Facial emotion processing in schizophrenia: no evidence for a deficit specific to negative emotions in a differential deficit design

People with schizophrenia perform poorly when recognising facial expressions of emotion, particularly negative emotions such as fear. This finding has been taken as evidence of a "negative emotion specific deficit", putatively associated with a dysfunction in the limbic system, particularly the amygdala. An alternative explanation is that greater difficulty in recognising negative emotions may reflect a priori differences in task difficulty. The present study uses a differential deficit design to test the above argument. Facial emotion recognition accuracy for seven emotion categories was compared across three groups. Eighteen schizophrenia patients and one group of healthy age- and gender-matched controls viewed identical sets of stimuli. A second group of 18 age- and gender-matched controls viewed a degraded version of the same stimuli. The level of stimulus degradation was chosen so as to equate overall level of accuracy to the schizophrenia patients. Both the schizophrenia group and the degraded image control group showed reduced overall recognition accuracy and reduced recognition accuracy for fearful and sad facial stimuli compared with the intact-image control group. There were no differences in recognition accuracy for any emotion category between the schizophrenia group and the degraded image control group. These findings argue against a negative emotion specific deficit in schizophrenia.     

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.     

Emotional face processing deficit in schizophrenia: A replication study in a South African Xhosa population

Schizophrenia is associated with a deficit in the recognition of negative emotions from facial expressions. The present study examined the universality of this finding by studying facial expression recognition in African Xhosa population. Forty-four Xhosa patients with schizophrenia and forty healthy controls were tested with a computerized task requiring rapid perceptual discrimination of matched positive (i.e. happy), negative (i.e. angry), and neutral faces. Patients were equally accurate as controls in recognizing happy faces but showed a marked impairment in recognition of angry faces. The impairment was particularly pronounced for high-intensity (open-mouth) angry faces. Patients also exhibited more false happy and angry responses to neutral faces than controls. No correlation between level of education or illness duration and emotion recognition was found but the deficit in the recognition of negative emotions was more pronounced in familial compared to non-familial cases of schizophrenia. These findings suggest that the deficit in the recognition of negative facial expressions may constitute a universal neurocognitive marker of schizophrenia.     

Lower effective connectivity between amygdala and parietal regions in response to fearful faces in schizophrenia

Behavioral abnormalities related to processing negative emotions such as fear have been demonstrated in schizophrenia. The amygdala is strongly associated with fear processing, and alterations in amygdala function and structure have been demonstrated in schizophrenia. Further, functional disconnectivity has been attributed as key to the etiology of schizophrenia, with a number of lines of evidence supporting this theory. In the present study, we examine the effective connectivity corresponding to fear processing, from the amygdala to the whole brain, and compare this between patients with schizophrenia and control participants. An implicit facial emotion processing task was performed by 19 patients with schizophrenia and 24 matched controls during fMRI scanning. During the task, participants made gender judgments from facial images with either neutral or fearful emotion. Neural response to fearful images versus neutral was used as contrast of interest to estimate effective connectivity between the amygdala and the whole brain using the psycho-physiological interactions approach. This connectivity was compared between patients with schizophrenia and healthy controls. We show that when looking at fearful compared to neutral faces patients with schizophrenia show significantly reduced effective connectivity from the amygdala to a large cluster of regions including parts of the precuneus and parietal lobe, compared to healthy controls. These regions have been associated with emotion processing and high level social cognition tasks involving self related processing and mental representations about other people. The reduced amygdala connectivity in schizophrenia shown here further illuminates the neural basis for the behavioral abnormalities in emotional and social function found in the disorder.     

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.     

Amygdala reactivity to masked negative faces is associated with automatic judgmental bias in major depression: a 3 T fMRI study

OBJECTIVE: In a previous study, we demonstrated that amygdala reactivity to masked negative facial emotions predicts negative judgmental bias in healthy subjects. In the present study, we extended the paradigm to a sample of 35 inpatients suffering from depression to investigate the effect of amygdala reactivity on automatic negative judgmental bias and clinical characteristics in depression. METHODS: Amygdala activity was recorded in response to masked displays of angry, sad and happy facial expressions by means of functional magnetic resonance imaging at 3 T. In a subsequent experiment, the patients performed an affective priming task that characterizes automatic emotion processing by investigating the biasing effect of subliminally presented emotional faces on evaluative ratings to subsequently presented neutral stimuli. RESULTS: Significant associations between (right) amygdala reactivity and automatic negative judgmental bias were replicated in our patient sample (r=-0.59, p<0.001). Further, negatively biased evaluative processing was associated with severity and longer course of illness (r=-0.57, p=0.001). CONCLUSION: Amygdala hyperactivity is a neural substrate of negatively biased automatic emotion processing that could be a determinant for a more severe disease course.     

An analysis of categorical perception of facial emotion in schizophrenia

BACKGROUND: Emotion perception deficits have been extensively documented in schizophrenia and are associated with poor social functioning. Yet fundamental questions about the nature and scope of these impairments remain unanswered from commonly used experimental tasks. An alternative categorical perception paradigm that focuses on distinguishing boundaries between emotions was used to evaluate whether schizophrenia patients demonstrate atypical patterns of categorical perception and a negativity bias in the identification of ambiguous facial expressions. METHOD: 47 schizophrenia outpatients and 31 nonpsychiatric controls completed a forced-choice emotion identification task. Stimuli consisted of a series of digitized facial images that were morphed in 10% signal intensity increments along continua between pairs of emotions (happy-sad; fearful-happy; angry-fearful; angry-sad) and presented in a random order. For each emotion continuum, measures of the response slope and the location of the boundary shift point between emotions were calculated for each group. RESULTS: The schizophrenia group demonstrated significantly shallower response curves than controls across all emotion continua. Despite these generally less precise demarcations between emotions, patients did not significantly differ from controls in the location of the shift point between emotions on any of the continua. CONCLUSIONS: Schizophrenia patients demonstrated impaired categorical perception of facial expressions with generally less sharp categorizations of ambiguous stimuli to one emotion category or another. However, patients did not demonstrate a negativity bias in their processing of ambiguous facial expressions. The emotional continuum paradigm can help to clarify the nature and boundaries of affect perception deficits in schizophrenia.     

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.     

Recognition of facial emotion in nine individuals with bilateral amygdala damage.

Findings from several case studies have shown that bilateral amygdala damage impairs recognition of emotions in facial expressions, especially fear. However, one study did not find such an impairment, and, in general, comparison across studies has been made difficult because of the different stimuli and tasks employed. In a collaborative study to facilitate such comparisons, we report here the recognition of emotional facial expressions in nine subjects with bilateral amygdala damage, using a sensitive and quantitative assessment. Compared to controls, the subjects as a group were significantly impaired in recognizing fear, although individual performances ranged from severely impaired to essentially normal. Most subjects were impaired on several negative emotions in addition to fear, but no subject was impaired in recognizing happy expressions. An analysis of response consistency showed that impaired recognition of fear could not be attributed simply to mistaking fear for another emotion. While it remains unclear why some subjects with amygdala damage included here are not impaired on our task, the results overall are consistent with the idea that the amygdala plays an important role in triggering knowledge related to threat and danger signaled by facial expressions.     

Differential amygdala response during facial recognition in patients with schizophrenia: an fMRI study

Human lesion or neuroimaging studies suggest that amygdala is involved in facial emotion recognition. Although impairments in recognition of facial and/or emotional expression have been reported in schizophrenia, there are few neuroimaging studies that have examined differential brain activation during facial recognition between patients with schizophrenia and normal controls. To investigate amygdala responses during facial recognition in schizophrenia, we conducted a functional magnetic resonance imaging (fMRI) study with 12 right-handed medicated patients with schizophrenia and 12 age- and sex-matched healthy controls. The experiment task was a type of emotional intensity judgment task. During the task period, subjects were asked to view happy (or angry/disgusting/sad) and neutral faces simultaneously presented every 3 s and to judge which face was more emotional (positive or negative face discrimination). Imaging data were investigated in voxel-by-voxel basis for single-group analysis and for between-group analysis according to the random effect model using Statistical Parametric Mapping (SPM). No significant difference in task accuracy was found between the schizophrenic and control groups. Positive face discrimination activated the bilateral amygdalae of both controls and schizophrenics, with more prominent activation of the right amygdala shown in the schizophrenic group. Negative face discrimination activated the bilateral amygdalae in the schizophrenic group whereas the right amygdala alone in the control group, although no significant group difference was found. Exaggerated amygdala activation during emotional intensity judgment found in the schizophrenic patients may reflect impaired gating of sensory input containing emotion.     

Brain correlates of musical and facial emotion recognition: evidence from the dementias

The recognition of facial expressions of emotion is impaired in semantic dementia (SD) and is associated with right-sided brain atrophy in areas known to be involved in emotion processing, notably the amygdala. Whether patients with SD also experience difficulty recognizing emotions conveyed by other media, such as music, is unclear. Prior studies have used excerpts of known music from classical or film repertoire but not unfamiliar melodies designed to convey distinct emotions. Patients with SD (n = 11), Alzheimer's disease (n = 12) and healthy control participants (n = 20) underwent tests of emotion recognition in two modalities: unfamiliar musical tunes and unknown faces as well as volumetric MRI. Patients with SD were most impaired with the recognition of facial and musical emotions, particularly for negative emotions. Voxel-based morphometry showed that the labelling of emotions, regardless of modality, correlated with the degree of atrophy in the right temporal pole, amygdala and insula. The recognition of musical (but not facial) emotions was also associated with atrophy of the left anterior and inferior temporal lobe, which overlapped with regions correlating with standardized measures of verbal semantic memory. These findings highlight the common neural substrates supporting the processing of emotions by facial and musical stimuli but also indicate that the recognition of emotions from music draws upon brain regions that are associated with semantics in language.     

Amygdala reactivity predicts automatic negative evaluations for facial emotions

The amygdala is a key structure in a limbic circuit involved in the rapid and unconscious processing of facial emotions. In the present study, the role of the amygdala in automatic, involuntary appraisal processes, which are believed to be a crucial component of emotion processing, was investigated in 23 healthy subjects. Amygdala activity was recorded in response to masked displays of angry, sad, and happy facial expressions using functional magnetic resonance imaging (fMRI). In a subsequent experiment, the subjects performed a masked affective priming task that characterizes automatic emotion processing by investigating the biasing effect of subliminally presented emotional faces on evaluative ratings to subsequently presented neutral stimuli. In the affective priming task, significant valence-congruent evaluation manipulation was observed. Subjects rated neutral targets more positively if they were primed by happy faces. Significant correlations were found between amygdala responses to masked negative facial expressions and negative evaluation shifts elicited by the corresponding emotion quality in the affective priming task. Spontaneous amygdala reactivity to facial emotions appears to be a determinant of automatic negative evaluative response tendencies. This finding might shed some light on how amygdala hyperresponsivity contributes to negative cognitive biases commonly observed in affective disorders.     

Imaging the up’s and down’s of emotion regulation in lifetime depression

Reappraisal is a particularly effective strategy for influencing emotional experiences, specifically for reducing the impact of negative stimuli. Although depression has repeatedly been linked to dysfunctional behavioral and neural emotion regulation, prefrontal and amygdala engagement seems to vary with clinical characteristics and the specific regulation strategy used. Whereas previous neuroimaging research has focused on down-regulating reactions to emotionally evocative scenes, the current study compared up- and down-regulation in response to angry facial expressions in patients with depression and healthy individuals. During the initial viewing of faces, patients with depression showed hypoactivation particularly in areas implicated in emotion generation, i.e., amygdala, insula and putamen. In contrast, up-regulating negative emotions yielded stronger recruitment of core face processing areas and posterior medial frontal cortex in patients than in controls. However, group differences did not extend to resting-state functional connectivity. Recurrent depression was inversely associated with amygdala activation specifically during down-regulation, but differences in medication status may limit the current findings. Despite a pattern of reduced neural emotional reactivity in mainly medicated patients, their ‘successful’ recruitment of the regulation network for up-regulation might point toward an effective use of reappraisal when increasing negative emotions. Future studies need to address how patients might benefit from transferring this ability to adaptive goals, such as improving interpersonal emotion regulation.     

Amygdala damage impairs emotion recognition from scenes only when they contain facial expressions

Bilateral damage to the human amygdala impairs recognition of negatively valenced emotions from facial expressions, but it is unclear if this finding generalizes to richer visual stimuli that contain cues in addition to faces. We investigated this issue in 4 subjects with bilateral amygdala damage, 23 with unilateral amygdala damage, 22 brain-damaged controls and 16 normal individuals. Subjects were shown two blocks of complex social scenes; all stimuli in the two blocks were identical, except that the first block had all facial expressions in the image erased. While control subjects were more accurate in recognizing emotions when facial expressions were present, subjects with bilateral amygdala damage did not show the same benefit for negative emotions, often performing equivalently across the two conditions. Most striking, subjects with bilateral amygdala damage were more accurate in recognizing scenes showing anger with faces erased than with faces present, an effect resulting in part from highly abnormal recognition of certain angry facial expressions. All four subjects with bilateral amygdala damage were impaired in recognizing angry faces shown in isolation, and frequently mistook expressions of anger for smiles, a mistake never made by any control subject. Bilateral amygdala damage thus disproportionately impairs recognition of certain emotions from complex visual stimuli when subjects utilize information from facial expressions.     

Basic emotions and psychological distress: association between recognition of facial expressions and Symptom Checklist-90 subscales

OBJECTIVE: Cross-cultural studies have demonstrated universal similarity in the recognition and expression of basic emotions in facial expressions. The so-called mood congruency effect, observed primarily in clinical populations, implies that subjects with depressed mood tend to judge positive emotions as neutral and neutral faces as negative. The objective was to investigate whether a mood congruency effect can be detected in case of mild impairments among healthy subjects. First, it was hypothesized that subjects with mild psychiatric symptom distress have poorer performance in affective facial recognition in general. Second, it was also hypothesized that these subjects have poorer functioning in neutral face recognition and that they are prone to attribute negative emotions, for example, sadness and fear to neutral faces. Third, it was also assumed that people with mild psychiatric symptom distress have poor performance in recognizing positive emotions. METHODS: Pictures representing the basic emotions were used to examine the recognition of facial emotions; the Symptom Checklist-90 was obtained to quantify overall psychological distress and the severity of psychiatric symptoms on 9 primary symptom dimensions, including somatization, obsessive-compulsive, interpersonal sensitivity, depression, anxiety, hostility, phobic anxiety, paranoid ideation, and psychoticism. One hundred seventeen healthy volunteers were recruited for the purpose of the study. RESULTS: Consistent with the first hypothesis, results indicated a significant negative association between the overall recognition rate of facial expressions and the level of psychiatric symptoms in a healthy population. Consistent with the second hypothesis, the level of psychiatric symptoms was related inversely with the neutral facial expression recognition and directly with the negative bias in neutral facial expressions. However, our data did not support the assumption that people with mild psychiatric symptom distress would have a poorer performance in recognizing positive emotions. CONCLUSIONS: These findings support the notion that difficulties in emotion processing in general and in neutral face recognition, including a negative bias in particular, are strongly related to psychological distress and the severity of psychiatric symptoms in a healthy population.     

Perceiving emotions in neutral faces: expression processing is biased by affective person knowledge

According to a widely held view, basic emotions such as happiness or anger are reflected in facial expressions that are invariant and uniquely defined by specific facial muscle movements. Accordingly, expression perception should not be vulnerable to influences outside the face. Here, we test this assumption by manipulating the emotional valence of biographical knowledge associated with individual persons. Faces of well-known and initially unfamiliar persons displaying neutral expressions were associated with socially relevant negative, positive or comparatively neutral biographical information. The expressions of faces associated with negative information were classified as more negative than faces associated with neutral information. Event-related brain potential modulations in the early posterior negativity, a component taken to reflect early sensory processing of affective stimuli such as emotional facial expressions, suggest that negative affective knowledge can bias the perception of faces with neutral expressions toward subjectively displaying negative emotions.     

Influence of Emotional Processing on Working Memory in Schizophrenia

Research on emotional processing in schizophrenia suggests relatively intact subjective responses to affective stimuli “in the moment.” However, neuroimaging evidence suggests diminished activation in brain regions associated with emotional processing in schizophrenia. We asked whether given a more vulnerable cognitive system in schizophrenia, individuals with this disorder would show increased or decreased modulation of working memory (WM) as a function of the emotional content of stimuli compared with healthy control subjects. In addition, we examined whether higher anhedonia levels were associated with a diminished impact of emotion on behavioral and brain activation responses. In the present study, 38 individuals with schizophrenia and 32 healthy individuals completed blocks of a 2-back WM task in a functional magnetic resonance imaging scanning session. Blocks contained faces displaying either only neutral stimuli or neutral and emotional stimuli (happy or fearful faces), randomly intermixed and occurring both as targets and non-targets. Both groups showed higher accuracy but slower reaction time for negative compared to neutral stimuli. Individuals with schizophrenia showed intact amygdala activity in response to emotionally evocative stimuli, but demonstrated altered dorsolateral prefrontal cortex (DLPFC) and hippocampal activity while performing an emotionally loaded WM-task. Higher levels of social anhedonia were associated with diminished amygdala responses to emotional stimuli and increased DLPFC activity in individuals with schizophrenia. Emotional arousal may challenge dorsal-frontal control systems, which may have both beneficial and detrimental influences. Our findings suggest that disturbances in emotional processing in schizophrenia relate to alterations in emotion-cognition interactions rather than to the perception and subjective experience of emotion per se.     

ADHD and schizophrenia phenomenology: visual scanpaths to emotional faces as a potential psychophysiological marker?

Commonalities in the clinical phenomenology and psychopharmacology of ADHD and schizophrenia are reviewed. The potential of psychostimulants to produce psychotic symptoms emphasizes the need for objective psychophysiological distinctions between these disorders. Impaired emotion perception in both disorders is discussed. It is proposed that visual scanpaths to facial expressions of emotion might prove a potentially useful psychophysiological distinction between ADHD and schizophrenia. There is consistent evidence that both facial affect recognition and scanpaths to facial expressions are impaired in schizophrenia, with emerging empirical evidence showing that facial affect recognition is impaired in ADHD also. Brain imaging studies show reduced activity in the medial prefrontal and limbic (amygdala) brain regions required to process emotional faces in schizophrenia, but suggest more localized loss of activity in these regions in ADHD. As amygdala activity in particular has been linked to effective visual scanning of face stimuli, it is postulated that condition-specific breakdowns in these brain regions that subserve emotional behavior might manifest as distinct scanpath aberrations to facial expressions of emotion in schizophrenia and ADHD.     

The Change in Facial Emotion Recognition Ability in Inpatients with Treatment Resistant Schizophrenia After Electroconvulsive Therapy

People with schizophrenia have impairments in emotion recognition along with other social cognitive deficits. In the current study, we aimed to investigate the immediate benefits of ECT on facial emotion recognition ability. Thirty-two treatment resistant patients with schizophrenia who have been indicated for ECT enrolled in the study. Facial emotion stimuli were a set of 56 photographs that depicted seven basic emotions: sadness, anger, happiness, disgust, surprise, fear, and neutral faces. The average age of the participants was 33.4 ± 10.5 years. The rate of recognizing the disgusted facial expression increased significantly after ECT (p < 0.05) and no significant changes were found in the rest of the facial expressions (p > 0.05). After the ECT, the time period of responding to the fear and happy facial expressions were significantly shorter (p < 0.05). Facial emotion recognition ability is an important social cognitive skill for social harmony, proper relation and living independently. At least, the ECT sessions do not seem to affect facial emotion recognition ability negatively and seem to improve identifying disgusted facial emotion which is related with dopamine enriched regions in brain.     

A multidimensional assessment of social cognition in psychometrically defined schizotypy

Individuals with schizophrenia exhibit impairments in multiple social cognitive domains. There is evidence that these impairments may be trait-related vulnerability markers for schizophrenia. However, the literature focusing on individuals vulnerable to developing schizophrenia-spectrum disorders, referred to as schizotypy, has produced inconsistent findings. This study's primary aim was to provide a more comprehensive understanding of social cognitive functioning within schizotypy than previous studies by employing a broad array of measures to assess multiple social cognitive domains, and examine how these domains relate to specific schizotypy traits (i.e., positive, negative, and disorganized) and Quality of Life (QOL). Facial emotion recognition, Theory of Mind (ToM), and aspects of emotional intelligence related to regulating one's own emotions (emotion management) and other's emotions (social management) were measured. Individuals with psychometrically defined schizotypy (n=36) and controls (n=26) were examined. The schizotypy group performed significantly worse than controls on facial emotion recognition, ToM, and emotion management, but not social management. Generally speaking, poorer social cognition performance was not a function of specific schizotypy traits. However, negative traits were associated with poorer facial emotion recognition, and disorganized traits were associated with better social management. Facial emotion recognition was associated with QOL in the schizotypy group.