Deficits in facial affect recognition among antisocial populations: a meta-analysis

Individuals with disorders marked by antisocial behavior frequently show deficits in recognizing displays of facial affect. Antisociality may be associated with specific deficits in identifying fearful expressions, which would implicate dysfunction in neural structures that subserve fearful expression processing. A meta-analysis of 20 studies was conducted to assess: (a) if antisocial populations show any consistent deficits in recognizing six emotional expressions; (b) beyond any generalized impairment, whether specific fear recognition deficits are apparent; and (c) if deficits in fear recognition are a function of task difficulty. Results show a robust link between antisocial behavior and specific deficits in recognizing fearful expressions. This impairment cannot be attributed solely to task difficulty. These results suggest dysfunction among antisocial individuals in specified neural substrates, namely the amygdala, involved in processing fearful facial affect.     

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.     

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.     

Conscious and unconscious processing of fear after right amygdala damage: A single case ERP-study

In this study, we describe a 58-year-old male patient (FZ) with a right-amygdala lesion after temporal lobe infarction. FZ is unable to recognize fearful facial expressions. Instead, he consistently misinterprets expressions of fear for expressions of surprise. Employing EEG/ERP measures, we investigated whether presentation of fearful and surprised facial expressions would lead to different response patterns. We also measured ERPs to aversively conditioned and unconditioned fearful faces.

We compared ERPs elicited by supraliminally and subliminally presented conditioned fearful faces (CS+), unconditioned fearful faces (CS–) and surprised faces. Despite FZ's inability to recognize fearful facial expressions in emotion recognition tasks, ERP components showed different response patterns to pictures of surprised and fearful facial expressions, indicating that covert or implicit recognition of fear is still intact.

Differences between ERPs to CS+ and CS– were only found when these stimuli were presented subliminally. This indicates that intact right amygdala function is not necessary for aversive conditioning.

Previous studies have stressed the importance of the right amygdala for discriminating facial emotional expressions and for classical conditioning. Our study suggests that the right amygdala is necessary for explicit recognition of fear, while implicit recognition of fear and classical conditioning may still occur following lesion of the right amygdala.     

Processing of emotional facial expressions in Korsakoff's syndrome

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

Mind your left: spatial bias in subcortical fear processing

Hemispheric lateralization of emotional processing has long been suggested, but its underlying neural mechanisms have not yet been defined. In this functional magnetic resonance imaging study, facial expressions were presented to 10 right-handed healthy adult females in an event-related visual half-field presentation paradigm. Differential activations to fearful versus neutral faces were observed in the amygdala, pulvinar, and superior colliculus only for faces presented in the left hemifield. Interestingly, the left hemifield advantage for fear processing was observed in both hemispheres. These results suggest a leftward bias in subcortical fear processing, consistent with the well-documented leftward bias of danger-associated behaviors in animals. The current finding highlights the importance of hemifield advantage in emotional lateralization, which might reflect the combination of hemispheric dominance and asymmetric interhemispheric information transfer.     

Neural mechanisms of facial recognition]

We review recent researches in neural mechanisms of facial recognition in the light of three aspects: facial discrimination and identification, recognition of facial expressions, and face perception in itself. First, it has been demonstrated that the fusiform gyrus has a main role of facial discrimination and identification. However, whether the FFA (fusiform face area) is really a special area for facial processing or not is controversial; some researchers insist that the FFA is related to 'becoming an expert' for some kinds of visual objects, including faces. Neural mechanisms of prosopagnosia would be deeply concerned to this issue. Second, the amygdala seems to be very concerned to recognition of facial expressions, especially fear. The amygdala, connected with the superior temporal sulcus and the orbitofrontal cortex, appears to operate the cortical function. The amygdala and the superior temporal sulcus are related to gaze recognition, which explains why a patient with bilateral amygdala damage could not recognize only a fear expression; the information from eyes is necessary for fear recognition. Finally, even a newborn infant can recognize a face as a face, which is congruent with the innate hypothesis of facial recognition. Some researchers speculate that the neural basis of such face perception is the subcortical network, comprised of the amygdala, the superior colliculus, and the pulvinar. This network would relate to covert recognition that prosopagnosic patients have.     

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.     

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.     

Fear recognition deficits after focal brain damage: a cautionary note

OBJECTIVE: To test the hypothesis that fear recognition deficits in neurologic patients reflect damage to an emotion-specific neural network. BACKGROUND: Previous studies have suggested that the perception of fear in facial expressions is mediated by a specialized neural system that includes the amygdala and certain posterior right-hemisphere cortical regions. However, the neuropsychological findings in patients with amygdala damage are inconclusive, and the contribution of distinct cortical regions to fear perception has only been examined in one study. Methods: We studied the recognition of six basic facial expressions by asking subjects to match these emotions with the appropriate verbal labels. RESULTS: Both normal control subjects (n = 80) and patients with focal brain damage (n = 63) performed significantly worse in recognizing fear than in recognizing any other facial emotion, with errors consisting primarily of mistaking fear for surprise. Although patients were impaired relative to control subjects in recognizing fear, we could not obtain convincing evidence that left, right, or bilateral lesions were associated with disproportionate impairments of fear perception once we adjusted for differences in overall recognition performance for the other five facial emotion categories. The proposed special role of the amygdala and posterior right-hemisphere cortical regions in fear perception was also not supported. CONCLUSIONS: Fear recognition deficits in neurologic patients may be attributable to task difficulty factors rather than damage to putative neural systems dedicated to fear perception.     

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.     

Common and unique impairments in facial-expression recognition in pervasive developmental disorder-not otherwise specified and Asperger's disorder

This study was designed to identify specific difficulties and associated features related to the problems with social interaction experienced by individuals with pervasive developmental disorder-not otherwise specified (PDD-NOS) using an emotion-recognition task. We compared individuals with PDD-NOS or Asperger's disorder (ASP) and typically developing individuals in terms of their ability to recognize facial expressions conveying the six basic emotions. Individuals with PDD-NOS and ASP were worse at recognizing fearful faces than were controls. Individuals with PDD-NOS were less accurate in recognizing disgusted faces than were those with ASP. The results suggest that PDD subtypes are characterized by shared and unique impairments in the ability to recognize facial expressions. Furthermore, the ability to recognize fearful but not disgusted expressions was negatively correlated with the severity of social dysfunction in PDD-NOS and ASP. The results suggest that impaired recognition of fearful and disgusted faces may reflect the severity of social dysfunction across PDD subtypes and the specific problems associated with PDD-NOS, respectively. Characteristics associated with different levels of symptom severity in PDD-NOS are discussed in terms of similarities with brain damage and other psychiatric disorders.     

Affective blindsight in the intact brain: neural interhemispheric summation for unseen fearful expressions

The emotional valence of facial expressions can be reliably discriminated even in the absence of conscious visual experience by patients with lesions to the primary visual cortex (affective blindsight). Prior studies in one such patient (GY) also showed that this non-conscious perception can influence conscious recognition of normally seen emotional faces. Here we report a similar online interaction across hemispheres between conscious and non-conscious perception of emotions in normal observers. Fearful and happy facial expressions were presented either unilaterally (to the left or right visual field) or simultaneously to both visual fields. In bilateral displays, conscious perception of one face in a pair was prevented by backward masking after 20 ms, while the opposite expression remained normally visible. The results showed a bidirectional influence of non-conscious fear processing over conscious recognition of happy as well as fearful expressions. Consciously perceived fearful faces were more readily recognized when they were paired with invisible emotionally congruent fearful expressions in the opposite field, as compared to the single presentation of the same unmasked faces. On the other hand, recognition of unmasked happy faces was delayed by the simultaneous presence of a masked fearful face. No such effect was reported for masked happy expressions. These findings show that non-conscious processing of fear may modulate ongoing conscious evaluation of facial expressions via neural interhemispheric summation even in the intact brain.     

Recognition of Pain as Another Deficit in Young Males with High Callous-Unemotional Traits

Prior research on callous-unemotional (CU) traits supports a deficit in recognizing fear in faces and body postures. Difficulties recognising others’ emotions may impair the typical behavioural inhibition for violent behaviour. However, recent research has begun to examine other distress cues such as pain. The present study examined emotion recognition skills, including pain, of school-excluded boys aged 11–16 years (N = 50). Using dynamic faces and body poses, we examined the relation between emotion recognition and CU traits using the youth psychopathic traits inventory (YPI) and the inventory of CU traits. Violent delinquency was covaried in regression analyses. Although fearful facial and fearful bodily expressions were unrelated to CU traits, recognition of dynamic pain facial expressions was negatively related to CU traits using the YPI. The failure to replicate a fear and sad deficit are discussed in relation to previous research. Also, findings are discussed in support of a general empathy deficit for distress cues which may underlie the problem behaviour of young males with CU traits.     

Citalopram modulation of neuronal responses to aversive face emotions: a functional MRI study

This study investigated the serotonergic modulation of face emotion processing using blood oxygen level-dependent (BOLD) functional MRI. In a placebo-controlled, balanced order design, intravenous citalopram (7.5 mg) was given to 12 male volunteers 60 min before a covert face emotion recognition task. Angry, disgusted and fearful faces produced BOLD signal responses, which were broadly consistent with previous findings. Citalopram enhanced the BOLD signal response in the left posterior insula (together with nonprespecified pulvinar and visual cortex) but attenuated activation in the left amygdala to disgusted faces and right amygdala activation to fearful faces. No citalopram modulation of BOLD responses to angry faces were found. These results suggest that serotonin modulates low-level amygdala activation to aversive stimuli.     

Neural responses to dynamic expressions of fear in schizophrenia

Abnormalities in social functioning are a significant feature of schizophrenia. One critical aspect of these abnormalities is the difficulty these individuals have with the recognition of facial emotions, particularly negative expressions such as fear. The present work focuses on fear perception and its relationship to the paranoid symptoms of schizophrenia, specifically, how underlying limbic system structures (i.e. the amygdala) react when probed with dynamic fearful facial expressions. Seven paranoid and eight non-paranoid subjects (all males) with a diagnosis of schizophrenia took part in functional magnetic resonance imaging study (1.5T) examining neural responses to emerging fearful expressions contrasted with dissipating fearful expressions. Subjects viewed emerging and dissipating expressions while completing a gender discrimination task. Their brain activation was compared to that of 10 healthy male subjects. Increased hippocampal activation was seen in the non-paranoid group, while abnormalities in the bilateral amygdalae were observed only in the paranoid individuals. These patterns may represent trait-related hippocampal dysfunction, coupled with state (specifically paranoia) related amygdala abnormalities. The findings are discussed in light of models of paranoia in schizophrenia.     

Facial emotion perception differs in young persons at genetic and clinical high-risk for psychosis

A large body of literature has documented facial emotion perception impairments in schizophrenia. More recently, emotion perception has been investigated in persons at genetic and clinical high-risk for psychosis. This study compared emotion perception abilities in groups of young persons with schizophrenia, clinical high-risk, genetic risk and healthy controls. Groups, ages 13–25, included 24 persons at clinical high-risk, 52 first-degree relatives at genetic risk, 91 persons with schizophrenia and 90 low risk persons who completed computerized testing of emotion recognition and differentiation. Groups differed by overall emotion recognition abilities and recognition of happy, sad, anger and fear expressions. Pairwise comparisons revealed comparable impairments in recognition of happy, angry, and fearful expressions for persons at clinical high-risk and schizophrenia, while genetic risk participants were less impaired, showing reduced recognition of fearful expressions. Groups also differed for differentiation of happy and sad expressions, but differences were mainly between schizophrenia and control groups. Emotion perception impairments are observable in young persons at-risk for psychosis. Preliminary results with clinical high-risk participants, when considered along findings in genetic risk relatives, suggest social cognition abilities to reflect pathophysiological processes involved in risk of 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.     

Normal recognition of emotional similarity between facial expressions following bilateral amygdala damage.

Bilateral damage to the amygdala in humans has been previously linked to two deficits in recognizing emotion in facial expressions: recognition of individual basic emotions, especially fear, and recognition of similarity among emotional expressions. Although several studies have examined recognition of individual emotions following amygdala damage, only one subject has been examined on recognition of similarity. To assess the extent to which deficits in recognizing similarity among facial expressions might be a general consequence of amygdala damage, we examined this ability in two subjects with complete bilateral amygdala damage. Both subjects had previously demonstrated entirely normal recognition of individual facial emotions. Here we report that these two patients also are intact in their ability to recognize similarity between emotional expressions. These results indicate that, like the recognition of individual basic emotions in facial expressions, the recognition of similarity among emotional expressions does not have an absolute dependence on the amygdala.     

Rapid amygdala gamma oscillations in response to fearful facial expressions

Neuroimaging studies have reported greater activation of the human amygdala in response to emotional facial expressions, especially for fear. However, little is known about how fast this activation occurs. We investigated this issue by recording the intracranial field potentials of the amygdala in subjects undergoing pre-neurosurgical assessment (n = 6). The subjects observed fearful, happy, and neutral facial expressions. Time-frequency statistical parametric mapping analyses revealed that the amygdala showed greater gamma-band activity in response to fearful compared with neutral facial expressions at 50-150 ms, with a peak at 135 ms. These results indicate that the human amygdala is able to rapidly process fearful facial expressions.