Facial fear processing and psychotic symptoms in schizophrenia: functional magnetic resonance imaging study

BACKGROUND: The recognition of negative facial affect is impaired in people with schizophrenia. The neural underpinnings of this deficit and its relationship to the symptoms of psychosis are still unclear. AIMS: To examine the association between positive and negative psychotic symptoms and activation within the amygdala and extrastriate visual regions of patients with schizophrenia during fearful and neutral facial expression processing. METHOD: Functional magnetic resonance imaging was used to measure neural responses to neutral and fearful facial expressions in 11 patients with schizophrenia and 9 healthy volunteers during an implicit emotional task. RESULTS: No association between amygdala activation and positive symptoms was found; the activation within the left superior temporal gyrus was negatively associated with the negative symptoms of the patients. CONCLUSIONS: Our results indicate an association between impaired extrastriate visual processing of facial fear and negative symptoms, which may underlie the previously reported difficulties of patients with negative symptoms in the recognition of facial fear.     

The face and its emotion: right N170 deficits in structural processing and early emotional discrimination in schizophrenic patients and relatives

Previous studies have reported facial emotion recognition impairments in schizophrenic patients, as well as abnormalities in the N170 component of the event-related potential. Current research on schizophrenia highlights the importance of complexly-inherited brain-based deficits. In order to examine the N170 markers of face structural and emotional processing, DSM-IV diagnosed schizophrenia probands (n=13), unaffected first-degree relatives from multiplex families (n=13), and control subjects (n=13) matched by age, gender and educational level, performed a categorization task which involved words and faces with positive and negative valence. The N170 component, while present in relatives and control subjects, was reduced in patients, not only for faces, but also for face-word differences, suggesting a deficit in structural processing of stimuli. Control subjects showed N170 modulation according to the valence of facial stimuli. However, this discrimination effect was found to be reduced both in patients and relatives. This is the first report showing N170 valence deficits in relatives. Our results suggest a generalized deficit affecting the structural encoding of faces in patients, as well as the emotion discrimination both in patients and relatives. Finally, these findings lend support to the notion that cortical markers of facial discrimination can be validly considered as vulnerability markers.     

Facial expression and sex recognition in schizophrenia and depression.

BACKGROUND: Impaired facial expression recognition in schizophrenia patients contributes to abnormal social functioning and may predict functional outcome in these patients. Facial expression processing involves individual neural networks that have been shown to malfunction in schizophrenia. Whether these patients have a selective deficit in facial expression recognition or a more global impairment in face processing remains controversial. OBJECTIVE: To investigate whether patients with schizophrenia exhibit a selective impairment in facial emotional expression recognition, compared with patients with major depression and healthy control subjects. METHODS: We studied performance in facial expression recognition and facial sex recognition paradigms, using original morphed faces, in a population with schizophrenia (n=29) and compared their scores with those of depression patients (n=20) and control subjects (n=20). RESULTS: Schizophrenia patients achieved lower scores than both other groups in the expression recognition task, particularly in fear and disgust recognition. Sex recognition was unimpaired. CONCLUSION: Facial expression recognition is impaired in schizophrenia, whereas sex recognition is preserved, which highly suggests an abnormal processing of changeable facial features in this disease. A dysfunction of the top-down retrograde modulation coming from limbic and paralimbic structures on visual areas is hypothesized.     

Deficits in facial affect recognition in unaffected siblings of Xhosa schizophrenia patients: evidence for a neurocognitive endophenotype

The present study in an African Xhosa sample examined whether familial vulnerability to schizophrenia is associated with deficits in facial affect recognition. Healthy comparison subjects, unaffected siblings of schizophrenia patients, and schizophrenia patients were tested with a task requiring rapid recognition of matched positive (happy), negative (angry), and neutral facial expressions. Siblings and patients demonstrated impaired recognition of negative relative to positive facial expressions whereas comparison subjects recognized negative and positive expressions at an equal level of accuracy. These results suggest that deficits in the processing negative affect from social cues are transmitted in families and may represent a heritable endophenotype of schizophrenia.     

Facial affect recognition in the course of schizophrenia

Deficits in facial affect recognition have been shown repeatedly in schizophrenia. However, the stability of this deficit over time remains to be clarified. A total of 36 remitted, 32 acutely ill schizophrenic patients and 21 healthy volunteers participated in a cross-sectional and longitudinal study. All subjects were assessed twice within 4 weeks (acute schizophrenics and normal controls), or 12 weeks, respectively (remitted schizophrenics). Subjects had to identify six basic emotions from corresponding facial expressions shown as photographs on a video screen. Both acute and remitted schizophrenics demonstrated a stable deficit over time in facial affect recognition unrelated to psychopathology and medication. This suggests that deficits in facial affect recognition in schizophrenia reflect a trait-like, rather than a state-dependent, characteristic.     

Impairment in the specificity of emotion processing in schizophrenia

OBJECTIVE: Deficits in emotion processing are a hallmark of schizophrenia, with consequences for social functioning and subjective well-being. However, their specificity and characteristics have not been ascertained psychometrically. The authors' purpose was to examine a differential deficit for processing emotional facets of the face compared to judgment of nonemotional features (age) and facial memory. The authors also sought to establish whether the deficit affects sensitivity or specificity of performance. METHOD: Participants were 20 patients with schizophrenia and 20 healthy subjects matched for age, gender, and parental education. The authors examined emotional discrimination abilities compared to age discrimination and recognition memory for faces with standardized faces displaying the universal emotions of happiness, sadness, anger, and fear. Percent correct in each condition and for each emotion were assessed as well as sensitivity (correct identification of a target emotion) and specificity (correct rejection of a nontarget emotion) for emotion recognition. RESULTS: Patients with schizophrenia were differentially impaired in the discrimination of emotional aspects of facial expressions compared to nonemotional aspects and memory. Within the emotional task, patients showed differential impairment in specificity and insensitivity to the emotion displayed. CONCLUSIONS: When identical stimuli were used across tasks, differential impairment was seen in patients with schizophrenia for processing emotional faces, although the nonemotional task proved harder for both groups. Impairment in the specificity of emotion identification may lead to misunderstanding of social communication and may underlie difficulties in social adjustment experienced by people with schizophrenia. Emotion discrimination tests could augment the neurobehavioral evaluation of patients.     

Impaired emotion perception in schizophrenia: a differential deficit

We investigated previously reported contradictory findings regarding the nature of deficits in emotion perception among patients with schizophrenia. Some studies have concluded that such deficits are due to a generalized impairment in visual processing of faces, while others have found it to be restricted to facial emotional expressions. We examined 37 patients and 32 healthy controls, matched on age and education, using three computerized tests: matching facial identity, matching facial emotional expressions, and discrimination of subtle differences in the valence of facial emotional expressions. Our results showed impaired matching of emotions in patients with schizophrenia. This impairment did not manifest on tasks that depended on perceiving the identity of faces or cues of the relative valence of facial emotional expressions. Our findings support the differential deficit hypothesis of emotion perception in schizophrenia.     

Perception of happy and sad facial expressions in chronic schizophrenia: evidence for two evaluative systems

BACKGROUND: Persons suffering from schizophrenia have impaired perception of emotional expressions, but it is not clear whether this is part of a generalized deficit in cognitive function. AIM: To test for existence of emotion-specific deficits by studying the effects of valence on recognition of facial emotional expressions. METHODS: 24 male subjects suffering from chronic schizophrenia were examined with two tests of perception of emotion: the Penn Emotion Acuity Test (PEAT 40) and the Emotion Differentiation Task (EMODIFF). Clinical state was assessed with the Scale for the Assessment of Negative Symptoms (SANS) and Scale for the Assessment of Positive Symptoms (SAPS), visual memory with the Benton Visual Retention Test (BVRT) and motor function with the finger tapping test. RESULTS: Identification of happy facial expressions showed significant negative correlation with age, cumulated time in hospital and length of current hospitalization; positive correlations were found with visual retention and finger tapping scores. Identification of sad facial expressions showed significant correlation only with cumulated time in hospital while identification of neutral facial expressions showed no significant correlations. Discrimination between degrees of happy but not sad facial expression showed a positive correlation with negative symptoms. CONCLUSION: Perception of happy and sad emotion relates differently to significant illness parameters. This differentiability supports the existence of an emotion-specific deficit in perception of emotions in schizophrenia and of separate channels for processing positive and negative emotions.     

Sustained attention in the context of emotional processing in patients with schizophrenia

Patients with schizophrenia show dysfunction in sustained attention and facial emotion processing. We investigated the interplay between sustained attention and emotion by presenting emotional faces as background during AX-CPT in patients with schizophrenia. Nineteen schizophrenia patients and 21 healthy control subjects participated. We presented AX-CPT number stimuli superimposed on the nose of background facial expressions (happy, neutral or sad) over three experimental blocks for each emotion. Signal detection sensitivity (A') and reaction time were measured. Patients showed a steeper sensitivity decline when happy faces (compared with sad faces) were presented as background stimuli. By contrast, controls' sensitivity was not affected by the background facial emotion stimuli. Across the emotion conditions, the decline of sensitivity over time was evident in patients, but not in controls. To our knowledge, the present study is the first to explore a change in sustained attention accompanied by simultaneous processing of emotional faces in schizophrenia patients. Our findings suggest that mechanisms underlying continuous performance test (CPT) performance decline over time and facial emotion deficit may interact with each other in patients with schizophrenia.     

Differential impairments of facial affect recognition in schizophrenia subtypes and major depression

The goal of this study was to assess facial affect recognition abilities in subjects with various schizophrenia subtypes and subjects with major depression. A total of six disorganized, 21 paranoid and 18 residual subjects with schizophrenia (DSM-IV criteria) were compared with 21 subjects with major depression (DSM-IV criteria) and 30 matched healthy control subjects. Two experimental tasks requiring the sorting and rating of emotional facial expressions were applied. Disorganized and paranoid subjects showed strong impairments in the sorting of emotional facial expressions. Depressive subjects displayed only minor deficits, and residual subjects were unimpaired. Subjects with disorganized schizophrenia rated emotional facial expressions as more aroused, and depressive subjects rated them as less aroused, than the other study groups. Our study demonstrates strong deficits in facial affect recognition in subjects with schizophrenia and pronounced disorganized or psychotic symptoms. Deficits in facial affect recognition are specific to schizophrenia. They may be considered as a state marker of schizophrenia.     

From neural signatures of emotional modulation to social cognition: individual differences in healthy volunteers and psychiatric participants

It is commonly assumed that early emotional signals provide relevant information for social cognition tasks. The goal of this study was to test the association between (a) cortical markers of face emotional processing and (b) social-cognitive measures, and also to build a model which can predict this association (a and b) in healthy volunteers as well as in different groups of psychiatric patients. Thus, we investigated the early cortical processing of emotional stimuli (N170, using a face and word valence task) and their relationship with the social-cognitive profiles (SCPs, indexed by measures of theory of mind, fluid intelligence, speed processing and executive functions). Group comparisons and individual differences were assessed among schizophrenia (SCZ) patients and their relatives, individuals with attention deficit hyperactivity disorder (ADHD), individuals with euthymic bipolar disorder (BD) and healthy participants (educational level, handedness, age and gender matched). Our results provide evidence of emotional N170 impairments in the affected groups (SCZ and relatives, ADHD and BD) as well as subtle group differences. Importantly, cortical processing of emotional stimuli predicted the SCP, as evidenced by a structural equation model analysis. This is the first study to report an association model of brain markers of emotional processing and SCP.     

Emotional information processing in violent patients with schizophrenia: association with psychopathy and symptomatology

Schizophrenia and psychopathy have been independently shown to be associated with deficits in the recognition of facial expressions. These disorders are highly co-morbid in forensic settings, and both are associated with aggressive behaviour. This study examines the relative contribution of psychopathic traits and psychotic symptoms to reported deficits in facial affect recognition in forensic patients with schizophrenia. Fifty-four male patients with schizophrenia were recruited from medium and high security hospitals. Participants were categorised into groups with high (HP), medium (MP) and low (LP) scores on the Psychopathy Checklist: Screening Version and based on symptomatology assessed using the Positive and Negative Syndrome Scale. Participants completed an animated facial affect recognition task assessing accuracy across the six basic emotions over high and low intensities. The HP group was found to have impaired recognition of sadness at low intensity compared with the LP group. In the overall sample, facial affect recognition for negatively valenced emotions was not related to positive or negative symptom scores. However, recognition accuracy for disgust was found to be negatively related to the severity of cognitive symptoms. Patients with high psychopathy scores and schizophrenia showed similar deficits in emotional information processing to those reported in the literature in non-psychotic psychopathic samples.     

Recognition memory for faces in schizophrenia patients and their first-degree relatives

It has consistently been shown that schizophrenia patients are impaired in recognition memory for faces. However, studies have not examined the specificity of this deficit relative to other cognitive functions nor the relationship between this deficit and particular schizophrenia symptoms. In addition, no studies have examined recognition memory for faces in unaffected biological relatives of schizophrenia patients who likely share some of the genetic diathesis for this disorder without presenting the potential confounds of mentally ill study samples. The Faces subtests from the Wechsler Memory Scale—Third Edition were used to evaluate recognition memory for faces in 39 schizophrenia patients, 33 of their first-degree relatives and 56 normal controls. Both schizophrenia patients and their relatives were impaired, relative to control participants, in recognition memory for faces after partialing out group differences in spatial attention or verbal memory. Further, recognition memory for faces was associated with positive symptoms in the schizophrenia group and schizotypal personality traits in the relative group. These findings may have important implications for reducing etiological heterogeneity among schizophrenia populations, identifying disorder susceptibility among their relatives and furthering understanding of disorder etiology.     

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.     

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.     

Impaired recognition of facial expressions of anger in Parkinson's disease patients acutely withdrawn from dopamine replacement therapy

We have previously reported that acute dopaminergic blockade in healthy volunteers results in a transient disruption of the recognition of facial expressions of anger, whilst leaving intact the recognition of other facial expressions (including fear and disgust) and facial identity processing. Parkinson's disease (PD) is characterised by cell loss in dopaminergic neuronal populations, and hence we predicted that PD would be associated with impaired anger recognition. We reasoned that treatment with dopamine replacement therapy (DRT) could mask any deficit present in PD, and therefore studied facial expression recognition in a group of PD patients transiently withdrawn from DRT. Seventeen PD patients were compared to 21 age- and IQ-matched controls on the Ekman 60 task, which required the forced-choice labelling of 10 exemplars of each of six facial expressions (anger, disgust, fear, sadness, happiness, surprise). In line with our predictions, PD patients showed a selective impairment in the recognition of facial expressions of anger. This deficit was not related to the PD patients' performance on the Benton unfamiliar-face matching task, which was normal, nor was the deficit related to overall disease severity, or to depression symptoms. However, as predicted by simulation theories, impaired anger recognition in PD was related to reduced levels of the anger-linked temperament trait, exploratory excitability. The results extend our previous findings of a role for dopamine in the processing of facial expressions of anger, and demonstrate the power of adopting a phylogenetic, comparative perspective on emotions.     

Symptom Correlates of Static and Dynamic Facial Affect Processing in Schizophrenia: Evidence of a Double Dissociation?

Schizophrenia patients have been shown to be compromised in their ability to recognize facial emotion. This deficit has been shown to be related to negative symptoms severity. However, to date, most studies have used static rather than dynamic depictions of faces. Nineteen patients with schizophrenia were compared with seventeen controls on 2 tasks; the first involving the discrimination of facial identity, emotion, and butterfly wings; the second testing emotion recognition using both static and dynamic stimuli. In the first task, the patients performed more poorly than controls for emotion discrimination only, confirming a specific deficit in facial emotion recognition. In the second task, patients performed more poorly in both static and dynamic facial emotion processing. An interesting pattern of associations suggestive of a possible double dissociation emerged in relation to correlations with symptom ratings: high negative symptom ratings were associated with poorer recognition of static displays of emotion, whereas high positive symptom ratings were associated with poorer recognition of dynamic displays of emotion. However, while the strength of associations between negative symptom ratings and accuracy during static and dynamic facial emotion processing was significantly different, those between positive symptom ratings and task performance were not. The results confirm a facial emotion-processing deficit in schizophrenia using more ecologically valid dynamic expressions of emotion. The pattern of findings may reflect differential patterns of cortical dysfunction associated with negative and positive symptoms of schizophrenia in the context of differential neural mechanisms for the processing of static and dynamic displays of facial emotion.     

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.     

Detecting subtle facial emotion recognition deficits in high-functioning Autism using dynamic stimuli of varying intensities

Autism Spectrum Disorders (ASD) are characterised by social and communication impairment, yet evidence for deficits in the ability to recognise facial expressions of basic emotions is conflicting. Many studies reporting no deficits have used stimuli that may be too simple (with associated ceiling effects), for example, 100% ‘full-blown’ expressions. In order to investigate subtle deficits in facial emotion recognition, 21 adolescent males with high-functioning Austism Spectrum Disorders (ASD) and 16 age and IQ matched typically developing control males completed a new sensitive test of facial emotion recognition which uses dynamic stimuli of varying intensities of expressions of the six basic emotions (Emotion Recognition Test; Montagne et al., 2007). Participants with ASD were found to be less accurate at processing the basic emotional expressions of disgust, anger and surprise; disgust recognition was most impaired - at 100% intensity and lower levels, whereas recognition of surprise and anger were intact at 100% but impaired at lower levels of intensity.     

Perception of emotions from faces and voices following unilateral brain damage

The importance of the right hemisphere in emotion perception in general has been well documented but its precise role is disputed. We compared the performance of 30 right hemisphere damaged (RHD) patients, 30 left hemisphere damaged (LHD) patients, and 50 healthy controls on both facial and vocal affect perception tasks of specific emotions. Brain damaged subjects had a single episode cerebrovascular accident localised to one hemisphere. The results showed that right hemisphere patients were markedly impaired relative to left hemisphere and healthy controls on test performance: labelling and recognition of facial expressions and recognition of emotions conveyed by prosody. This pertained at the level of individual basic emotions, positive versus negative, and emotional expressions in general. The impairment remained highly significant despite covarying for the group's poorer accuracy on a neutral facial perception test and identification of neutral vocal expressions. The LHD group were only impaired relative to controls on facial emotion tasks when their performance was summed over all the emotion categories and before age and other cognitive factors were taken into account. However, on the prosody test the LHD patients showed significant impairment, performing mid-way between the right hemisphere patients and healthy comparison group. Recognition of positive emotional expressions was better than negative in all subjects, and was not relatively poorer in the LHD patients. Recognition of individual emotions in one modality correlated weakly with recognition in another, in all three groups. These data confirm the primacy of the right hemisphere in processing all emotional expressions across modalities--both positive and negative--but suggest that left hemisphere emotion processing is modality specific. It is possible that the left hemisphere has a particular role in the perception of emotion conveyed through meaningful speech.