Functional brain activation to emotional and nonemotional faces in healthy children: Evidence for developmentally undifferentiated amygdala function during the school-age period

The amygdala is a key region in emotion processing. In particular, fMRI studies have demonstrated that the amygdala is active during the viewing of emotional faces. Previous research has consistently found greater amygdala responses to fearful than to neutral faces in adults, convergent with a focus in the animal literature on the amygdala’s role in fear processing. Studies have shown that the amygdala also responds differentially to other facial emotion types in adults. Yet the literature regarding when this differential amygdala responsivity develops is limited and mixed. Thus, the goal of the present study was to examine amygdala responses to emotional and neutral faces in a relatively large sample of healthy school-age children (N?=?52). Although the amygdala was active in response to emotional and neutral faces, the results did not support the hypothesis that the amygdala responds differentially to emotional faces in 7- to 12-year-old children. Nonetheless, amygdala activity was correlated with the severity of subclinical depression symptoms and with emotional regulation skills. Additionally, sex differences were observed in frontal, temporal, and visual regions, as well as effects of pubertal development in visual regions. These findings suggest important differences in amygdala reactivity in childhood.     

Temporal precedence of emotion over attention modulations in the lateral amygdala: Intracranial ERP evidence from a patient with temporal lobe epilepsy

Previous fMRI studies have reported mixed evidence for the influence of selective attention on amygdala responses to emotional stimuli, with some studies showing “automatic” emotional effects to threat-related stimuli without attention (or even without awareness), but other studies showing a gating of amygdala activity by selective attention with no response to unattended stimuli. We recorded intracranial local field potentials from the intact left lateral amygdala in a human patient prior to surgery for epilepsy and tested, with a millisecond time resolution, for neural responses to fearful faces appearing at either task-relevant or task-irrelevant locations. Our results revealed an early emotional effect in the amygdala arising prior to, and independently of, attentional modulation. However, at a later latency, we found a significant modulation of the differential emotional response when attention was directed toward or away from fearful faces. These results suggest separate influences of emotion and attention on amygdala activation and may help reconcile previous discrepancies concerning the relative responsiveness of the human amygdala to emotional and attentional factors.     

The involvement of distinct visual channels in rapid attention towards fearful facial expressions

This paper reports five experiments demonstrating that the low spatial frequency components of faces are critical to the production of rapid attentional responses towards fearful facial expressions. In our main experiments, low spatial frequency (LSF) or high spatial frequency (HSF) face pairs, consisting of one fearful and one neutral expression, were presented on a computer screen for a brief period. Participants were required to identify as quickly as possible the orientation of a bar target that immediately replaced one of the faces. Responses were faster when targets replaced the location of LSF fearful faces, compared with LSF neutral faces. By contrast, there were no differences between responses to targets replacing HSF fearful versus HSF neutral faces. This facilitation in spatial orienting occurred specifically with short time intervals between faces and target, and is consistent with a rapid processing of fear cues from LSF inputs that can serve to guide attention towards threat events.     

A tale of two negatives: differential memory modulation by threat-related facial expressions

Facial expressions serve as cues that encourage viewers to learn about their immediate environment. In studies assessing the influence of emotional cues on behavior, fearful and angry faces are often combined into one category, such as "threat-related," because they share similar emotional valence and arousal properties. However, these expressions convey different information to the viewer. Fearful faces indicate the increased probability of a threat, whereas angry expressions embody a certain and direct threat. This conceptualization predicts that a fearful face should facilitate processing of the environment to gather information to disambiguate the threat. Here, we tested whether fearful faces facilitated processing of neutral information presented in close temporal proximity to the faces. In Experiment 1, we demonstrated that, compared with neutral faces, fearful faces enhanced memory for neutral words presented in the experimental context, whereas angry faces did not. In Experiment 2, we directly compared the effects of fearful and angry faces on subsequent memory for emotional faces versus neutral words. We replicated the findings of Experiment 1 and extended them by showing that participants remembered more faces from the angry face condition relative to the fear condition, consistent with the notion that anger differs from fear in that it directs attention toward the angry individual. Because these effects cannot be attributed to differences in arousal or valence processing, we suggest they are best understood in terms of differences in the predictive information conveyed by fearful and angry facial expressions.     

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.     

Neural correlates of emotional intelligence in adolescent children

The somatic marker hypothesis posits a key role for the ventromedial prefrontal cortex, amygdala, and insula in the ability to utilize emotions to guide decision making and behavior. However, the relationship between activity in these brain regions and emotional intelligence (EQ) during adolescence, a time of particular importance for emotional and social development, has not been studied. Using functional magnetic resonance imaging (fMRI), we correlated scores from the Bar-On Emotional Quotient Inventory, Youth Version (EQ-i:YV) with brain activity during perception of fearful faces in 16 healthy children and adolescents. Consistent with the neural efficiency hypothesis, higher EQ correlated negatively with activity in the somatic marker circuitry and other paralimbic regions. Positive correlations were observed between EQ and activity in the cerebellum and visual association cortex. The findings suggest that the construct of self-reported EQ in adolescents is inversely related to the efficiency of neural processing within the somatic marker circuitry during emotional provocation.     

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.     

Attending to the fear in your eyes: Facilitated orienting and delayed disengagement

Fearful facial expressions convey threat-related information and automatically elicit modulations in spatial attention. The eye-region appears to be a particularly important feature for recognising and responding to fearful faces. However, it is unknown as to whether or not fearful eyes initiate modulations in spatial attention. In the current study, three dot-probe experiments with fearful and neutral eye stimuli were performed. The results of Experiment 1 demonstrate that fearful eyes capture spatial attention through facilitated attentional orienting to threat and delayed attentional disengagement from threat. In Experiments 2 and 3, these attentional effects were replicated, while ruling out the influence of overall size/shape and brightness differences between fearful and neutral eyes, respectively. Thus, fearful eye-whites appear to be a salient feature of fearful facial expressions that elicit modulations in spatial attention.     

The amygdala is involved in affective priming effect for fearful faces

The object of this study was to investigate whether the amygdala is involved in affective priming effect after stimuli are encoded unconsciously and consciously. During the encoding phase, each masked face (fearful or neutral) was presented to participants six times for 17ms each, using a backward masking paradigm. During the retrieval phase, participants made a fearful/neutral judgment for each face. Half of the faces had the same valence as that seen during encoding (congruent condition) and the other half did not (incongruent condition). Participants were divided into unaware and aware groups based on their subjective and objective awareness assessments. The fMRI results showed that during encoding, the amygdala elicited stronger activation for fearful faces than neutral faces but differed in the hemisphere according to the awareness level. During retrieval, the amygdala showed a significant repetition priming effect, with the congruent faces producing less activation than the incongruent faces, especially for fearful faces. These data suggest that the amygdala is important in unconscious retrieving of memories for emotional faces whether they are encoded consciously or unconsciously.     

Through the eyes of anxiety: Dissecting threat bias via emotional-binocular rivalry

An extensive body of research has demonstrated that anxious individuals abnormally process threat-related content. Yet, the manner in which clinical anxiety affects the selection of threatening signals and their maintenance within consciousness is yet to be explored. The present study used an emotional binocular rivalry (e-BR) procedure, in which pictures of faces depicting either fearful or neutral expressions competed with pictures of a house for conscious perception. We assumed that first- or cumulative-preferred perception of faces with fearful over neutral expression (i.e., initial or sustained threat bias, respectively) stand for preferential selection or maintenance of fear content in awareness, correspondingly. Unmedicated patients with social anxiety disorder (SAD) and panic disorder (PAD) were compared to healthy controls for threat-related perceptual biases in the e-BR. At first perception of face, both SAD and PAD patients showed a greater initial threat bias than healthy controls. In contrast, at cumulative dwell-time of face, patient groups demonstrated a diminished sustained threat bias relative to healthy controls, yet in a different manner. SAD patients showed a sustained threat bias, though it was smaller than in healthy controls. Furthermore, increased levels of reported anxiety among SAD patients were associated with enhanced sustained perception of neutral faces. PAD patients, on the other hand, showed no sustained threat bias and a diminished cumulative perception of fearful faces with increased levels of anxiety traits. These findings indicate that anxiety disorders commonly involve an initially enhanced selection of threat signals into awareness, followed by disorder-specific manifestation of diminished preferred maintenance of threat in awareness. (PsycINFO Database Record (c) 2012 APA, all rights reserved).     

Intersubject variability in fearful face processing: the linkbetween behavior and neural activation

Stimuli that signal threat show considerable variability in the extents to which they enhance behavior, even among healthy individuals. However, the neural underpinning of this behavioral variability is not well understood. By manipulating expectation of threat in an fMRI study of fearful versus neutral face categorization, we uncovered a network of areas underlying variability in threat processing in healthy adults. We explicitly altered expectations by presenting face images at three different expectation levels: 80 %, 50 %, and 20 %. Subjects were instructed to report as quickly and accurately as possible whether the face was fearful (signaled threat) or not. An uninformative cue preceded each face by 4 s. By taking the difference between reaction times (RTs) to fearful and neutral faces, we quantified an overall fear RT bias (i.e., faster to fearful than to neutral faces) for each subject. This bias correlated positively with late-trial fMRI activation (8 s after the face) during unexpected-fearful-face trials in bilateral ventromedial prefrontal cortex, the left subgenual cingulate cortex, and the right caudate nucleus, and correlated negatively with early-trial fMRI activation (4 s after the cue) during expected-neutral-face trials in bilateral dorsal striatum and the right ventral striatum. These results demonstrate that the variability in threat processing among healthy adults is reflected not only in behavior, but also in the magnitude of activation in medial prefrontal and striatal regions that appear to encode affective value.     

BRIEF REPORT

We employed a psychophysiological marker of directed attention (the visual scanpath) to investigate visuocognitive processing of particular facial expressions in healthy individuals (N = 47). Visual scanpaths were recorded using video-oculography while subjects viewed digitised photographs of threat-related (fear, anger) and nonthreat (sad, happy, neutral) facial expressions. Hypotheses regarding the existence of a differential viewing strategy for threat-related facial expressions were based upon the adaptive significance of rapid detection and effective appraisal of social threat from conspecific face stimuli. When compared with each of the nonthreat faces, viewing strategies for expressions of anger and fear were characterised by increased distance between fixations (extended scanning), with more fixations, of longer duration, to feature areas of these faces. The extended scanning style suggests that threat-related faces evoke a "vigilant" style of scanning, whereby longer saccadic eye movements may reflect heightened autonomic responses to threat, while the increased foveal attention to feature areas of threat-related faces may facilitate cognitive appraisal of the personal significance and direction of impending threat. These results suggest the existence of distinct visuocognitive patterns for processing threat-related facial expressions, in response to the evolutionary advantage of detecting and appraising social threat.     

When time stands still: fear-specific modulation of temporal bias due to threat

The current study was designed to test the fear-specific nature of temporal bias due to threat. A temporal bisection procedure was used in which participants (N = 46) were initially trained to recognize short (400 ms) and long (1,600 ms) standard durations. In the test phase, participants were asked to judge whether the duration of computer-generated faces drawn to appear threatening, fearful, and neutral, was closer to either the short or long duration they had learnt earlier. Past research was replicated-the durations of the arousing facial expressions were overestimated relative to a low arousal (neutral) expression. Overestimation for threat was positively correlated with individual differences in fearfulness, trait anxiety, and distress. Multiple regression analyses were carried out to test the hypothesis was that individual differences in anxiety and fearfulness but not other traits would uniquely predict temporal overestimation due to threat. The results showed that fearfulness but not other traits (trait anxiety, anger, distress, activity, and sociability) was a unique and strong (partial r = .47) predictor of increased overestimation for both threatening and fearful expressions. The findings support the hypothesis that threat-related expressions activate a fear-specific system (?hman & Mineka, 2001) or fear representations (Beck & Clark, 1997) in fearful individuals.     

Experimental manipulation of infant temperament affects amygdala functional connectivity

In this functional magnetic resonance imaging (fMRI) study we examined neural processing of infant faces associated with a happy or a sad temperament in nulliparous women. We experimentally manipulated adult perception of infant temperament in a probabilistic learning task. In this task, participants learned about an infant's temperament through repeated pairing of the infant face with positive or negative facial expressions and vocalizations. At the end of the task, participants were able to differentiate between “mostly sad” infants who cried often and “mostly happy” infants who laughed often. Afterwards, brain responses to neutral faces of infants with a happy or a sad temperament were measured with fMRI and compared to brain responses to neutral infants with no temperament association. Our findings show that a brief experimental manipulation of temperament can change brain responses to infant signals. We found increased amygdala connectivity with frontal regions and the visual cortex, including the occipital fusiform gyrus, during the perception of infants with a happy temperament. In addition, amygdala connectivity was positively related to the post-manipulation ratings of infant temperament, indicating that amygdala connectivity is involved in the encoding of the rewarding value of an infant with a happy temperament.     

Amygdala activation during masked presentation of emotional faces predicts conscious detection of threat-related faces

It has been argued that critical functions of the human amygdala are to modulate the moment-to-moment vigilance level and to enhance the processing and the consolidation of memories of emotionally arousing material. In this functional magnetic resonance study, pictures of human faces bearing fearful, angry, and happy expressions were presented to nine healthy volunteers using a backward masking procedure based on neutral facial expression. Activation of the left and right amygdala in response to the masked fearful faces (compared to neutral faces) was significantly correlated with the number of fearful faces detected. In addition, right but not left amygdala activation in response to the masked angry faces was significantly related to the number of angry faces detected. The present findings underscore the role of the amygdala in the detection and consolidation of memory for marginally perceptible threatening facial expression.     

A preliminary study of medial temporal lobe function in youths with a history of caregiver deprivation and emotional neglect

Previous research findings have linked caregiver deprivation and emotional neglect with sensitivity to threatening cues. The present preliminary study investigated whether dysfunctions of the medial temporal lobe could underlie these associations. Using fMRI, we measured medial temporal lobe responses to emotional faces (angry, fearful, happy, neutral) among 30 youths. Eleven of the youths had a history of caregiver deprivation and emotional neglect. Attention states (i.e., attention to anger, fear, or physical attributes, or passive viewing) were systematically manipulated. Relative to comparison youths, youths with a history of caregiver deprivation and emotional neglect showed significantly greater left amygdala and left anterior hippocampus activation during the processing of threatening information. To our knowledge, these findings are the first to demonstrate altered medial temporal lobe function during the processing of threat cues in youths with a history of caregiver deprivation and emotional neglect.     

Individual differences in cardiac vagal tone are associated with differential neural responses to facial expressions at different spatial frequencies: An ERP and sLORETA study

A previous study has shown that greater cardiac vagal tone, reflecting effective self-regulatory capacity, was correlated with superior visual discrimination of fearful faces at high spatial frequency Park et al. (Biological Psychology 90:171?C178, 2012b). The present study investigated whether individual differences in cardiac vagal tone (indexed by heart rate variability) were associated with different event-related brain potentials (ERPs) in response to fearful and neutral faces. Thirty-six healthy participants discriminated the emotion of fearful and neutral faces at broad, high, and low spatial frequencies, while ERPs were recorded. Participants with low resting heart rate variability??characterized by poor functioning of regulatory systems??exhibited significantly greater N200 activity in response to fearful faces at low spatial frequency and greater LPP responses to neutral faces at high spatial frequency. Source analyses??estimated by standardized low-resolution brain electromagnetic tomography (sLORETA)??tended to show that participants with low resting heart rate variability exhibited increased source activity in visual areas, such as the cuneus and the middle occipital gyrus, as compared with participants with high resting heart rate variability. The hyperactive neural activity associated with low cardiac vagal tone may account for hypervigilant response patterns and emotional dysregulation, which heightens the risk of developing physical and emotional problems.     

Emotional context influences access of visual stimuli to anxious individuals' awareness

Anxiety has been associated with enhanced unconscious processing of threat and attentional biases towards threat. Here, we focused on the phenomenology of perception in anxiety and examined whether threat-related material more readily enters anxious than non-anxious individuals' awareness. In six experiments, we compared the stimulus exposures required for each anxiety group to become objectively or subjectively aware of masked facial stimuli varying in emotional expression. Crucially, target emotion was task irrelevant. We found that high trait-anxiety individuals required less sensory evidence (shorter stimulus exposure times) to become aware of the face targets. This anxiety-based difference was observed for fearful faces in all experiments, but with non-threat faces, it emerged only when these were presented among threatening faces. Our findings suggest a prominent role for affective context in high-anxiety individuals' conscious perception of visual stimuli. Possible mechanisms underlying the influence of context in lowering awareness thresholds in anxious individuals are discussed.     

The effect of fearful faces on the attentional blink is task dependent

In a set of three rapid serial visual presentation experiments, we investigated the effect of fearful and neutral face stimuli on the report of trailing scene targets. When the emotional expression of the face stimuli had to be indicated, fearful faces induced a stronger attentional blink (AB) than did neutral faces. However, with identical physical stimulation, the enhancement of the AB by fearful faces disappeared when participants had to judge the faces’ gender. If faces did not have to be reported, no AB was observed. Thus, fearful faces exhibited an effect on the AB that crucially depended on the observer’s attentional set. Hence, the AB can be influenced by an emotional T1 when T1 has to be reported, but this influence is modulated by task context. This result indicates a close connection between temporal attention and emotional processing that is modulated by task context.     

Facing threat: infants' and adults' visual scanning of faces with neutral, happy, sad, angry, and fearful emotional expressions

Human faces are among the most important visual stimuli that we encounter at all ages. This importance partly stems from the face as a conveyer of information on the emotional state of other individuals. Previous research has demonstrated specific scanning patterns in response to threat-related compared to non-threat-related emotional expressions. This study investigated how visual scanning patterns toward faces which display different emotional expressions develop during infancy. The visual scanning patterns of 4-month-old and 7-month-old infants and adults when looking at threat-related (i.e., angry and fearful) versus non-threat-related (i.e., happy, sad, and neutral) emotional faces were examined. We found that infants as well as adults displayed an avoidant looking pattern in response to threat-related emotional expressions with reduced dwell times and relatively less fixations to the inner features of the face. In addition, adults showed a pattern of eye contact avoidance when looking at threat-related emotional expressions that was not yet present in infants. Thus, whereas a general avoidant reaction to threat-related facial expressions appears to be present from very early in life, the avoidance of eye contact might be a learned response toward others' anger and fear that emerges later during development.