Facial emotion recognition impairment in chronic temporal lobe epilepsy

Purpose:   To evaluate facial emotion recognition (FER) in a cohort of 176 patients with chronic temporal lobe epilepsy (TLE).
Methods:   FER was tested by matching facial expressions with the verbal labels for the following basic emotions: happiness, sadness, fear, disgust, and anger. Emotion recognition performances were analyzed in medial (n = 140) and lateral (n = 36) TLE groups. Fifty healthy subjects served as controls. The clinical and neuroradiologic variables potentially affecting the ability to recognize facial expressions were taken into account.
Results:   The medial TLE (MTLE) group showed impaired FER (86% correct recognition) compared to both the lateral TLE patients (FER = 93.5%) and the controls (FER = 96.4%), with 42% of MTLE patients recording rates of FER that were lower [by at least 2 standard deviations (SDs)] than the control mean. The MTLE group was impaired compared to the healthy controls in the recognition of all basic facial expressions except happiness. The patients with bilateral MTLE were the most severely impaired, followed by the right and then the left MTLE patients. FER was not affected by type of lesion, number of antiepileptic drugs (AEDs), aura semiology, or gender. Conversely, the early onset of seizures/epilepsy was related to FER deficits. These deficits were already established in young adulthood, with no evidence of progression in older MTLE patients.
Conclusion:   These results on a large cohort of TLE patients demonstrate that emotion recognition deficits are common in MTLE patients and widespread across negative emotions. We confirm that early onset seizures with right or bilateral medial temporal dysfunction lead to severe deficits in recognizing facial expressions of emotions.     

Seeing happy emotion in fearful and angry faces: qualitative analysis of facial expression recognition in a bilateral amygdala-damaged patient

Neuropsychological studies reported that bilateral amygdala-damaged patients had impaired recognition of facial expressions of fear. However, the specificity of this impairment remains unclear. To address this issue, we carried out two experiments concerning the recognition of facial expression in a patient with bilateral amygdala damage (HY). In Experiment 1, subjects matched the emotion of facial expressions with appropriate verbal labels, using standardized photographs of facial expressions illustrating six basic emotions. The performance of HY was compared with age-matched normal controls (n = 13) and brain-damaged controls (n = 9). HY was less able to recognize facial expressions showing fear than normal controls. In addition, the error pattern exhibited by HY for facial expressions of fear and anger were distinct from those exhibited by both control groups, and suggested that HY confused these emotions with happiness. In Experiment 2, subjects were presented with morphed facial expressions that blended happiness and fear, happiness and anger, or happiness and sadness. Subjects were requested to categorize these expressions by two-way forced-choice selection. The performance of HY was compared with age-matched normal controls (n = 8). HY categorized the morphed fearful and angry expressions blended with some happy content as happy facial expressions more frequently than normal controls. These findings support the idea that amygdala-damaged patients have impaired processing of facial expressions relating to certain negative emotions, particularly fear and anger. More specifically, amygdala-damaged patients seem to give positively biased evaluations for these negative facial expressions.     

Selective Impairment of Basic Emotion Recognition in People with Autism: Discrimination Thresholds for Recognition of Facial Expressions of Varying Intensities

Autism spectrum disorders (ASD) are characterized by early onset qualitative impairments in reciprocal social development. However, whether individuals with ASD exhibit impaired recognition of facial expressions corresponding to basic emotions is debatable. To investigate subtle deficits in facial emotion recognition, we asked 14 children diagnosed with high-functioning autism (HFA)/AS and 17 typically developing peers to complete a new highly sensitive test of facial emotion recognition. The test stimuli comprised faces expressing increasing degrees of emotional intensity that slowly changed from a neutral to a full-intensity happiness, sadness, surprise, anger, disgust, or fear expression. We assessed individual differences in the intensity of stimuli required to make accurate judgments about emotional expressions. We found that, different emotions had different identification thresholds and the two groups were generally similar in terms of the sequence of discrimination threshold of six basic expressions. It was easier for individuals in both groups to identify emotions that were relatively fully expressed (e.g., intensity >?50%). Compared with control participants, children with ASD generally required stimuli with significantly greater intensity for the correct identification of anger, disgust, and fear expressions. These results suggest that individuals with ASD do not have a general but rather a selective impairment in basic emotion recognition.     

Processing of emotional facial expressions in Korsakoff's syndrome

Interpersonal contacts depend to a large extent on understanding emotional facial expressions of others. Several neurological conditions may affect proficiency in emotional expression recognition. It has been shown that chronic alcoholics are impaired in labelling emotional expressions. More specifically, they mislabel sad expressions, regarding them as more hostile. Surprisingly, there has been relatively little research on patients with Korsakoff's syndrome as a result of chronic alcohol abuse. The current study investigated 23 patients diagnosed with Korsakoff's syndrome compared to 23 matched control participants. This study is the first to make use of a newly developed sensitive paradigm to measure emotion recognition for several emotions (anger, disgust, fear, happiness, sadness and surprise). The results show that patients with Korsakoff's syndrome are impaired at recognizing angry, fearful and surprised facial emotional expressions. These deficits might be due to the reported sub-cortical brain dysfunction in Korsakoff's syndrome.     

Facial emotion recognition in schizophrenia: intensity effects and error pattern

OBJECTIVE: The authors used color photographs of emotional and neutral expressions to investigate recognition patterns of five universal emotions in schizophrenia. METHOD: Twenty-eight stable outpatients with schizophrenia (19 men and nine women) and 61 healthy subjects (29 men and 32 women) completed an emotion discrimination test that presented mild and extreme intensities of happy, sad, angry, fearful, disgusted, and neutral faces, balanced for gender and ethnicity. Analyses evaluated accuracy of identifying emotions as a function of intensity, diagnosis, and gender of poser and rater. RESULTS: Patients performed worse than comparison subjects on recognition of all emotions and neutral faces combined, including mild and extreme expressions. For specific emotions, patients performed worse on recognition of fearful, disgusted, and neutral expressions. For all emotions except disgust, recognition of extreme intensity was better than recognition of mild intensity. However, patients showed less benefit from increased intensity for all emotions combined, and the difference was most pronounced for fear. Thus, patients were more impaired than healthy comparison subjects in identifying high-intensity expressions, even though this was an easier task than identifying low-intensity expressions. In the comparison of patterns of errors, patients and healthy subjects differed only in misattributions of neutral expressions; patients overattributed disgusted expressions and underattributed happy expressions. CONCLUSIONS: Patients with schizophrenia were impaired in overall emotion recognition, particularly fear and disgust, and did not benefit from increased emotional intensity. Error patterns indicate that patients misidentified neutral cues as negatively valenced.     

Emotion recognition in temporal lobe epilepsy: A systematic review

There is increasing interest in the understanding of emotion recognition deficits in temporal lobe epilepsy (TLE), the most common form of focal epilepsies. There are conflicting reports about impairments for different emotions in right and left temporal lobe epilepsy patients. A systematic review and a narrative synthesis was conducted for studies investigating emotion recognition (ER) in TLE. Embase, MEDLINE, PsychINFO and Pubmed were searched from 1990 to March 2015 and reference lists were reviewed. 996 citations were identified and 43 studies were finally included.ER deficits are consistently observed across studies. A fear recognition deficit is always reported, followed by deficits in sadness and disgust recognition. Deficits are observed across visual and auditory domains. Conflicting evidence is present concerning the severity of ER deficits in right and left TLE. Studies on anterior temporal lobectomy report data similar to that observed in pre-surgical patients.Current evidence supports the conclusion that recognition of negative emotions is commonly impaired in TLE, particularly for fear, and in the visual domain. Future work should focus on more ecologically valid test, on longitudinal studies to assess the role of anterior temporal lobectomy, and to correlate ER measures to social functioning in everyday life.     

Rôle de la flexibilité cognitive dans la reconnaissance d’expressions émotionnelles chez les personnes atteintes de Troubles du Spectre Autistique

The present research tested whether young children with Autism Spectrum Disorders (ASDs) shows impaired recognition of basic-emotion expressions (anger, fear, happiness, sadness, disgust) and the same emotions embedded in a social background (i.e. simple versus complex facial emotion recognition), compared with typically developing (TD) children. Moreover, we investigated whether cognitive flexibility could be linked with these faces processing skills. Our results showed that performance in ASD children was similar to the group of TD children for simple emotion recognition whereas TD children outperformed ASDs children in the complex task. In the second part, our study tends to confirm a link between cognitive flexibility and faces processing skills in children with ASD, especially when different contextual cues are present to extract facial emotion. We confirm previous findings demonstrating that individuals with ASDs use an effortful “systematizing” process to recognize emotion expressions, whereas TD individuals use a more holistic process. These results are discussed within the context of current neuropsychological studies on “weak central coherence”, hyper-systemizing theory, and lack of cognitive flexibility in ASD.     

Differential deficits in expression recognition in gene-carriers and patients with Huntington's disease

Previous studies in symptomatic patients and asymptomatic gene-carriers of Huntington's disease (HD) reported a differential deficit in the recognition of facial expressions of disgust. This impairment may point to involvement of the basal ganglia in the recognition of disgust. In this study, we compared the performance of 20 patients with symptoms of HD, 20 gene-carriers of HD and 20 healthy controls on two tests of facial expressions in order to further investigate the role of the basal ganglia in disgust recognition. Recognition of fear, rather than disgust, was most severely impaired in the patients, who were also impaired at recognising expressions of anger, disgust and sadness. Direct testing for a differential deficit in disgust at the group level (and at the level of individual HD cases) revealed that the patients were in fact significantly more impaired on the other negative expressions than on disgust. The gene-carriers were not impaired on any expression, although there was a trend for the gene-carriers to be poorer at recognising fearful faces than the controls. We argue that the expression recognition performance of the patients and gene-carriers simply reflects differences in task difficulty, rather than dysfunction of any mechanisms dedicated to specific emotions. In contrast to previous studies in patients or gene-carriers of HD, our findings provide no evidence for a role of the basal ganglia in the recognition of disgust and cast doubt on whether results from HD patients and gene-carriers can be used in support of a double dissociation between recognition of disgust and fear.     

Effects of diazepam on facial emotion recognition

OBJECTIVE: There have been few studies of the pharmacologic modulation of facial emotion recognition. The present study aimed to replicate and extend the finding that recognition of facial anger was selectively impaired by diazepam. The hypothesis was that, in comparison with placebo, diazepam would impair the recognition of facial anger in healthy volunteers, but not the recognition of 5 other basic emotions: happiness, surprise, fear, sadness and disgust. DESIGN: A randomized, counterbalanced, double-blind, placebo-controlled, within-subjects comparison of diazepam with placebo. SETTING: A university psychopharmacology research unit. PARTICIPANTS: Healthy male (n = 6) and female (n = 22) volunteers, aged 18-45 years. PROCEDURES: Subjects were tested on 2 tasks following the administration of diazepam, 15 mg, and placebo on separate occasions. In the first "multimorph" task, images of facial expressions were morphed to produce continua between the neutral and full expressions of 6 basic emotions. Accuracy and identification thresholds were assessed for stimuli in which the intensity of expression gradually increased. In the second "emotional hexagon" task, facial expressions were morphed between pairs of emotions. Single images were presented, and accuracy and speed of response were assessed. RESULTS: Diazepam produced broad impairments in response accuracy, recognition thresholds and response speed on the facial emotion tasks that were not limited to angry expressions. CONCLUSIONS: The present study found that diazepam, 15 mg, impaired facial emotion recognition, but not selectively. In the emotional hexagon task, a reaction-time analysis suggested that the identification of facial anger might be differentially sensitive to variations in stimulus duration, complicating the interpretation of this paradigm.     

Impaired facial emotion recognition and reduced amygdalar volume in schizophrenia

Structural abnormalities of the amygdala and impaired facial emotion recognition have been reported in schizophrenia. Most studies demonstrated reduced amygdalar volumes in schizophrenia patients, and difficulty in recognizing negative facial emotions has also been reported. However, findings on the deficit in facial emotion recognition have been inconsistent, and the relationships between this impairment and amygdalar volume reduction remain unclear. In this study, we investigated these relationships by performing volumetric analysis of the amygdala and evaluation of facial emotion recognition performance in the same subjects with schizophrenia. The sample group comprised 20 schizophrenia patients and 20 matched healthy controls. We measured the volumes of the amygdalae with high-resolution magnetic resonance imaging (MRI) at 3.0 Tesla. Additionally, we included a task that evaluated the subjects' ability to recognize the intensity of basic facial emotions. We found that impaired facial emotion recognition in schizophrenia patients is emotion-specific (sadness, surprise, disgust, and anger). Moreover, the volume of each amygdala on either side of the brain was reduced. Finally, we found a correlation between left amygdalar volume and the recognition of sadness in facial expressions. This study demonstrated that amygdala dysfunction may contribute to impaired facial emotion recognition in schizophrenia.     

Impaired recognition of facial emotions from low-spatial frequencies in Asperger syndrome

The theory of 'weak central coherence' [Happe, F., & Frith, U. (2006). The weak coherence account: Detail-focused cognitive style in autism spectrum disorders. Journal of Autism and Developmental Disorders, 36(1), 5-25] implies that persons with autism spectrum disorders (ASDs) have a perceptual bias for local but not for global stimulus features. The recognition of emotional facial expressions representing various different levels of detail has not been studied previously in ASDs. We analyzed the recognition of four basic emotional facial expressions (anger, disgust, fear and happiness) from low-spatial frequencies (overall global shapes without local features) in adults with an ASD. A group of 20 participants with Asperger syndrome (AS) was compared to a group of non-autistic age- and sex-matched controls. Emotion recognition was tested from static and dynamic facial expressions whose spatial frequency contents had been manipulated by low-pass filtering at two levels. The two groups recognized emotions similarly from non-filtered faces and from dynamic vs. static facial expressions. In contrast, the participants with AS were less accurate than controls in recognizing facial emotions from very low-spatial frequencies. The results suggest intact recognition of basic facial emotions and dynamic facial information, but impaired visual processing of global features in ASDs.     

Facial emotion perception in patients with epilepsy: A systematic review with meta-analysis

Facial emotion perception is a fundamental social competency relying on a specialised, yet distributed, neural network. This review aimed to determine whether patients with epilepsy have facial emotion perception accuracy impairments overall, or for a subset of emotions (anger, disgust, happiness, sadness, fear, and surprise), and the relationship to epilepsy type, demographic/treatment variables, and brain organisation. Database searches used PRISMA guidelines with strict inclusion/exclusion criteria. Thirty included studies assessed patients with temporal lobe (TLE; n = 709), frontocentral (FCE; n = 22), and genetic generalised (GGE; n = 48) epilepsy. Large deficits emerged in patients with epilepsy compared to controls (n = 746; Hedges’ g = 0.908–1.076). Patients with TLE were significantly impaired on all emotions except surprise; patients with GGE were significantly impaired in anger, disgust, and fear perception. Meta-regression of patients with TLE revealed younger age at testing was associated with lower accuracy. This review provides evidence for marked global deficits of emotion perception in epilepsy, with differential emotion-specific impairment patterns in patients with TLE and GGE.     

Recognition of emotion with temporal lobe epilepsy and asymmetrical amygdala damage

PURPOSE: Impairments in emotion recognition occur when there is bilateral damage to the amygdala. In this study, ability to recognize auditory and visual expressions of emotion was investigated in people with asymmetrical amygdala damage (AAD) and temporal lobe epilepsy (TLE). METHODS: Recognition of five emotions was tested across three participant groups: those with right AAD and TLE, those with left AAD and TLE, and a comparison group. Four tasks were administered: recognition of emotion from facial expressions, sentences describing emotion-laden situations, nonverbal sounds, and prosody. RESULTS: Accuracy scores for each task and emotion were analysed, and no consistent overall effect of AAD on emotion recognition was found. However, some individual participants with AAD were significantly impaired at recognizing emotions, in both auditory and visual domains. CONCLUSIONS: The findings indicate that a minority of individuals with AAD have impairments in emotion recognition, but no evidence of specific impairments (e.g., visual or auditory) was found.     

Emotion recognition deficits in the elderly

In two studies, healthy elderly adults were poor at recognizing certain emotions. In study one, an emotion face morphed to express a new emotion. The elderly were impaired when recognizing anger and sadness, whereas no differences were found between the two age groups in recognizing fear or happiness, or in a task requiring reasoning about non=emotion stimuli. In study two, the elderly were impaired when judging which of two faces was more angry, sad, or fearful, but they were not impaired when judging other emotions or when judging which of two beakers was more full. The elderly were also impaired when matching emotion sounds to angry, sad, and disgusted faces, but not to other emotions and not when matching non-emotion (e.g., machine) sounds to machines. Elderly deficits were independent of performance on a task requiring basic face processing (gender recognition). Overall, the results provide support for an age-related decline in the recognition of some emotions that is independent of changes in perceptual abilities, processing speed, fluid IQ, basic face processing abilities, and reasoning about non face stimuli. Recognition of emotion stimuli might be mediated by regions of the brain that are independent from those associated with a more general cognitive decline.     

The relation between anger and different forms of disgust: Implications for emotion recognition impairments in Huntington's disease

Initial reports of emotion recognition in Huntington's disease (HD) found disproportionate impairments in recognising disgust. Not all subsequent studies have found this pattern, and a review of the literature to date shows that marked impairments in recognising anger are also often seen in HD. However, the majority of studies have based their conclusions on a single test of facial expression recognition. In the current study we revisit this issue of emotion recognition in HD to address whether the pattern found on one test of facial expression recognition generalised to another, and to different modalities using tests of emotion recognition from facial expressions, vocal expressions, and short verbal vignettes. The results showed evidence of impairments in recognising anger, fear and disgust across the three domains, with recognition of anger the most severely impaired. Given work identifying different subtypes of disgust that are associated with different facial features, a second study examined the recognition of three disgust expressions that healthy participants reliably associate with unpleasant tastes, unpleasant smells, and a more general elaborated or expanded form of disgust that includes reactions to violations of moral standards. The results showed a disproportionate impairment in recognising faces associated with the expanded form, the subtype most closely aligned with anger. We conclude that the related emotions of disgust and anger associated with social disapproval are frequently impaired in HD and discuss factors that might cause one emotion to show more severe impairments than the other.     

Disgust and happiness recognition correlate with anteroventral insula and amygdala volume respectively in preclinical Huntington's disease

Patients with Huntington's disease (HD) can show disproportionate impairments in recognizing facial signals of disgust, but the neural basis of this deficit remains unclear. Functional imaging studies have implicated the anterior insula in the ability to recognize disgust, but have identified other structures as well, including the basal ganglia. In view of variable insula and basal ganglia volume changes in HD, we used voxel-based morphometry to map regional variations in gray matter (GM) volume in participants carrying the mutation for HD, and correlated this with their performance on a test of facial emotion recognition for six basic emotions (disgust, fear, anger, happiness, sadness, surprise). The volume of the anteroventral insula was strongly correlated with performance on the disgust recognition task. The amygdala volume (bilaterally) correlated with the ability to recognize happy facial expressions. There was marked specificity of the regional correlations for the emotion involved. Recognition of other emotion expressions, or more general cognitive or motor performance as measured by a standardized rating scale, did not correlate with regional brain volume in this group. Control participants showed no effect for any measure. The strong linear correlations for disgust and happiness recognition imply direct involvement of the anterior insula in disgust appreciation, and a similar role for the amygdala in recognizing happy facial expressions. The absence of a significant correlation with the basal ganglia suggests a less critical role for these structures in disgust recognition than has previously been suggested. The findings also highlight the role of neurodegenerative diseases combined with statistical imaging techniques in elucidating the brain basis of behavior and cognition.     

Evidence for altered amygdala activation in schizophrenia in an adaptive emotion recognition task

Deficits in social cognition seem to present an intermediate phenotype for schizophrenia, and are known to be associated with an altered amygdala response to faces. However, current results are heterogeneous with respect to whether this altered amygdala response in schizophrenia is hypoactive or hyperactive in nature. The present study used functional magnetic resonance imaging to investigate emotion-specific amygdala activation in schizophrenia using a novel adaptive emotion recognition paradigm. Participants comprised 11 schizophrenia outpatients and 16 healthy controls who viewed face stimuli expressing emotions of anger, fear, happiness, and disgust, as well as neutral expressions. The adaptive emotion recognition approach allows the assessment of group differences in both emotion recognition performance and associated neuronal activity while also ensuring a comparable number of correctly recognized emotions between groups. Schizophrenia participants were slower and had a negative bias in emotion recognition. In addition, they showed reduced differential activation during recognition of emotional compared with neutral expressions. Correlation analyses revealed an association of a negative bias with amygdala activation for neutral facial expressions that was specific to the patient group. We replicated previous findings of affected emotion recognition in schizophrenia. Furthermore, we demonstrated that altered amygdala activation in the patient group was associated with the occurrence of a negative bias. These results provide further evidence for impaired social cognition in schizophrenia and point to a central role of the amygdala in negative misperceptions of facial stimuli in schizophrenia.     

Recognition of facial expressions of emotion by persons with mental retardation. A matched comparison study.

Children and adults with mental retardation were tested on their ability to recognize facial expressions of emotion. The sample consisted of 80 children and adults with mental retardation and a control group of 80 nonhandicapped children matched on mental age and gender. Ekman and Friesen's normed photographs of the six basic emotions (anger, disgust, fear, happiness, sadness, and surprise) were used in a recognition task of facial expressions. Subjects were individually read two-sentence stories identifying a specific emotion, presented with a randomized array of the six photographs of the basic facial expressions of emotion, and then asked to select the photograph that depicted the emotion identified in the story. This procedure was repeated with 24 different stories, with each of the six basic emotions being represented four times. Results showed that, as a group, individuals with mental retardation were not as proficient as their mental-age-matched nonhandicapped control subjects at recognizing facial expressions of emotion. Although adults with mild mental retardation were more proficient at this task than those with moderate mental retardation, this finding was not true for children. There was a modest difference between the children with moderate mental retardation and their nonhandicapped matched controls in their ability to recognize facial expression of disgust.     

Facial expression recognition across the adult life span

We report three experiments investigating the recognition of emotion from facial expressions across the adult life span. Increasing age produced a progressive reduction in the recognition of fear and, to a lesser extent, anger. In contrast, older participants showed no reduction in recognition of disgust, rather there was some evidence of an improvement. The results are discussed in terms of studies from the neuropsychological and functional imaging literature that indicate that separate brain regions may underlie the emotions fear and disgust. We suggest that the dissociable effects found for fear and disgust are consistent with the differential effects of ageing on brain regions involved in these emotions.     

Social cognition in temporal lobe epilepsy: A systematic review and meta-analysis

ObjectiveThere is increasing evidence suggesting that social cognitive abilities are impaired in temporal lobe epilepsy (TLE), the most common form of focal epilepsies.MethodsIn this meta-analysis, 31 studies investigating theory of mind (ToM) and facial emotion recognition performances of 1356 patients with TLE (351 postsurgery) and 859 healthy controls were included.ResultsPatients with TLE had significant deficits in ToM (d = 0.73–0.89) and recognition of facial emotions. There were no significant differences in severity of social cognitive deficits between patients with TLE with or without medial temporal lobectomy. Earlier onset of seizures was associated with ToM impairment. Right-sided TLE was associated with more severe deficits in recognition of fear, sadness, and disgust.ConclusionsSocial cognitive information processing is impaired in TLE, and the potential role of these deficits in functional impairment needs to be further investigated.