A differential neural response to threatening and non-threatening negative facial expressions in paranoid and non-paranoid schizophrenics

Several studies have demonstrated impaired facial expression recognition in schizophrenia. Few have examined the neural basis for this; none have compared the neural correlates of facial expression perception in different schizophrenic patient subgroups. We compared neural responses to facial expressions in 10 right-handed schizophrenic patients (five paranoid and five non-paranoid) and five normal volunteers using functional Magnetic Resonance Imaging (fMRI). In three 5-min experiments, subjects viewed alternating 30-s blocks of black-and-white facial expressions of either fear, anger or disgust contrasted with expressions of mild happiness. After scanning, subjects categorised each expression. All patients were less accurate in identifying expressions, and showed less activation to these stimuli than normals. Non-paranoids performed poorly in the identification task and failed to activate neural regions that are normally linked with perception of these stimuli. They categorised disgust as either anger or fear more frequently than paranoids, and demonstrated in response to disgust expressions activation in the amygdala, a region associated with perception of fearful faces. Paranoids were more accurate in recognising expressions, and demonstrated greater activation than non-paranoids to most stimuli. We provide the first evidence for a distinction between two schizophrenic patient subgroups on the basis of recognition of and neural response to different negative facial expressions.     

Is a lack of disgust something to fear? A functional magnetic resonance imaging facial emotion recognition study in euthymic bipolar disorder patients

OBJECTIVES: To determine the neural responses invoked in the recognition of facial fear and disgust in euthymic bipolar patients as compared with healthy subjects. METHODS: This study examined 10 female euthymic bipolar patients, and 10 suitably matched healthy subjects using functional magnetic resonance imaging (fMRI) while subjects were engaged in an explicit facial emotion recognition task involving fear, disgust and neutral expressions. The activation paradigm involved nominating the facial expression using specified response keys. Behavioural data were collected and analysed and both within-group (Fear versus Neutral; Disgust versus Neutral) and random-effects between-group analyses were performed on fMRI data using BrainVoyager (Brain Innovations, Maastricht, the Netherlands). RESULTS: Patients were equally accurate in identifying facial expressions as healthy subjects but were slower to respond, especially with respect to fear and disgust. Responses to fear and disgust (within-group analyses) resulted in activation of anticipated brain regions such as amygdala and insula, respectively. However, between-group random effects analysis revealed differential responses to both disgust and fear in both healthy subjects and euthymic bipolar patients such that euthymic bipolar patients responded largely to fear and healthy subjects responded more so to disgust. This partitioning of responsiveness was reflected by differential activation involving the hippocampus and amygdala. CONCLUSIONS: Greater responsiveness to fear with hippocampal activation in patients perhaps reflects recollection of traumatic events associated with past experiences of illness or simply the use of a more mnemonic (hippocampal) as opposed to affective (amygdala) approach when performing the task. It is possible that in bipolar disorder, prefrontal-subcortical network dysfunction that relegates neural processing to limbic regions is impaired and that clinically euthymic bipolar patients, although able to accurately and effectively identify emotions such as fear and disgust, are limited in their ability to interpret their salience. The implications of these findings are discussed.     

Depression is associated with increased sensitivity to signals of disgust: A functional magnetic resonance imaging study

Emotions of fear and disgust are related to core symptoms of depression. The neurobiological mechanisms of these associations are poorly understood. This functional magnetic resonance imaging study aimed at examining the Blood oxygenation level dependent (BOLD) response to facial expressions of fear and disgust in patients with major depressive disorder.Nine patients in an episode of major depression and nine healthy controls underwent two functional magnetic resonance imaging experiments where they judged the gender of facial identities displaying different degrees (mild, strong) of fear or disgust, intermixed with non-emotional faces.Compared with healthy controls, patients with depression demonstrated greater activation in left insula, left orbito-frontal gyrus, left middle/inferior temporal gyrus, and right middle/inferior temporal gyrus to expressions of strong disgust. Depressed patients also demonstrated reduced activation in left inferior parietal lobe to mildly fearful faces.Enhanced activation to facial expressions of disgust may reflect an emotion processing bias that suggests high relevance of emotion of disgust to depression.     

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.     

Disgust and Huntington's disease

The disproportionate impairment for the recognition of facial expressions of disgust in patients with Huntington's disease (HD) forms a double dissociation with the impaired recognition of fear that has been reported in amygdala patients. The dissociation has generated discussion regarding the potential existence of neural substrates dedicated to the recognition of facial signals of specific emotions. The aim of this study was to establish whether the impairment for disgust in HD was restricted solely to the domain of facial perception, or whether HD patients also demonstrate impairment in other kinds of disgust. Fourteen HD patients and fourteen age and education matched healthy controls participated in seven disparate emotion processing tasks. (1) A measure of knowledge for the situational determinants of distinct emotions; (2) recognition of emotion expressed in nonverbal vocalisations; (3) recognition of the emotional content of explicit lexical stimuli; (4) recognition of emotional content in pictures of emotion scenes; (5) a disgust experience questionnaire; (6) a measure of olfactory hedonic responsiveness; (7) a measure of gustatory perception. While verbal aspects of disgust processing were preserved, parallel impairments were revealed for olfactory disgust, vocal disgust expressions, the classification of disgusting pictures, and declarative knowledge of disgust elicitors. The finding of impaired perception of disgust signalled through different input domains suggests that the inability to recognise the facial expression in this population reflects a fundamental problem with disgust processing.     

An attention modulated response to disgust in human ventral anterior insula

The human brain is expert in analyzing rapidly and precisely facial features, especially emotional expressions representing a powerful communication vector. The involvement of insula in disgust recognition has been reported in behavioral and functional imaging studies. However, we do not know whether specific insular fields are involved in disgust processing nor what the processing time course is. Using depth electrodes implanted during presurgical evaluation of patients with drug-refractory temporal lobe epilepsy, we recorded intracerebral event-related potentials to human facial emotional expressions, that is, fear, disgust, happiness, surprise, and neutral expression. We studied evoked responses in 13 patients with insular contacts to specify the insular fields involved in disgust processing and assess the timing of their activation. We showed that specific potentials to disgust beginning 300 milliseconds after stimulus onset and lasting 200 milliseconds were evoked in the ventral anterior insula in four patients. The occurrence and latency of event-related potentials to disgust in the ventral anterior insula were affected by selective attention. The analysis of spatial and temporal characteristics of insular responses to disgust facial expression lead us to underline the crucial role of ventral anterior insula in the categorization of facial emotional expressions, particularly the disgust.     

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.     

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.     

Impaired recognition of facial emotion in mania

OBJECTIVE: Recognition of facial emotion was examined in manic subjects to explore whether aberrant interpersonal interactions are related to impaired perception of social cues. METHOD: Manic subjects with bipolar I disorder (N=8), euthymic subjects with bipolar I (N=8) or bipolar II (N=8) disorder, and healthy comparison subjects (N=10) matched pictures of faces to the words "fear," "disgust," "anger," "sadness," "surprise," and "happiness." RESULTS: The manic subjects showed worse overall recognition of facial emotion than all other groups. They showed worse recognition of fear and disgust than the healthy subjects. The euthymic bipolar II disorder subjects showed greater fear recognition than the manic and euthymic bipolar I disorder subjects. CONCLUSIONS: Impaired perception of facial emotion may contribute to behaviors in mania. Impaired recognition of fear and disgust, with relatively preserved recognition of other basic emotions, contrasts with findings for depression and is consistent with a mood-congruent positive bias.     

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.     

Defective emotion recognition in early HD is neuropsychologically and anatomically generic

Huntington's disease (HD) is an inherited neurodegenerative disorder that classically presents with motor, cognitive and psychiatric symptoms. However, other abnormalities also occur in this condition, notably deficient recognition of facial emotional expressions. Deficits in emotion recognition impact significantly on the lives of HD patients and their families and thus it is important to clarify the onset and pattern of impairment. This study investigated facial emotion recognition in a large cohort of early HD patients, and premanifest gene-carriers. We used voxel-based morphometry (VBM) to examine the neuroanatomical correlates of emotion recognition performance. Forty patients with early HD, 21 premanifest gene carriers and 20 controls were assessed using 24 faces from the Ekman Pictures of Facial Affect, and volumetric brain MRI. The HD group was significantly worse than controls at recognising, surprise, disgust, anger and fear, and worse than the premanifest group at recognising disgust and anger. When patient data were expressed as z-scores, recognition of anger was significantly worse than disgust in the early HD group. In the VBM analysis, these deficits were associated with common regional atrophy: impaired recognition of surprise, disgust, anger and fear were all associated with striatal volume loss. Fear was associated with additional atrophy of the right insula and left and right lateral orbitofrontal cortex. Even in early HD there is a wide-ranging impairment in recognition of negative emotions denoting 'threat'. Our findings implicate a generic fronto-subcortical network in the pathogenesis of these emotion recognition deficits.     

Recognition of facial expressions in obsessive-compulsive disorder

Sprengelmeyer et al. [Sprengelmeyer, R., Young, A. W., Pundt, I., Sprengelmeyer, A., Calder, A. J., Berrios, G., et al. (1997). Disgust implicated in obsessive-compulsive disorder. Proceedings of the Royal Society of London, 264, 1767-1773] found that patients with OCD showed severely impaired recognition of facial expressions of disgust. This result has potential to provide a unique window into the psychopathology of OCD, but several published attempts to replicate this finding have failed. The current study compared OCD patients to normal controls and panic disorder patients on ability to recognize facial expressions of negative emotions. Overall, the OCD patients were impaired in their ability to recognize disgust expressions, but only 33% of patients showed this deficit. These deficits were related to OCD symptom severity and general functioning, factors that may account for the inconsistent findings observed in different laboratories.     

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.     

Enhanced recognition of disgust in bipolar illness.

BACKGROUND: Bipolar disorder is associated with functional and structural abnormalities in the brain circuits involved in processing emotional stimuli. Although impairments of cognitive function have been found to persist in bipolar patients during periods of euthymic mood, it is not known whether abnormalities in emotional processing also occur during these periods of recovery. METHODS: The present investigation assessed the ability of euthymic patients with bipolar disorder to recognize different facial expressions of emotion, compared with matched controls. A nonemotional facial categorization task was used to control for possible nonspecific differences in perception or attention. RESULTS: In contrast to the small impairments seen in the nonemotional categorization task, patients with bipolar disorder showed a robust facilitation in the discrimination of disgusted facial expressions. The recognition of other basic negative and positive emotions was unchanged. CONCLUSIONS: The present results suggest a selective facilitation of the processes involved in recognizing facial expressions of disgust in patients with bipolar disorder. This difference in perception may be relevant to the decreased self-esteem and social functioning that have been associated with the euthymic phase of this disorder.     

Mixed emotions: alcoholics' impairments in the recognition of specific emotional facial expressions

Facial expression recognition is a central feature of emotional and social behaviour and previous studies have found that alcoholics are impaired in this skill when presented with single emotions of differing intensities. The aim of this study was to explore biases in alcoholics' recognition of emotions when they were a mixture of two closely related emotions. The amygdala is intimately involved in encoding of emotions, especially those related to fear. In animals an increased number of withdrawals from alcohol leads to increased seizure sensitivity associated with facilitated transmission in the amygdala and related circuits. A further objective therefore was to explore the effect of previous alcohol detoxifications on the recognition of emotional facial expressions. Fourteen alcoholic inpatients were compared with 14 age and sex matched social drinking controls. They were asked to rate how much of each of six emotions (happiness, surprise, fear, sadness, disgust and anger) were present in morphed pictures portraying a mix of two of those emotions. The alcoholic group showed enhanced fear responses to all of the pictures compared to the controls and showed a different pattern of responding on anger and disgust. There were no differences between groups on decoding of sad, happy and surprised expressions. In addition the enhanced fear recognition found in the alcoholic group was related to the number of previous detoxifications. These results provide further evidence for impairment in facial expression recognition present in alcoholic patients. In addition, since the amygdala has been associated with the processing of facial expressions of emotion, particularly those of fear, the present data furthermore suggest that previous detoxifications may be related to changes within the amygdala.     

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.     

Impaired recognition of musical emotions and facial expressions following anteromedial temporal lobe excision

We have shown that an anteromedial temporal lobe resection can impair the recognition of scary music in a prior study (Gosselin et al., 2005). In other studies ( [Adolphs et?al., 2001] and [Anderson et?al., 2000] ), similar results have been obtained with fearful facial expressions. These findings suggest that scary music and fearful faces may be processed by common cerebral structures. To assess this possibility, we tested patients with unilateral anteromedial temporal excision and normal controls in two emotional tasks. In the task of identifying musical emotion, stimuli evoked either fear, peacefulness, happiness or sadness. Participants were asked to rate to what extent each stimulus expressed these four emotions on 10-point scales. The task of facial emotion included morphed stimuli whose expression varied from faint to more pronounced and evoked fear, happiness, sadness, surprise, anger or disgust. Participants were requested to select the appropriate label. Most patients were found to be impaired in the recognition of both scary music and fearful faces. Furthermore, the results in both tasks were correlated, suggesting a multimodal representation of fear within the amygdala. However, inspection of individual results showed that recognition of fearful faces can be preserved whereas recognition of scary music can be impaired. Such a dissociation found in two cases suggests that fear recognition in faces and in music does not necessarily involve exactly the same cerebral networks and this hypothesis is discussed in light of the current literature.     

No disgust recognition deficit in obsessive-compulsive disorder

BACKGROUND: Patients with basal ganglia abnormalities misclassify facial expressions of disgust as expressions of anger when asked to identify the emotion depicted in photographs of individuals displaying different emotions. Sprengelmeyer, Young, Pundt et al. (1997) reported a similar disgust recognition deficit in patients with obsessive-compulsive disorder (OCD)--an anxiety disorder associated with basal ganglia abnormality. METHODS: In the present experiment, we attempted to replicate Sprengelmeyer, Young, Pundt et al.'s (1997) findings. RESULTS: We failed to replicate Sprengelmeyer, Young, Pundt et al.'s finding of disgust recognition deficits in OCD patients relative to healthy control subjects. One patient with especially severe OCD did, however, exhibit impairment by misclassifying disgust expressions as anger expressions. DISCUSSION: These data do not confirm the presence of disgust recognition deficits in individuals with OCD. In light of the deficits exhibited by one subject with severe OCD, disgust recognition deficits may be confined to an unidentified subset of people with OCD.     

The face of rejection: rejection sensitivity moderates dorsal anterior cingulate activity to disapproving facial expressions

Previous research has examined neural responses to threatening facial expressions such as those displaying anger, fear, and disgust. Here, we examined neural responses to a different type of threatening facial expression that primarily signifies a threat to social connection, namely a "disapproving" facial expression. We hypothesized that neural responses to disapproving facial expressions would be moderated by individual differences in rejection sensitivity. Using functional magnetic resonance imaging (fMRI), we scanned participants while they viewed brief video clips of facial expressions depicting disapproval, anger, and disgust. As expected, all three expressions yielded bilateral amygdala activation relative to a resting baseline. Additionally, individuals who scored higher on a measure of rejection sensitivity exhibited greater dorsal anterior cingulate cortex activity in response to disapproving facial expressions, but not in response to anger or disgust facial expressions. Results suggest that, at the neural level, individuals high in rejection sensitivity may be more sensitive to facial expressions signaling potential rejection, but not to threatening facial expressions in general. Results also suggest that disapproving facial expressions convey a distinct type of threat and should be considered in future studies of socially threatening facial expressions.