monitored while 36 participants produced facial configurations denoting anger, disgust, fear, joy, and sadness. EEG alpha power was analyzed during each facial pose, with facial conditions grouped according to the approach/withdrawal motivational model of emotion. This model suggests that "approach" emotions are associated with relatively greater left frontal brain activity whereas "withdrawal" emotions are associated with relatively greater right frontal brain activity. In the context of a bilateral decrease in activation, facial poses of emotions in the withdrawal condition resulted in relatively less left frontal activation in the lateral-frontal, midfrontal and frontal-temporal-central region, but not in the parietal region, as predicted. Findings in the approach condition were less consistently supportive of predictions of the approach/withdrawal model. Implications for the approach/withdrawal model and for the emotion eliciting potential of voluntary facial movement are discussed.     

Facial expression recognition and emotional regulation in narcolepsy with cataplexy

Cataplexy is pathognomonic of narcolepsy with cataplexy, and defined by a transient loss of muscle tone triggered by strong emotions. Recent researches suggest abnormal amygdala function in narcolepsy with cataplexy. Emotion treatment and emotional regulation strategies are complex functions involving cortical and limbic structures, like the amygdala. As the amygdala has been shown to play a role in facial emotion recognition, we tested the hypothesis that patients with narcolepsy with cataplexy would have impaired recognition of facial emotional expressions compared with patients affected with central hypersomnia without cataplexy and healthy controls. We also aimed to determine whether cataplexy modulates emotional regulation strategies. Emotional intensity, arousal and valence ratings on Ekman faces displaying happiness, surprise, fear, anger, disgust, sadness and neutral expressions of 21 drug‐free patients with narcolepsy with cataplexy were compared with 23 drug‐free sex‐, age‐ and intellectual level‐matched adult patients with hypersomnia without cataplexy and 21 healthy controls. All participants underwent polysomnography recording and multiple sleep latency tests, and completed depression, anxiety and emotional regulation questionnaires. Performance of patients with narcolepsy with cataplexy did not differ from patients with hypersomnia without cataplexy or healthy controls on both intensity rating of each emotion on its prototypical label and mean ratings for valence and arousal. Moreover, patients with narcolepsy with cataplexy did not use different emotional regulation strategies. The level of depressive and anxious symptoms in narcolepsy with cataplexy did not differ from the other groups. Our results demonstrate that narcolepsy with cataplexy accurately perceives and discriminates facial emotions, and regulates emotions normally. The absence of alteration of perceived affective valence remains a major clinical interest in narcolepsy with cataplexy, and it supports the argument for optimal behaviour and social functioning in narcolepsy with cataplexy.