Task instructions modulate neural responses to fearful facial expressions.

BACKGROUND: The amygdala, hippocampus, ventral, and dorsal prefrontal cortices have been demonstrated to be involved in the response to fearful facial expressions. Little is known, however, about the effect of task instructions upon the intensity of responses within these regions to fear-inducing stimuli. METHODS: Using functional magnetic resonance imaging, we examined neural responses to alternating, 30-sec blocks of fearful and neutral expressions in nine right-handed male volunteers during three different 5-min conditions: 1) passive viewing; 2) performance of a gender-decision task, with no explicit judgment of facial emotion; 3) performance of an emotionality judgment task - an explicitly emotional task. RESULTS: There was a significant effect of task upon activation within the left hippocampus and the left inferior occipital gyrus, and upon the magnitude of response within the left hippocampus, with maximal activation in these regions occurring during passive viewing, and minimal during performance of the explicit task. Performance of the gender-decision and explicit tasks, but not passive viewing, was also associated with activation within ventral frontal cortex. CONCLUSIONS: Neural responses to fearful facial expressions are modulated by task instructions.     

Seeing happy emotion in fearful and angry faces: qualitative analysis of facial expression recognition in a bilateral amygdala-damaged patient

Neuropsychological studies reported that bilateral amygdala-damaged patients had impaired recognition of facial expressions of fear. However, the specificity of this impairment remains unclear. To address this issue, we carried out two experiments concerning the recognition of facial expression in a patient with bilateral amygdala damage (HY). In Experiment 1, subjects matched the emotion of facial expressions with appropriate verbal labels, using standardized photographs of facial expressions illustrating six basic emotions. The performance of HY was compared with age-matched normal controls (n = 13) and brain-damaged controls (n = 9). HY was less able to recognize facial expressions showing fear than normal controls. In addition, the error pattern exhibited by HY for facial expressions of fear and anger were distinct from those exhibited by both control groups, and suggested that HY confused these emotions with happiness. In Experiment 2, subjects were presented with morphed facial expressions that blended happiness and fear, happiness and anger, or happiness and sadness. Subjects were requested to categorize these expressions by two-way forced-choice selection. The performance of HY was compared with age-matched normal controls (n = 8). HY categorized the morphed fearful and angry expressions blended with some happy content as happy facial expressions more frequently than normal controls. These findings support the idea that amygdala-damaged patients have impaired processing of facial expressions relating to certain negative emotions, particularly fear and anger. More specifically, amygdala-damaged patients seem to give positively biased evaluations for these negative facial expressions.     

Imitating expressions: emotion-specific neural substrates in facial mimicry

Intentionally adopting a discrete emotional facial expressioncan modulate the subjective feelings corresponding to that emotion;however, the underlying neural mechanism is poorly understood.We therefore used functional brain imaging (functional magneticresonance imaging) to examine brain activity during intentionalmimicry of emotional and non-emotional facial expressions andrelate regional responses to the magnitude of expression-inducedfacial movement. Eighteen healthy subjects were scanned whileimitating video clips depicting three emotional (sad, angry,happy), and two ‘ingestive’ (chewing and licking)facial expressions. Simultaneously, facial movement was monitoredfrom displacement of fiducial markers (highly reflective dots)on each subject's face. Imitating emotional expressions enhancedactivity within right inferior prefrontal cortex. This patternwas absent during passive viewing conditions. Moreover, themagnitude of facial movement during emotion-imitation predictedresponses within right insula and motor/premotor cortices. Enhancedactivity in ventromedial prefrontal cortex and frontal polewas observed during imitation of anger, in ventromedial prefrontaland rostral anterior cingulate during imitation of sadness andin striatal, amygdala and occipitotemporal during imitationof happiness. Our findings suggest a central role for rightinferior frontal gyrus in the intentional imitation of emotionalexpressions. Further, by entering metrics for facial muscularchange into analysis of brain imaging data, we highlight sharedand discrete neural substrates supporting affective, actionand social consequences of somatomotor emotional expression.     

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.     

A differential pattern of neural response toward sad versus happy facial expressions in major depressive disorder.

BACKGROUND: Accurate recognition of facial expressions is crucial for social functioning. In depressed individuals, implicit and explicit attentional biases away from happy and toward sad stimuli have been demonstrated. These may be associated with the negative cognitions in these individuals. METHODS: Using event-related functional magnetic resonance imaging (fMRI), neural responses to happy and sad facial expressions were measured in 14 healthy individuals and 16 individuals with major depressive disorder. RESULTS: Healthy but not depressed individuals demonstrated linear increases in response in bilateral fusiform gyri and right putamen to expressions of increasing happiness, while depressed individuals demonstrated linear increases in response in left putamen, left parahippocampal gyrus/amygdala, and right fusiform gyrus to expressions of increasing sadness. There was a negative correlation in depressed individuals between depression severity and magnitude of neural response within right fusiform gyrus to happy expressions. CONCLUSIONS: Our findings indicate preferential increases in neural response to sad but not happy facial expressions in neural regions involved in the processing of emotional stimuli in depressed individuals. These findings may be associated with the above pattern of implicit and explicit attentional biases in these individuals and suggest a potential neural basis for the negative cognitions and social dysfunction in major depression.     

Neural responses to facial expressions support the role of the amygdala in processing threat

The amygdala is known to play an important role in the response to facial expressions that convey fear. However, it remains unclear whether the amygdala’s response to fear reflects its role in the interpretation of danger and threat, or whether it is to some extent activated by all facial expressions of emotion. Previous attempts to address this issue using neuroimaging have been confounded by differences in the use of control stimuli across studies. Here, we address this issue using a block design functional magnetic resonance imaging paradigm, in which we compared the response to face images posing expressions of fear, anger, happiness, disgust and sadness with a range of control conditions. The responses in the amygdala to different facial expressions were compared with the responses to a non-face condition (buildings), to mildly happy faces and to neutral faces. Results showed that only fear and anger elicited significantly greater responses compared with the control conditions involving faces. Overall, these findings are consistent with the role of the amygdala in processing threat, rather than in the processing of all facial expressions of emotion, and demonstrate the critical importance of the choice of comparison condition to the pattern of results.     

Subcortical and ventral prefrontal cortical neural responses to facial expressions distinguish patients with bipolar disorder and major depression.

BACKGROUND: Bipolar disorder (BD) is characterised by abnormalities in mood and emotional processing, but the neural correlates of these, their relationship to depressive symptoms, and the similarities with deficits in major depressive disorder (MDD) remain unclear. We compared responses within subcortical and prefrontal cortical regions to emotionally salient material in patients with BP and MDD using functional magnetic resonance imaging. METHODS: We measured neural responses to mild and intense expressions of fear, happiness, and sadness in euthymic and depressed BD patients, healthy control subjects, and depressed MDD patients. RESULTS: Bipolar disorder patients demonstrated increased subcortical (ventral striatal, thalamic, hippocampal) and ventral prefrontal cortical responses particularly to mild and intense fear, mild happy, and mild sad expressions. Healthy control subjects demonstrated increased subcortical responses to intense happy and mild fear, and increased dorsal prefrontal cortical responses to intense sad expressions. Overall, MDD patients showed diminished neural responses to all emotional expressions except mild sadness. Depression severity correlated positively with hippocampal response to mild sadness in both patient groups. CONCLUSIONS: Compared with healthy controls and MDD patients, BD patients demonstrated increased subcortical and ventral prefrontal cortical responses to both positive and negative emotional expressions.     

The BOLD signal in the amygdala does not differentiate between dynamic facial expressions

The amygdala has been considered to be essential for recognizingfear in other people's facial expressions. Recent studies sheddoubt on this interpretation. Here we used movies of facialexpressions instead of static photographs to investigate theputative fear selectivity of the amygdala using fMRI under moreecological conditions. The amygdala was found to respond moreto movies of facial expressions than to pattern motion, butno differences were found between the responses to neutral,happy, disgusted and fearful facial expressions. This lack ofemotional selectivity was replicated in three experiments usingthree different tasks (passive observation, delayed match tosample and viewing for imitation) and two different analysismethods (voxel-by-voxel and anatomical region of interest).Our data therefore provide strong support for the idea thatunder more ecologically valid conditions, the contribution ofthe amygdala towards the detection of fearful facial expressionsmust be more indirect than previously assumed.     

Widespread and lateralized social brain activity for processing dynamic facial expressions

Dynamic facial expressions of emotions constitute natural and powerful means of social communication in daily life. A number of previous neuroimaging studies have explored the neural mechanisms underlying the processing of dynamic facial expressions, and indicated the activation of certain social brain regions (e.g., the amygdala) during such tasks. However, the activated brain regions were inconsistent across studies, and their laterality was rarely evaluated. To investigate these issues, we measured brain activity using functional magnetic resonance imaging in a relatively large sample (n = 51) during the observation of dynamic facial expressions of anger and happiness and their corresponding dynamic mosaic images. The observation of dynamic facial expressions, compared with dynamic mosaics, elicited stronger activity in the bilateral posterior cortices, including the inferior occipital gyri, fusiform gyri, and superior temporal sulci. The dynamic facial expressions also activated bilateral limbic regions, including the amygdalae and ventromedial prefrontal cortices, more strongly versus mosaics. In the same manner, activation was found in the right inferior frontal gyrus (IFG) and left cerebellum. Laterality analyses comparing original and flipped images revealed right hemispheric dominance in the superior temporal sulcus and IFG and left hemispheric dominance in the cerebellum. These results indicated that the neural mechanisms underlying processing of dynamic facial expressions include widespread social brain regions associated with perceptual, emotional, and motor functions, and include a clearly lateralized (right cortical and left cerebellar) network like that involved in language processing.     

Facing puberty: associations between pubertal development and neural responses to affective facial displays

Adolescence is marked by profound psychosocial and physiological changes. Although investigations into the interactions between these forces have begun to shed light on the neural correlates of affective processing during the transition to adolescence, relatively little is known about the relationship between pubertal development and emotion perception at the neural level. In the current longitudinal study, 45 neurotypical participants were shown affective facial displays while undergoing fMRI, at ages 10 and 13. Neural responses to emotional expressions at both time points were then correlated with a self-report measure of pubertal development, revealing positive associations with activity in amygdala, thalamus and visual cortical areas at age 10 that increased in magnitude and extent by age 13. At the latter time point, pubertal development was additionally correlated with enhanced responses to faces in temporal pole, ventrolateral prefrontal cortex (PFC) and dorsomedial PFC. Longitudinal comparisons revealed that the relationships between pubertal development and activity in the amygdala, hippocampus and temporal pole were significantly stronger during early adolescence than late childhood. These results suggest that pubertal development per se is linked to neural processing of socioemotional stimuli, particularly with respect to the integration of complex perceptual input and higher order cortical processing of affective content.     

Hypersensitivity to low intensity fearful faces in autism when fixation is constrained to the eyes

Previous studies that showed decreased brain activation in people with autism spectrum disorder (ASD) viewing expressive faces did not control that participants looked in the eyes. This is problematic because ASD is characterized by abnormal attention to the eyes. Here, we collected fMRI data from 48 participants (27 ASD) viewing pictures of neutral faces and faces expressing anger, happiness, and fear at low and high intensity, with a fixation cross between the eyes. Group differences in whole brain activity were examined for expressive faces at high and low intensity versus neutral faces. Group differences in neural activity were also investigated in regions of interest within the social brain, including the amygdala and the ventromedial prefrontal cortex (vmPFC). In response to low intensity fearful faces, ASD participants showed increased activation in the social brain regions, and decreased functional coupling between the amygdala and the vmPFC. This oversensitivity to low intensity fear coupled with a lack of emotional regulation capacity could indicate an excitatory/inhibitory imbalance in their socio‐affective processing system. This may result in social disengagement and avoidance of eye‐contact to handle feelings of strong emotional reaction. Our results also demonstrate the importance of careful control of gaze when investigating emotional processing in ASD. Hum Brain Mapp 38:5943–5957, 2017. © 2017 Wiley Periodicals, Inc.     

Judgment of facial expressions and depression persistence

In research it has been demonstrated that cognitive and interpersonal processes play significant roles in depression development and persistence. The judgment of emotions displayed in facial expressions by depressed patients allows for a better understanding of these processes. In this study, 48 major depression outpatients and healthy control subjects, matched on the gender of the patients, judged facial expressions as to the emotions the expressions displayed. These judgments were conducted at the patients' outpatient admission (T1). The depression severity of the patients was measured at T1, 13 weeks later (T2) and at a 6-month follow-up (T3). It was found that the judgment of negative emotions in the facial expressions was related to both the depression severity at T1 and depression persistence (T2 and T3), whereas the judgment of positive emotions was not related to the patients' depression. The judgment of the emotion of sadness was the best predictor of the patients' depression persistence. Additionally, it was found that the patients judged significantly more sadness in the facial expressions than the control subjects. These findings are related to previous data of facial expression judgments of depressed patients and future research directions are discussed.     

Time courses of left and right amygdalar responses to fearful facial expressions

Despite the many studies highlighting the role of the amygdala in fear perception, few have examined differences between right and left amygdalar responses. Using functional magnetic resonance imaging (fMRI), we examined neural responses in three groups of healthy volunteers (n = 18) to alternating blocks of fearful and neutral faces. Initial observation of extracted time series of both amygdalae to these stimuli indicated more rapid decreases of right than left amygdalar responses to fearful faces, and increasing magnitudes of right amygdalar responses to neutral faces with time. We compared right and left responses statistically by modeling each time series with (1) a stationary fit model (assuming a constant magnitude of amygdalar response to consecutive blocks of fearful faces) and (2) an adaptive model (no assumptions). Areas of significant sustained nonstationarity (time series points with significantly greater adaptive than stationary model fits) were demonstrated for both amygdalae. There was more significant nonstationarity of right than left amygdalar responses to neutral, and left than right amygdalar responses to fearful faces. These findings indicate significant variability over time of both right and left amygdalar responses to fearful and neutral facial expressions and are the first demonstration of specific differences in time courses of right and left amygdalar responses to these stimuli.     

Neural responses to happy facial expressions in major depression following antidepressant treatment

OBJECTIVE: Processing affective facial expressions is an important component of interpersonal relationships. However, depressed patients show impairments in this system. The present study investigated the neural correlates of implicit processing of happy facial expressions in depression and identified regions affected by antidepressant therapy. METHOD: Two groups of subjects participated in a prospective study with functional magnetic resonance imaging (fMRI). The patients were 19 medication-free subjects (mean age, 43.2 years) with major depression, acute depressive episode, unipolar subtype. The comparison group contained 19 matched healthy volunteers (mean age, 42.8 years). Both groups underwent fMRI scans at baseline (week 0) and at 8 weeks. Following the baseline scan, the patients received treatment with fluoxetine, 20 mg daily. The fMRI task was implicit affect recognition with standard facial stimuli morphed to display varying intensities of happiness. The fMRI data were analyzed to estimate the average activation (overall capacity) and differential response to variable intensity (dynamic range) in brain systems involved in processing facial affect. RESULTS: An attenuated dynamic range of response in limbic-subcortical and extrastriate visual regions was evident in the depressed patients, relative to the comparison subjects. The attenuated extrastriate cortical activation at baseline was increased following antidepressant treatment, and symptomatic improvement was associated with greater overall capacity in the hippocampal and extrastriate regions. CONCLUSIONS: Impairments in the neural processing of happy facial expressions in depression were evident in the core regions of affective facial processing, which were reversed following treatment. These data complement the neural effects observed with negative affective stimuli.     

Neural responses to facial expressions of disgust but not fear are modulated by washing symptoms in OCD.

BACKGROUND: Washing symptoms in Obsessive-Compulsive Disorder (OCD) are associated with increased trait sensitivity to disgust. This study explored neural systems underlying sensitivity to symptom-unrelated disgust and fear in OCD using functional neuroimaging. METHODS: Seventeen OCD subjects and 19 controls viewed facial expressions of disgust and fear (versus neutral) presented just above the level of conscious awareness in a backward masking paradigm. RESULTS: The OCD group showed greater activation than controls in the left ventrolateral prefrontal cortex, but reduced activation in the thalamus, to facial expressions of disgust. There were no between-group differences in response to fear. Further analysis using a median-split to divide OCD subjects into high and low washers suggested that the enhanced ventrolateral prefrontal cortex response was being driven by predominantly female OCD subjects with high washing symptoms. These subjects also reported higher levels of trait sensitivity to disgust. CONCLUSIONS: These findings are consistent with previous reports of increased response to symptom-relevant and generally disgusting stimuli in neural regions associated with disgust and autonomic response processing in OCD patients with prominent washing symptoms. Together, these findings point to increased sensitivity to disgust stimuli as a component of the pathophysiology of the washing/contamination symptom dimension of OCD.     

Emergence of enhanced attention to fearful faces between 5 and 7 months of age

The adult brain is endowed with mechanisms subserving enhanced processing of salient emotional and social cues. Stimuli associated with threat represent one such class of cues. Previous research suggests that preferential allocation of attention to social signals of threat (i.e. a preference for fearful over happy facial expressions) emerges during the second half of the first year. The present study was designed to determine the age of onset for infants’ attentional bias for fearful faces. Allocation of attention was studied by measuring event-related potentials (ERPs) and looking times (in a visual paired comparison task) to fearful and happy faces in 5- and 7-month-old infants. In 7-month-olds, the preferential allocation of attention to fearful faces was evident in both ERPs and looking times, i.e. the negative central mid-latency ERP amplitudes were more negative, and the looking times were longer for fearful than happy faces. No such differences were observed in the 5-month-olds. It is suggested that an enhanced sensitivity to facial signals of threat emerges between 5 and 7 months of age, and it may reflect functional development of the neural mechanisms involved in processing of emotionally significant stimuli.     

Perception of facial expressions of emotion in bipolar disorder

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