Impaired facial expression recognition in children with temporal lobe epilepsy: impact of early seizure onset on fear recognition

The amygdala has been implicated in the recognition of facial emotions, especially fearful expressions, in adults with early-onset right temporal lobe epilepsy (TLE). The present study investigates the recognition of facial emotions in children and adolescents, 8–16 years old, with epilepsy. Twenty-nine subjects had TLE (13 right, 16 left) and eight had fronto-central epilepsy (FCE). Each was matched on age and gender with a control subject. Subjects were asked to label the emotions expressed in pictures of children's faces miming five basic emotions (happiness, sadness, fear, disgust and anger) or neutrality (no emotion). All groups of children with epilepsy performed less well than controls. Patterns of impairment differed according to the topography of the epilepsy: the left-TLE (LTLE) group was impaired in recognizing fear and neutrality, the right-TLE (RTLE) group was impaired in recognizing disgust and, the FCE group was impaired in recognizing happiness. We clearly demonstrated that early seizure onset is associated with poor recognition of facial expression of emotion in TLE group, particularly for fear. Although right-TLE and left-TLE subjects were both impaired in the recognition of facial emotion, their psychosocial adjustment, as measured by the CBCL questionnaire [Achenbach, T. M. (1991). Manual for the Child Behavior Checklist and Youth Self-report. Burlington, VT: University of Vermont Department of Psychiatry], showed that poor recognition of fearful expressions was related to behavioral disorders only in children with right-TLE. Our study demonstrates for the first time that early-onset TLE can compromise the development of recognizing facial expressions of emotion in children and adolescents and suggests a link between impaired fear recognition and behavioral disorders.     

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.     

Recognition of emotions from faces and voices in medial temporal lobe epilepsy

Patients with chronic medial temporal lobe epilepsy (MTLE) can be impaired in different tasks that evaluate emotional or social abilities. In particular, the recognition of facial emotions can be affected (Meletti S, Benuzzi F, Rubboli G, et al. Neurology 2003;60:426-31. Meletti S, Benuzzi F, Cantalupo G, Rubboli G, Tassinari CA, Nichelli P. Epilepsia 2009;50:1547-59). To better understand the nature of emotion recognition deficits in MTLE we investigated the decoding of basic emotions in the visual (facial expression) and auditory (emotional prosody) domains in 41 patients. Results showed deficits in the recognition of both facial and vocal expression of emotions, with a strong correlation between performances across the two tasks. No correlation between emotion recognition and measures of IQ, quality of life (QOLIE-31), and depression (Beck Depression Inventory) was significant, except for a weak correlation between prosody recognition and IQ. These data suggest that emotion recognition impairment in MTLE is not dependent on the sensory channel through which the emotional stimulus is transmitted. Moreover, these findings support the notion that emotional processing is at least partly independent of measures of cognitive intelligence.     

A comparison of emotional and cognitive intelligence in people with and without temporal lobe epilepsy

Medial temporal lobe structures have been hypothesized to be important in emotional intelligence (EI) and social cognition. There is some evidence associating temporal lobe epilepsy (TLE) with impairments in social cognition. This study aimed to establish whether TLE is also associated with deficits in EI. Sixteen patients with TLE and 14 controls without epilepsy matched for age and current intelligence quotient were compared on measures of EI, recognition of facial expressions of emotion, and distress. Results indicated that patients with TLE showed both impaired EI and impaired recognition of facial expressions. They also reported greater psychological distress, which correlated negatively with EI. It is suggested that some of the psychosocial problems experienced by patients with TLE can be conceptualized as the consequences of deficits in EI, possibly resulting from epilepsy-related disruption to medial temporal lobe functioning.     

Facial emotion recognition after curative nondominant temporal lobectomy in patients with mesial temporal sclerosis

PURPOSE: The right (nondominant) amygdala is crucial for processing facial emotion recognition (FER). Patients with temporal lobe epilepsy (TLE) associated with mesial temporal sclerosis (MTS) often incur right amygdalar damage, resulting in impaired FER if TLE onset occurred before age 6 years. Consequently, early right mesiotemporal insult has been hypothesized to impair plasticity, resulting in FER deficits, whereas damage after age 5 years results in no deficit. The authors performed this study to test this hypothesis in a uniformly seizure-free postsurgical population. METHODS: Controls (n=10), early-onset patients (n=7), and late-onset patients (n=5) were recruited. All patients had nondominant anteromedial temporal lobectomy (AMTL), Wada-confirmed left-hemisphere language dominance and memory support, MTS on both preoperative MRI and biopsy, and were Engel class I 5 years postoperatively. By using a standardized (Ekman and Friesen) human face series, subjects were asked to match the affect of one of two faces to that of a simultaneously presented target face. Target faces expressed fear, anger, or happiness. RESULTS: Statistical analysis revealed that the early-onset group had significantly impaired FER (measured by percentage of faces correct) for fear (p=0.036), whereas the FER of the late-onset group for fear was comparable to that of controls. FER for anger and happiness was comparable across all three groups. CONCLUSIONS: Despite seizure control/freedom after AMTL, early TLE onset continues to impair FER for frightened expressions (but not for angry or happy expression), whereas late TLE onset does not impair FER, with no indication that AMTL resulted in FER impairment. These results indicate that proper development of the right amygdala is necessary for optimal fear recognition, with other neural processes unable to compensate for early amygdalar damage.     

Impaired Perception of Emotional Expression in Amyotrophic Lateral Sclerosis

MethodsTwenty-four patients with ALS and 24 age- and sex-matched healthy controls completed neuropsychological tests and facial emotion recognition tasks [ChaeLee Korean Facial Expressions of Emotions (ChaeLee-E)]. The ChaeLee-E test includes facial expressions for seven emotions: happiness, sadness, anger, disgust, fear, surprise, and neutral.ResultsThe ability to perceive facial emotions was significantly worse among ALS patients performed than among healthy controls [65.2±18.0% vs. 77.1±6.6% (mean±SD), p=0.009]. Eight of the 24 patients (33%) scored below the 5th percentile score of controls for recognizing facial emotions.ConclusionsEmotion perception deficits occur in Korean ALS patients, particularly regarding facial expressions of emotion. These findings expand the spectrum of cognitive and behavioral dysfunction associated with ALS into emotion processing dysfunction.     

Recognition of facial emotions and identity in patients with mesial temporal lobe and idiopathic generalized epilepsy: An eye-tracking study

PurposeTo describe visual scanning pattern for facial identity recognition (FIR) and emotion recognition (FER) in patients with idiopathic generalized (IGE) and mesial temporal lobe epilepsy (MTLE). Secondary endpoint was to correlate the results with cognitive function.MethodsBenton Facial Recognition Test (BFRT) and Ekman&Friesen series were performed for FIR and FER respectively in 23 controls, 20 IGE and 19 MTLE patients. Eye movements were recorded by a Hi-Speed eye-tracker system. Neuropsychological tools explored cognitive function.ResultsCorrect FIR rate was 78% in controls, 70.7% in IGE and 67.4% (p = 0.009) in MTLE patients. FER hits reached 82.7% in controls, 74.3% in IGE (p = 0.006) and 73.4% in MTLE (p = 0.002) groups. IGE patients failed in disgust (p = 0.005) and MTLE ones in fear (p = 0.009) and disgust (p = 0.03). FER correlated with neuropsychological scores, particularly verbal fluency (r = 0.542, p < 0.001). Eye-tracking revealed that controls scanned faces more diffusely than IGE and MTLE patients for FIR, who tended to top facial areas. A longer scanning of the top facial area was found in the three groups for FER. Gap between top and bottom facial region fixation time decreased in MTLE patients, with more but shorter fixations in bottom facial region. However, none of these findings were statistically significant.ConclusionFIR was impaired in MTLE patients, and FER in both IGE and MTLE, particularly for fear and disgust. Although not statistically significant, those with impaired FER tended to perform more diffuse eye-tracking over the faces and have cognitive dysfunction.     

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.     

Recognition of emotion from moving facial and prosodic stimuli in depressed patients

BACKGROUND: It has been suggested that depressed patients have a "negative bias" in recognising other people's emotions; however, the detailed structure of this negative bias is not fully understood. OBJECTIVES: To examine the ability of depressed patients to recognise emotion, using moving facial and prosodic expressions of emotion. METHODS: 16 depressed patients and 20 matched (non-depressed) controls selected one basic emotion (happiness, sadness, anger, fear, surprise, or disgust) that best described the emotional state represented by moving face and prosody. RESULTS: There was no significant difference between depressed patients and controls in their recognition of facial expressions of emotion. However, the depressed patients were impaired relative to controls in their recognition of surprise from prosodic emotions, judging it to be more negative. CONCLUSIONS: We suggest that depressed patients tend to interpret neutral emotions, such as surprise, as negative. Considering that the deficit was seen only for prosodic emotive stimuli, it would appear that stimulus clarity influences the recognition of emotion. These findings provide valuable information on how depressed patients behave in complicated emotional and social situations.     

Emotion recognition and experience in Huntington's disease: is there a differential impairment?

Findings on affective processing deficits in Huntington's disease (HD) have been inconsistent. It is still not clear whether HD patients are afflicted by specific deficits in emotion recognition and experience. We tested 28 symptomatic HD patients and presented them with pictures depicting facial expressions of emotions (Karolinska-Set) and with affective scenes (International Affective Picture System; IAPS). The faces were judged according to the displayed intensity of six basic emotions, whereas the scenes received intensity ratings for the elicited emotions in the viewer. Patients' responses were compared with those of 28 healthy controls. HD patients gave lower intensity ratings for facial expressions of anger, disgust and surprise than controls. Patients' recognition deficits were associated with reduced functional capacity, such as problems with social interactions. Moreover, their classification accuracy was reduced for angry, disgusted, sad and surprised faces. When judging affective scenes for the elicitation of happiness, disgust and fear, HD patients had a tendency to estimate them as more intense than controls. This finding points to a differential impairment in emotion recognition and emotion experience in HD. We found no significant correlations between emotion experience/recognition ratings and CAG repeats, symptom duration and UHDRS Motor Assessment in the patient group.     

Perception of facial expressions of emotion in bipolar disorder

OBJECTIVES: Some studies have reported deficits in the perception of facial expressions among depressed individuals compared with healthy controls, while others have reported negative biases in expression perception. We examined whether altered perception of emotion reflects an underlying trait-like effect in affective disorder by examining facial expression perception in euthymic bipolar patients. METHODS: Sensitivity to six different facial expressions, as well as accuracy of emotion recognition, was examined among 17 euthymic bipolar patients and 17 healthy controls using an interactive computer program. RESULTS: No differences were found between euthymic bipolar patients and controls in terms of sensitivity to any particular emotion. Although initial analysis of the data suggested impairment in the recognition of fear among the patients, identification of this emotion was not relatively impaired compared with that of the other emotions. CONCLUSIONS: The study did not find any conclusive evidence for trait-like deficits in the perception of facially conveyed emotions in bipolar disorder. Altered perception of facial expressions that has been found to accompany depressed mood may instead reflect mood-congruent biases.     

Do positive emotions predict symptomatic change in bipolar disorder?

Objectives:  Bipolar disorder is associated with positive emotion disturbance, though it is less clear which specific positive emotions are affected.
Methods:  The present study examined differences among distinct positive emotions in recovered bipolar disorder (BD) patients (n = 55) and nonclinical controls (NC) (n = 32) and whether they prospectively predicted symptom severity in patients with BD. At baseline, participants completed self-report measures of several distinct trait positive emotions. Structured assessments of diagnosis and current mood symptoms were obtained for BD participants. At a six-month follow-up, a subset of BD participants' (n = 39) symptoms were reassessed.
Results:  BD participants reported lower joy, compassion, love, awe, and contentment compared to NC participants. BD and NC participants did not differ in pride or amusement. For BD participants, after controlling for baseline symptom severity, joy and amusement predicted increased mania severity, and compassion predicted decreased mania severity at the six-month follow-up. Furthermore, amusement predicted increased depression severity and pride predicted decreased severity of depression. Awe, love, and contentment did not predict symptom severity.
Conclusions:  These results are consistent with a growing literature highlighting the importance of positive emotion in the course of bipolar disorder.     

Perception of emotional facial expressions at different intensities in early-symptomatic Huntington's disease

BACKGROUND: While there is abundant evidence that patients with Huntington's disease (HD) have an impairment in the recognition of the emotional facial expression of disgust, previous studies have only examined emotion perception using full-blown facial expressions. OBJECTIVE: The current study examines the perception of facial emotional expressions in HD at different levels of intensity to investigate whether more subtle deficits can be detected, possible also in other emotions. METHOD: We compared early symptomatic HD patients with healthy matched controls on emotion perception, presenting short video clips of a neutral face changing into one of the six basic emotions (happiness, anger, fear, surprise, disgust and sadness) with increasing intensity. Overall face perception ability as well as depressive symptoms were taken into account. RESULTS: A specific impairment in recognizing the emotions disgust and anger was found, which was present even at low emotion intensities. CONCLUSION: These results extend previous findings and support the use of more sensitive emotion perception paradigms, which enable the detection of subtle neurobehavioral deficits even in the pre- and early symptomatic stages of the disease.     

Impaired fear processing in right mesial temporal sclerosis: a fMRI study

Lesion and neuroimaging studies have demonstrated that the mesial temporal lobe is crucial for recognizing emotions from facial expressions. In humans, bilateral amygdala damage is followed by impaired recognition of facial expressions of fear. To evaluate the influence of unilateral mesial temporal lobe damage we examined recognition of facial expressions and functional magnetic resonance (fMRI) brain activation associated with incidental processing of fearful faces in thirteen mesial temporal lobe epilepsy (MTLE) patients (eight with right MTLE, five with left MTLE). We also examined the effect of early versus later damage, comparing subjects with hippocampal-amygdalar sclerosis (MTS) and seizures occurring before five years of age to epilepsy patients with late onset seizures. Fourteen healthy volunteers participated as controls. Neuropsychological testing demonstrated that the ability of right MTLE patients to recognize fearful facial expressions is impaired. Patients with early onset of seizures were the most severely impaired. This deficit was associated with defective activation of a neural network involved in the processing of fearful expressions, which in controls and left MTLE included the left inferior frontal cortex and several occipito-temporal structures of both hemispheres.     

The misclassification of facial expressions in generalised social phobia

The aim of this study was to investigate facial expression recognition (FER) accuracy in social phobia and in particular to explore how facial expressions of emotion were misclassified. We hypothesised that compared with healthy controls, subjects with social phobia would be no less accurate in their identification of facial emotions (as reported in previous studies) but that they would misclassify facial expressions as expressing threatening emotions (anger, fear or disgust). Thirty individuals with social phobia and twenty-seven healthy controls completed a FER task which featured six basic emotions morphed using computer techniques between 0 percent (neutral) and 100 percent intensity (full emotion). Supporting our hypotheses we found no differences between the groups on measures of the accuracy of emotion recognition but that compared with healthy controls the social phobia group were more likely both to misclassify facial expressions as angry and to interpret neutral facial expressions as angry. The healthy control group were more likely to misclassify neutral expressions as sad. The importance of the role of these biases in social phobia needs further replication but may help in understanding the disorder and provide an interesting area for future research and therapy.     

Diminished sensitivity and specificity at recognising facial emotional expressions of varying intensity underlie emotion-specific recognition deficits in autism spectrum disorders

BackgroundA plethora of research on facial emotion recognition in autism spectrum disorders (ASD) exists and reported deficits in ASD compared to controls, particularly for negative basic emotions. However, these studies have largely used static high intensity stimuli. The current study investigated facial emotion recognition across three levels of expression intensity from videos, looking at accuracy rates to investigate impairments in facial emotion recognition and error patterns (’confusions’) to explore potential underlying factors.MethodTwelve individuals with ASD (9 M/3F; M(age) = 17.3) and 12 matched controls (9 M/3F; M(age) = 16.9) completed a facial emotion recognition task including 9 emotion categories (anger, disgust, fear, sadness, surprise, happiness, contempt, embarrassment, pride) and neutral, each expressed by 12 encoders at low, intermediate, and high intensity.ResultsA facial emotion recognition deficit was found overall for the ASD group compared to controls, as well as deficits in recognising individual negative emotions at varying expression intensities. Compared to controls, the ASD group showed significantly more, albeit typical, confusions between emotion categories (at high intensity), and significantly more confusions of emotions as ‘neutral’ (at low intensity).ConclusionsThe facial emotion recognition deficits identified in ASD, particularly for negative emotions, are in line with previous studies using other types of stimuli. Error analysis showed that individuals with ASD had difficulties detecting emotional information in the face (sensitivity) at low intensity, and correctly identifying emotional information (specificity) at high intensity. These results suggest different underlying mechanisms for the facial emotion recognition deficits at low vs high expression intensity.     

An event related functional magnetic resonance imaging study of facial emotion processing in Asperger syndrome.

BACKGROUND: People with Asperger syndrome (AS) have life-long deficits in social behavior. The biological basis of this is unknown, but most likely includes impaired processing of facial emotion. Human social communication involves processing different facial emotions, and at different intensities. However nobody has examined brain function in people with AS when implicitly (unconsciously) processing four primary emotions at varying emotional intensities. METHODS: We used event-related functional magnetic resonance imaging (MRI) to examine neural responses when people with AS and controls implicitly processed neutral expressions, and mild (25%) and intense (100%) expressions of fear, disgust, happiness, and sadness. We included 18 right-handed adults; 9 with AS and 9 healthy controls who did not differ significantly in IQ. RESULTS: Both groups significantly activated 'face perception' areas when viewing neutral faces, including fusiform and extrastriate cortices. Further, both groups had significantly increased activation of fusiform and other extrastriate regions to increasing intensities of fear and happiness. However, people with AS generally showed fusiform and extrastriate hyporesponsiveness compared to controls across emotion types and intensities. CONCLUSIONS: Fusiform and extrastriate cortices are activated by facial expressions of four primary emotions in people with AS, but generally to a lesser degree than controls. This may partly explain the social impairments of people with AS.     

Alexithymia and impaired facial affect recognition in multiple sclerosis

Despite the high relevance of emotion processing for social functioning, the study of the impairment of facial affect in multiple sclerosis (MS) has received little attention. Previous research reported evidence for emotion processing deficits but the nature and extent are not fully explained. Thirty-five MS patients underwent dedicated neuropsychological assessment of emotion processing using two facial affect recognition tasks and self-report measures of alexithymia. For comparison, healthy participants served as controls. Relative to healthy controls, MS patients were impaired in facial affect recognition on four of the six Ekman basic emotions, except happiness and disgust. The MS patients were more alexithymic than the healthy controls. These data provide evidence for deficits in the recognition of emotional face expressions and emotional introspection.     

Misreading the facial signs: specific impairments and error patterns in recognition of facial emotions with negative valence in borderline personality disorder

Patients with borderline personality disorder (BPD) exhibit impairment in labeling of facial emotional expressions. However, it is not clear whether these deficits affect the whole domain of basic emotions, are valence-specific, or specific to individual emotions. Whether BPD patients' errors in a facial emotion recognition task create a specific pattern also remains to be elucidated. Our study tested two hypotheses: first, we hypothesized, that the emotion perception impairment in borderline personality disorder is specific to the negative emotion domain. Second, we hypothesized, that BPD patients would show error patterns in a facial emotion recognition task more commonly and more systematically than healthy comparison subjects. Participants comprised 33 inpatients with BPD and 32 matched healthy control subjects who performed a computerized version of the Ekman 60 Faces test. The indices of emotion recognition and the direction of errors were processed in separate analyses. Clinical symptoms and personality functioning were assessed using the Symptom Checklist-90-Revised and the Young Schema Questionnaire Long Form. Results showed that patients with BPD were less accurate than control participants in emotion recognition, in particular, in the discrimination of negative emotions, while they were not impaired in the recognition of happy facial expressions. In addition, patients over-attributed disgust and surprise and under-attributed fear to the facial expressions relative to controls. These findings suggest the importance of carefully considering error patterns, besides measuring recognition accuracy, especially among emotions with negative affective valence, when assessing facial affect recognition in BPD.     

Recognition of disgust is selectively preserved in Alzheimer's disease

The neural substrates that subserve decoding of different emotional expressions are subject to different rates of degeneration and atrophy in Alzheimer's disease (AD), and there is therefore reason to anticipate that a differentiated profile of affect recognition impairment may emerge. However, it remains unclear whether AD differentially affects the recognition of specific emotions. Further, there is only limited research focused on whether affect recognition deficits in AD generalize to more ecologically valid stimuli. In the present study, relatively mild AD participants (n = 24), older controls (n = 30) and younger controls (n = 30) were administered measures of affect recognition. Significant AD deficits were observed relative to both the younger and older control groups on a measure that involved labeling of static images of facial affect. AD deficits on this measure were observed in relation to all emotions assessed (anger, sadness, happiness, surprise and fear), with the exception of disgust, which was preserved even relative to the younger adult group. The relative preservation of disgust could not be attributed to biases in the choice of labels made, and it is suggested instead that this finding might reflect the relative sparing of the basal ganglia in AD. No significant AD effect was observed for the more ecologically valid measure that involved dynamic displays of facial expressions, in conjunction with paralinguistic and body movement cues, although a trend for greater AD difficulty was observed.