A differential neural response in the human amygdala to fearful and happy facial expressions

The amygdala is thought to play a crucial role in emotional and social behaviour. Animal studies implicate the amygdala in both fear conditioning and face perception. In humans, lesions of the amygdala can lead to selective deficits in the recognition of fearful facial expressions and impaired fear conditioning, and direct electrical stimulation evokes fearful emotional responses. Here we report direct in vivo evidence of a differential neural response in the human amygdala to facial expressions of fear and happiness. Positron-emission tomography (PET) measures of neural activity were acquired while subjects viewed photographs of fearful or happy faces, varying systematically in emotional intensity. The neuronal response in the left amygdala was significantly greater to fearful as opposed to happy expressions. Furthermore, this response showed a significant interaction with the intensity of emotion (increasing with increasing fearfulness, decreasing with increasing happiness). The findings provide direct evidence that the human amygdala is engaged in processing the emotional salience of faces, with a specificity of response to fearful facial expressions.     

Hemispheric perception of emotional valence from facial expressions.

The authors previously reported that normal subjects are better at discriminating happy from neutral faces when the happy face is located to the viewer's right of the neutral face; conversely, discrimination of sad from neutral faces is better when the sad face is shown to the left, supporting a role for the left hemisphere in processing positive valence and for the right hemisphere in processing negative valence. Here, the authors extend this same task to subjects with unilateral cerebral damage (31 right, 28 left). Subjects with right damage performed worse when discriminating sad faces shown on the left, consistent with the prior findings. However, subjects with either left or right damage actually performed superior to normal controls when discriminating happy faces shown on the left. The authors suggest that perception of negative valence relies preferentially on the right hemisphere, whereas perception of positive valence relies on both left and right hemispheres. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The aftermath of 9/11: Effect of intensity and recency of trauma on outcome.

Does trauma exposure have a long-term impact on the brain and behavior of healthy individuals? The authors used functional magnetic resonance imaging to assess the impact of proximity to the disaster of September 11, 2001, on amygdala function in 22 healthy adults. More than three years after the terrorist attacks, bilateral amygdala activity in response to viewing fearful faces compared to calm ones was higher in people who were within 1.5 miles of the World Trade Center on 9/11, relative to those who were living more than 200 miles away (all were living in the New York metropolitan area at time of scan). This activity mediated the relationship between group status and current symptoms of posttraumatic stress disorder. In turn, the effect of group status on both amygdala activation (fearful vs. calm faces) and current symptoms was statistically explained by time since worst trauma in lifetime and intensity of worst trauma, as indicated by reported symptoms at time of the trauma. These data are consistent with a model of heightened amygdala reactivity following high-intensity trauma exposure, with relatively slow recovery. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Brain activation while forming memories of fearful and neutral faces in women and men.

Event-related functional MRI (fMRI) was used to assess brain activity during encoding of fearful and neutral faces in 12 women and 12 men. In a subsequent memory analysis, the authors separated successful from unsuccessful encoding of both types of faces, based on whether they were remembered or forgotten in a later recognition memory test. Overall, women and men recruited overlapping neural circuitries. Both sexes activated right-sided medial-temporal regions during successful encoding of fearful faces. Successful encoding of neutral faces was associated with left-sided lateral prefrontal and right-sided superior frontal activation in both sexes. In women, relatively greater encoding related activity for neutral faces was seen in the superior parietal and parahippocampal cortices. By contrast, men activated the left and right superior/middle frontal cortex more than women during successful encoding of the same neutral faces. These findings suggest that women and men use similar neural networks to encode facial information, with only subtle sex differences observed for neutral faces. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Attentional capture by irrelevant emotional distractor faces.

We establish attentional capture by emotional distractor faces presented as a “singleton” in a search task in which the emotion is entirely irrelevant. Participants searched for a male (or female) target face among female (or male) faces and indicated whether the target face was tilted to the left or right. The presence (vs. absence) of an irrelevant emotional singleton expression (fearful, angry, or happy) in one of the distractor faces slowed search reaction times compared to the singleton absent or singleton target conditions. Facilitation for emotional singleton targets was found for the happy expression but not for the fearful or angry expressions. These effects were found irrespective of face gender and the failure of a singleton neutral face to capture attention among emotional faces rules out a visual odd-one-out account for the emotional capture. The present study thus establishes irrelevant, emotional, attentional capture. (PsycINFO Database Record (c) 2011 APA, all rights reserved)     

Looking for Foes and Friends: Perceptual and Emotional Factors When Finding a Face in the Crowd.

In a face-in-the-crowd setting, the authors examined visual search for photographically reproduced happy, angry, and fearful target faces among neutral distractor faces in 3 separate experiments. Contrary to the hypothesis, happy targets were consistently detected more quickly and accurately than angry and fearful targets, as were directed compared with averted targets. There was no consistent effect of social anxiety. A facial emotion recognition experiment suggested that the happy search advantage could be due to the ease of processing happy faces. In the final experiment with perceptually controlled schematic faces, the authors reported more effective detection of angry than happy faces. This angry advantage was most obvious for highly socially anxious individuals when their social fear was experimentally enhanced. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The fearful-face advantage is modulated by task demands: Evidence from the attentional blink.

Fearful faces receive privileged access to awareness relative to happy and nonemotional faces. We investigated whether this advantage depends on currently available attentional resources. In an attentional blink paradigm, observers detected faces presented during the attentional blink period that could depict either a fearful or a happy expression. Perceptual load of the blink-inducing target was manipulated by increasing flanker interference. For the low-load condition, fearful faces were detected more often than happy faces, replicating previous reports. More important, this advantage for fearful faces disappeared for the high-load condition, during which fearful and happy faces were detected equally often. These results suggest that the privileged access of fearful faces to awareness does not occur mandatorily, but instead depends on attentional resources. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Anxiety and sensitivity to gaze direction in emotionally expressive faces.

This study investigated the role of neutral, happy, fearful, and angry facial expressions in enhancing orienting to the direction of eye gaze. Photographs of faces with either direct or averted gaze were presented. A target letter (T or L) appeared unpredictably to the left or the right of the face, either 300 ms or 700 ms after gaze direction changed. Response times were faster in congruent conditions (i.e., when the eyes gazed toward the target) relative to incongruent conditions (when the eyes gazed away from the target letter). Facial expression did influence reaction times, but these effects were qualified by individual differences in self-reported anxiety. High trait-anxious participants showed an enhanced orienting to the eye gaze of faces with fearful expressions relative to all other expressions. In contrast, when the eyes stared straight ahead, trait anxiety was associated with slower responding when the facial expressions depicted anger. Thus, in anxiety-prone people attention is more likely to be held by an expression of anger, whereas attention is guided more potently by fearful facial expressions. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Anteromedial Temporal Lobe Damage Blocks Startle Modulation by Fear and Disgust.

The acoustic startle reflex (ASR) is potentiated during negative emotion, but attenuated during positive emotional experience. The modulation of the ASR by fear depends critically on the amygdala. The authors investigated ASR modulation to fearful, disgusting, pleasant, and neutral stimuli in 12 patients with unilateral damage to the anteromedial temporal lobe including the amygdala (6 left, 6 right), 1 patient with bilateral temporal lobe damage including the amygdala, and 12 comparison participants. Both groups with unilateral damage, as well as the subject with bilateral damage, showed a complete lack of ASR potentiation to both fear and disgust stimuli. The findings suggest that potentiation of the ASR by disgust and fear depends on the integrity of the anteromedial temporal lobe. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

A functional MRI study of human amygdala responses to facial expressions of fear versus anger.

Functional magnetic resonance imaging (fMRI) of the human brain was used to compare changes in amygdala activity associated with viewing facial expressions of fear and anger. Pictures of human faces bearing expressions of fear or anger, as well as faces with neutral expressions, were presented to 8 healthy participants. The blood oxygen-level dependent (BOLD) fMRI signal within the dorsal amygdala was significantly greater to Fear versus Anger, in a direct contrast. Significant BOLD signal changes in the ventral amygdala were observed in contrasts of Fear versus Neutral expressions and, in a more spatially circumscribed region, to Anger versus Neutral expressions. Thus, activity in the amygdala is greater to fearful facial expressions when contrasted with either neutral or angry faces. Furthermore, directly contrasting fear with angry faces highlighted involvement of the dorsal amygdaloid region. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Dispositional mindfulness and depressive symptomatology: Correlations with limbic and self-referential neural activity during rest.

To better understand the relationship between mindfulness and depression, we studied normal young adults (n = 27) who completed measures of dispositional mindfulness and depressive symptomatology, which were then correlated with (a) rest: resting neural activity during passive viewing of a fixation cross, relative to a simple goal-directed task (shape-matching); and (b) reactivity: neural reactivity during viewing of negative emotional faces, relative to the same shape-matching task. Dispositional mindfulness was negatively correlated with resting activity in self-referential processing areas, whereas depressive symptomatology was positively correlated with resting activity in similar areas. In addition, dispositional mindfulness was negatively correlated with resting activity in the amygdala, bilaterally, whereas depressive symptomatology was positively correlated with activity in the right amygdala. Similarly, when viewing emotional faces, amygdala reactivity was positively correlated with depressive symptomatology and negatively correlated with dispositional mindfulness, an effect that was largely attributable to differences in resting activity. These findings indicate that mindfulness is associated with intrinsic neural activity and that changes in resting amygdala activity could be a potential mechanism by which mindfulness-based depression treatments elicit therapeutic improvement. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Emotion recognition from faces and prosody following temporal lobectomy.

The anteromedial temporal lobe has been found to participate in processing emotion, but there are unresolved discrepancies in the literature. To address this issue, the authors investigated recognition of emotion from faces and from prosody in 26 participants with unilateral temporal lobectomy (15 left, 11 right) and in 50 brain-damaged controls. Participants with right, but not left, temporal lobectomy did significantly worse in recognizing fear from facial expressions. There were no group differences in recognizing emotional prosody. Neither IQ nor basic perceptual function accounted for task performance; however, there was a moderate negative correlation between extent of amygdala damage and overall performance. Consistent with some prior studies, these findings support a role for the right anteromedial temporal lobe (including amygdala) in recognizing emotion from faces but caution in drawing conclusions from small group samples. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Neural structures associated with recognition of facial expressions of basic emotions

People with Huntington's disease and people suffering from obsessive compulsive disorder show severe deficits in recognizing facial expressions of disgust, whereas people with lesions restricted to the amygdala are especially impaired in recognizing facial expressions of fear. This double dissociation implies that recognition of certain basic emotions may be associated with distinct and non-overlapping neural substrates. Some authors, however, emphasize the general importance of the ventral parts of the frontal cortex in emotion recognition, regardless of the emotion being recognized. In this study, we used functional magnetic resonance imaging to locate neural structures that are critical for recognition of facial expressions of basic emotions by investigating cerebral activation of six healthy adults performing a gender discrimination task on images of faces expressing disgust, fear and anger. Activation in response to these faces was compared with that for faces showing neutral expressions. Disgusted facial expressions activated the right putamen and the left insula cortex, whereas enhanced activity in the posterior part of the right gyrus cinguli and the medial temporal gyrus of the left hemisphere was observed during processing of angry faces. Fearful expressions activated the right fusiform gyrus and the left dorsolateral frontal cortex. For all three emotions investigated, we also found activation of the inferior part of the left frontal cortex (Brodmann area 47). These results support the hypotheses derived from neuropsychological findings, that (i) recognition of disgust, fear and anger is based on separate neural systems, and that (ii) the output of these systems converges on frontal regions for further information processing.     

Emotional expression modulates perceived gaze direction.

Gaze perception is an important social skill, as it portrays information about what another person is attending to. Gaze direction has been shown to affect interpretation of emotional expression. Here the authors investigate whether the emotional facial expression has a reciprocal influence on interpretation of gaze direction. In a forced-choice yes-no task, participants were asked to judge whether three faces expressing different emotions (anger, fear, happiness, and neutral) in different viewing angles were looking at them or not. Happy faces were more likely to be judged as looking at the observer than were angry, fearful, or neutral faces. Angry faces were more often judged as looking at the observer than were fearful and neutral expressions. These findings are discussed on the background of approach and avoidance orientation of emotions and of the self-referential positivity bias. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

A subcortical pathway to the right amygdala mediating "unseen" fear

Neuroimaging studies have shown differential amygdala responses to masked ("unseen") emotional stimuli. How visual signals related to such unseen stimuli access the amygdala is unknown. A possible pathway, involving the superior colliculus and pulvinar, is suggested by observations of patients with striate cortex lesions who show preserved abilities to localize and discriminate visual stimuli that are not consciously perceived ("blindsight"). We used measures of right amygdala neural activity acquired from volunteer subjects viewing masked fear-conditioned faces to determine whether a colliculo-pulvinar pathway was engaged during processing of these unseen target stimuli. Increased connectivity between right amygdala, pulvinar, and superior colliculus was evident when fear-conditioned faces were unseen rather than seen. Right amygdala connectivity with fusiform and orbitofrontal cortices decreased in the same condition. By contrast, the left amygdala, whose activity did not discriminate seen and unseen fear-conditioned targets, showed no masking-dependent changes in connectivity with superior colliculus or pulvinar. These results suggest that a subcortical pathway to the right amygdala, via midbrain and thalamus, provides a route for processing behaviorally relevant unseen visual events in parallel to a cortical route necessary for conscious identification.     

Fearful expressions gain preferential access to awareness during continuous flash suppression.

Rapid evaluation of ecologically relevant stimuli may lead to their preferential access to awareness. Continuous flash suppression allows assessment of affective processing under conditions in which stimuli have been rendered invisible due to the strongly suppressive nature of dynamic noise relative to static images. The authors investigated whether fearful expressions emerge from suppression into awareness more quickly than images of neutral or happy expressions. Fearful faces were consistently detected faster than neutral or happy faces. Responses to inverted faces were slower than those to upright faces but showed the same effect of emotional expression, suggesting that some key feature or features in the inverted faces remained salient. When using stimuli solely representing the eyes, a similar bias for detecting fear emerged, implicating the importance of information from the eyes in the preconscious processing of fear expressions. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Cortical brain regions engaged by masked emotional faces in adolescents and adults: An fMRI study.

Face-emotion processing has shown signs of developmental change during adolescence. Functional magnetic resonance imaging (fMRI) was used on 10 adolescents and 10 adults to contrast brain regions engaged by a masked emotional-face task (viewing a fixation cross and a series of masked happy and masked fearful faces), while blood oxygen level dependent signal was monitored by a 1.5-T MRI scanner. Brain regions differentially engaged in the 2 age groups were mapped by using statistical parametric mapping. Summed across groups, the contrast of masked face versus fixation-cross viewing generated activations in occipital-temporal regions previously activated in passive face-viewing tasks. Adolescents showed higher maxima for activations in posterior association cortex for 3 of the 4 statistical contrasts. Adolescents and adults differed in the degree to which posterior hemisphere brain areas were engaged by viewing masked facial displays of emotion. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Detection of emotional faces: Salient physical features guide effective visual search.

In this study, the authors investigated how salient visual features capture attention and facilitate detection of emotional facial expressions. In a visual search task, a target emotional face (happy, disgusted, fearful, angry, sad, or surprised) was presented in an array of neutral faces. Faster detection of happy and, to a lesser extent, surprised and disgusted faces was found both under upright and inverted display conditions. Inversion slowed down the detection of these faces less than that of others (fearful, angry, and sad). Accordingly, the detection advantage involves processing of featural rather than configural information. The facial features responsible for the detection advantage are located in the mouth rather than the eye region. Computationally modeled visual saliency predicted both attentional orienting and detection. Saliency was greatest for the faces (happy) and regions (mouth) that were fixated earlier and detected faster, and there was close correspondence between the onset of the modeled saliency peak and the time at which observers initially fixated the faces. The authors conclude that visual saliency of specific facial features--especially the smiling mouth--is responsible for facilitated initial orienting, which thus shortens detection. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The combined effect of gaze direction and facial expression on cueing spatial attention.

Empirical evidence shows an effect of gaze direction on cueing spatial attention, regardless of the emotional expression shown by a face, whereas a combined effect of gaze direction and facial expression has been observed on individuals' evaluative judgments. In 2 experiments, the authors investigated whether gaze direction and facial expression affect spatial attention depending upon the presence of an evaluative goal. Disgusted, fearful, happy, or neutral faces gazing left or right were followed by positive or negative target words presented either at the spatial location looked at by the face or at the opposite spatial location. Participants responded to target words based on affective valence (i.e., positive/negative) in Experiment 1 and on letter case (lowercase/uppercase) in Experiment 2. Results showed that participants responded much faster to targets presented at the spatial location looked at by disgusted or fearful faces but only in Experiment 1, when an evaluative task was used. The present findings clearly show that negative facial expressions enhance the attentional shifts due to eye-gaze direction, provided that there was an explicit evaluative goal present. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Different neural responses to stranger and personally familiar faces in shy and bold adults.

The shy-bold continuum is a fundamental behavioral trait conserved across human and nonhuman animals. Individual differences along the shy-bold continuum are presumed to arise from, and are maintained by, differences in the excitability of forebrain limbic areas involved in the evaluation of stimulus saliency. To test this hypothesis, the authors conducted an event-related functional MRI (fMRI) study in which brain scans were acquired on shy and bold adults during the presentation of neutral stranger and personally familiar faces. Shy adults exhibited greater bilateral amygdala activation during the presentation of stranger faces and greater left amygdala activation during personally familiar faces than their bold counterparts. Bold adults exhibited greater bilateral nucleus accumbens activation in response to stranger and personally familiar faces than shy adults. Findings suggest that there are distinct neural substrates underlying and maintaining individual differences along a shy-bold continuum in humans. (PsycINFO Database Record (c) 2010 APA, all rights reserved)