Fearful Eyes Research Articles

Oxytocin Modulates Amygdala Reactivity to Masked Fearful Eyes.

The amygdala reveals enhanced reactivity to fearful eye whites, even when they are backwardly masked by a neutral face and therefore processed with limited visual awareness. In our fMRI study, we investigated whether this effect is indeed associated with fear detection within the eyes of the neutral face mask, or more generally, with reactivity to any salient increase in eye white area. In addition, we examined whether a single dose of intranasal oxytocin would modulate amygdala responses to masked fearful eye whites via a double-blind, placebo-controlled pharmacological protocol. We found that increased amygdala responses to salient changes within a face's eye region occurred specifically for masked fearful eyes but not for similar increases in white area as induced by nonsocial control stimuli. Administration of oxytocin attenuated amygdala responses to masked fearful eye whites. Our results suggest that the amygdala is particularly tuned to potential threat signals from the eye region. The dampening effects of oxytocin on early amygdala reactivity may reflect reduced vigilance for facial threat cues at a preconscious level. Future studies may investigate whether this early modulation accounts for the beneficial effects of oxytocin on social cognition in anxiety-related disorders, as suggested by previous studies.

Empathy in young people: change in patterns of eye gaze and brain activity with the manipulation of visual attention to emotional faces.

Event Abstract Back to Event Empathy in young people: change in patterns of eye gaze and brain activity with the manipulation of visual attention to emotional faces. Jason M. Bruggemann1*, Karen Burton1, Kristin Laurens2, Vaughan Macefield3, Mark Dadds4, Melissa Green2 and Rhoshel Lenroot1 1 University of New South Wales, School of Psychiatry & Neuroscience Research Australia, Australia 2 University of New South Wales, School of Psychiatry, Australia 3 University of New South Wales, Neuroscience Research Australia, Australia 4 University of New South Wales, School of Psychology, Australia Background and aims: Understanding the emotional state of others is fundamental to effective social interaction and the development of empathy. Critical information is conveyed via the eyes, and reduced attention to the eyes is associated with poorer emotion recognition and empathic deficits in individuals with disorders affecting social cognition such as autism or some types of conduct problems. Deliberately redirecting attention to the eyes may be a way of improving behaviour. However, the effects of directing attention on brain activity during emotional processing has not been studied previously. Our aim was to determine whether manipulation of visual attention in youths affects their eye gaze patterns and brain responses to expression of emotions in others. Method: Eighteen typically developing male youths aged 8-16 performed an implicit facial emotion processing task while viewing different facial expressions (fearful, neutral, happy), presented in three separate blocks under three different instructions: undirected, eye-gaze and mouth-gaze. Eye tracking (dwell time) and functional-MRI data were acquired concurrently as measures of visual attention and brain response, respectively. Results: Eye tracking indicated that the youths attended more to the eyes than the mouth in the undirected condition. Redirecting attention to the eyes and mouth significantly increased attention to these areas. Compared to undirected, directing attention to the fearful eyes also produced a greater increase in attention than neutral eyes. Attention directed to eyes elicited greater brain activity in frontal regions than undirected attention. Conclusions: The undirected eye gaze patterns indicate natural orienting to eyes in healthy youths, which can be effectively altered with instruction. Directing attention to fearful eyes engaged attention relatively longer than neutral, consistent with the threat value of fearful faces. These data also demonstrate that manipulation of visual attention modulates activity in frontal regions, perhaps reflecting greater engagement of executive function due to attentional demands. Understanding attentional manipulation effects in a healthy sample will inform ongoing work addressing potentially perturbed response patterns in a conduct problem cohort. Keywords: Attention, emotion, face processing, Empathy, Conduct Disorder, fMRI, eye tracking, Dwell time Conference: ASP2015 - 25th Annual Conference of the Australasian Society for Psychophysiology, Sydney, Australia, 2 Dec - 4 Dec, 2015. Presentation Type: Oral Presentation Topic: Psychophysiology Citation: Bruggemann JM, Burton K, Laurens K, Macefield V, Dadds M, Green M and Lenroot R (2015). Empathy in young people: change in patterns of eye gaze and brain activity with the manipulation of visual attention to emotional faces.. Conference Abstract: ASP2015 - 25th Annual Conference of the Australasian Society for Psychophysiology. doi: 10.3389/conf.fnhum.2015.219.00011 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 01 Nov 2015; Published Online: 30 Nov 2015. * Correspondence: Dr. Jason M Bruggemann, University of New South Wales, School of Psychiatry & Neuroscience Research Australia, Randwick, NSW, 2031, Australia, j.bruggemann@unsw.edu.au Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Jason M Bruggemann Karen Burton Kristin Laurens Vaughan Macefield Mark Dadds Melissa Green Rhoshel Lenroot Google Jason M Bruggemann Karen Burton Kristin Laurens Vaughan Macefield Mark Dadds Melissa Green Rhoshel Lenroot Google Scholar Jason M Bruggemann Karen Burton Kristin Laurens Vaughan Macefield Mark Dadds Melissa Green Rhoshel Lenroot PubMed Jason M Bruggemann Karen Burton Kristin Laurens Vaughan Macefield Mark Dadds Melissa Green Rhoshel Lenroot Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

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.

Social anxiety and interpretation of ambiguous smiles

This study investigated whether social anxiety facilitates the discrimination between genuine and ambiguous smiles. Socially anxious (N=20) and nonanxious (N=20) participants categorized as “happy” or “not happy” faces with either (1) a truly happy expression (i.e., happy eyes and a smile), (2) truly nonhappy expressions (e.g., angry eyes and an angry mouth), or (3) blended expressions with a smiling mouth and nonhappy (e.g., angry, sad, etc.) eyes. Results indicated that, relative to nonanxious participants, those high in social anxiety were more likely to judge as “not happy” any blended expression with nonhappy eyes, and they were faster in judging as “not happy” the blended expressions with angry, fearful, or disgusted eyes (but not those with sad, surprised, or neutral eyes). These results suggest, respectively, that social anxiety inhibits a benign interpretation of all the ambiguous expressions with a smile, and speeds up the detection of threatening eyes in such expressions. Importantly, no differences appeared as a function of social anxiety for truly happy or nonhappy faces. This rules out a response-bias explanation, and also reveals that social anxiety does not affect sensitivity in the recognition of prototypical expressions.

Neural responses to fearful eyes in children with conduct problems and varying levels of callous–unemotional traits

Children with conduct problems (CP) are a heterogeneous group. Those with high levels of callous-unemotional traits (CP/HCU) appear emotionally under-reactive at behavioural and neural levels whereas those with low levels of CU traits (CP/LCU) appear emotionally over-reactive, compared with typically developing (TD) controls. Investigating the degree to which these patterns of emotional reactivity are malleable may have important translational implications. Instructing participants with CP/HCU to focus on the eyes of fearful faces (i.e. the most salient feature) can ameliorate their fear-recognition deficits, but it is unknown whether this is mediated by amygdala response. It is also unknown whether focusing on fearful eyes is associated with increased amygdala reactivity in CP/LCU. Functional magnetic resonance imaging (fMRI) was used to measure neural responses to fearful and calm faces in children with CP/HCU, CP/LCU and TD controls (n = 17 per group). On half of trials participants looked for a blue dot anywhere within target faces; on the other half, participants were directed to focus on the eye region. Reaction time (RT) data showed that CP/LCU were selectively slowed in the fear/eyes condition. For the same condition, CP/LCU also showed increased amygdala and subgenual anterior cingulate cortex (sgACC)/orbitofrontal cortex (OFC) responses compared with TD controls. RT and amygdala response to fear/eyes were correlated in CP/LCU only. No effects of focusing on the eye region were observed in CP/HCU. These data extend the evidence base suggesting that CU traits index meaningful heterogeneity in conduct problems. Focusing on regulating reactive emotional responses may be a fruitful strategy for children with CP/LCU.

Fear and happiness in the eyes: An intra-cerebral event-related potential study from the human amygdala

We present the response pattern of intracranial event-related potentials (ERPs) recorded from depth-electrodes in the human amygdala (four patients) to faces or face parts encoding fearful, happy or neutral expressions. The amygdala showed increased amplitude ERPs (from 200 to 400 ms post-stimulus) in response to the eye region of the face compared to whole faces and to the mouth region. In particular, a strong emotional valence effect was observed, both at group and at single-subject level, with a preferential response to fearful eyes respect to every other stimulus category from 200 to 400 ms after stimulus presentation. A preferential response to smiling eyes compared to happy faces and smiling mouths was also observed at group level from 300 to 400 ms post-stimulus presentation. A complementary time–frequency analysis was performed showing that an increase in the theta frequency band (4–7 Hz) accounted for the main event-related band power (ERBP) change during the 200–500 ms post stimulus interval. The analysis of the ERBPs changes according to their emotional valence showed a strong increase in theta ERBP to fearful eyes, which was higher respect to any other facial stimulus. Moreover, theta ERBP increase to “smiling eyes” was larger respect with that evoked by smiling mouths and whole happy faces. Minimal post-stimulus ERBPs changes were evoked by neutral stimuli. These data are consistent with a special role of the amygdala in processing facial signals, both with negative and positive valence, conveyed by the eye region of the face.

Do fearful eyes activate empathy-related brain regions in individuals with callous traits?

Psychopathy, a developmental disorder characterized by profound social disturbance, is associated with impaired recognition of distress cues. Since distress processing and moral socialization are closely linked, uncovering techniques to improve distress recognition could have positive treatment implications for developmental disorders that feature empathy impairments. Previous studies demonstrate that fear-recognition deficits can be remedied by redirecting attention to critical cues (the eyes for fearful faces). However, it remains unclear whether this manipulation increases activity in empathy-related brain regions, or has an alternate compensatory effect that may not promote prosocial behaviours. In this fMRI study, a community sample of individuals with high vs low callous traits completed an emotion recognition task that varied whether the most or least socially meaningful facial features were visible (the eyes were isolated or occluded). For fearful faces, individuals with high callous traits showed significantly less amygdala and medial prefrontal cortex activity than those with low callous traits when the eyes were occluded, but not when they were isolated. Consistent with recent models of the amygdala that emphasize orientation to disambiguate stimuli rather than represent distress, individuals with low trait empathy showed greater amygdala activity to the least vs most socially meaningful features of fearful faces.

The volatility of the amygdala response to masked fearful eyes

Recently, it has been suggested that backwardly masked, and thus subliminally presented, fearful eyes are processed by the amygdala. Here, we investigated in four functional magnetic resonance imaging experiments whether the amygdala responds to subliminally presented fearful eyes per se or whether an interaction of masked eyes with the masks or with parts of the masks used for backward masking might be responsible for the amygdala activation. In these experiments, we varied the mask as well as the position of the target eyes. The results show that the amygdala does not respond to masked fearful eyes per se but to an interaction between masked fearful eyes and the eyes of neutral faces used for masking. This finding questions the hypothesis that the amygdala processes context-free parts of the human face without awareness.

Fearful faces but not fearful eyes alone delay attention disengagement in 7-month-old infants.

Adult-like attentional biases toward fearful faces can be observed in 7-month-old infants. It is possible, however, that infants merely allocate attention to simple features such as enlarged fearful eyes. In the present study, 7-month-old infants (n = 15) were first shown individual emotional faces to determine their visual scanning patterns of the expressions. Second, an overlap task was used to examine the latency of attention disengagement from centrally presented faces. In both tasks, the stimuli were fearful, happy, and neutral facial expressions, and a neutral face with fearful eyes. Eye-tracking data from the first task showed that infants scanned the eyes more than other regions of the face; however, there were no differences in scanning patterns across expressions. In the overlap task, infants were slower in disengaging attention from fearful as compared to happy and neutral faces and also to neutral faces with fearful eyes. Together, these results provide evidence that threat-related stimuli tend to hold attention preferentially in 7-month-old infants and that the effect does not reflect a simple response to differentially salient eyes in fearful faces.

Human brain responsivity to different intensities of masked fearful eye whites: An ERP study

Previous studies have shown differential event-related potentials (ERPs) to intensities of fearful facial expressions. There are indications that the eyes may be particularly relevant for the recognition of fearful expressions, even the amount of white sclera exposed above and on sides of the dark pupil could activate the amygdala response. To investigate whether the ERP differences between intensities of fearful expressions are driven by the differential salience of the eyes in the fearful faces, ERPs were measured within a backward masking paradigm, where observers were asked to do a gender-decision task with male and female neutral faces. The emotional stimuli used were low-intensity (50%), prototypical (100%), and caricatured (150%) fearful eye whites that were derived from corresponding intensities of fearful faces respectively. Three groups of white squares that have the same pixels as the eye whites were created as control conditions. Analysis of the ERP data showed a linear increase in amplitudes of the parietal–occipital P120 by three intensities of fearful eye whites. These ERP effects were proved sensitive to intensities of negative emotions but not to the simple physical features as the same patterns of differences were not observed on white squares. Larger parietal–occipital P250 amplitudes were observed for caricatured 150% than low-intensity 50% fearful eye whites. It might reflect the subcortical pathway of emotion-specific, fearful processing. The results demonstrate that the human brain is sensitive to intensities of fear, even if just shown intensities of fearful eye white in the absence of awareness.

An investigation of basic facial expression recognition in autism spectrum disorders

This study was designed to test three competing hypotheses (impaired configural processing; impaired Theory of Mind; atypical amygdala functioning) to explain the basic facial expression recognition profile of adults with autism spectrum disorders (ASD). In Experiment 1 the Ekman and Friesen (1976) series were presented upright and inverted. Individuals with ASD were significantly less accurate than controls at recognising upright facial expressions of fear, sadness and disgust and their pattern of errors suggested some configural processing difficulties. Impaired recognition of inverted facial expressions suggested some additional difficulties processing the facial features. Unexpectedly, the clinical group misidentified fear as anger. In Experiment 2 feature processing of facial expressions was investigated by presenting stimuli in a piecemeal fashion, starting with either just the eyes or the mouth. Individuals with ASD were impaired at recognising fear from the eyes and disgust from the mouth; they also confused fearful eyes as being angry. The findings are discussed in terms of the three competing hypotheses tested.

The left amygdala knows fear: laterality in the amygdala response to fearful eyes.

The detection of threat is a role that the amygdala plays well, evidenced by its increased response to fearful faces in human neuroimaging studies. A critical element of the fearful face is an increase in eye white area (EWA), hypothesized to be a significant cue in activating the amygdala. However, another important social signal that can increase EWA is a lateral shift in gaze direction, which also serves to orient attention to potential threats. It is unknown how the amygdala differentiates between these increases in EWA and those that are specifically associated with fear. Using functional magnetic resonance imaging, we show that the left amygdala distinguished between fearful eyes and gaze shifts despite similar EWA increases whereas the right amygdala was less discriminatory. Additional analyses also revealed selective hemispheric response patterns in the left fusiform gyrus. Our data show clear hemispheric differences in EWA-based fear activation, suggesting the existence of parallel mechanisms that code for emotional face information.

The volatility of the amygdala response to masked fearful eyes

The volatility of the amygdala response to masked fearful eyes

Probing the sanctum sanctorum: New eyes and approaches explore the diversity of vertebrate brains

Probing the <i>sanctum sanctorum</i>: New eyes and approaches explore the diversity of vertebrate brains

Human Amygdala Responsivity to Masked Fearful Eye Whites

The amygdala was more responsive to fearful (larger) eye whites than to happy (smaller) eye whites presented in a masking paradigm that mitigated subjects' awareness of their presence and aberrant nature. These data demonstrate that the amygdala is responsive to elements of.

Human Amygdala Responses to Fearful Eyes

Fearfulfacial expressions evoke increased neural responses in human amygdala. We used event-related fMRI to investigate whether eye or mouth components of a fearful face are critical in evoking this increased amygdala activity. In addition to prototypical fearful (FF) and neutral (NN) faces, subjects viewed two types of chimerical face: fearful eyes combined with a neutral mouth (FN), and neutral eyes combined with a fearful mouth (NF). FF faces evoked specific responses in left anterior amygdala. FN faces evoked responses in bilateral posterior amygdala and superior colliculus. Responses in right amygdala, superior colliculus, and pulvinar exhibited significant time × condition interactions with respect to faces with fearful eyes (FF, FN) vs neutral eyes (NF, NN). These data indicate that fearful eyes alone are sufficient to evoke increased amygdala activity. In addition, however, left amygdala displayed discriminatory responses to fearful eyes in different configural contexts (i.e., in FF and FN faces). These results suggest, therefore, that human amygdala responds to both feature-specific and configural aspects of fearful facial expressions.

Journey to the Styx: A Broadcast Talk

Styx—river of Hell! Why, there is magic in the very name. What memories of our childhood it conjures up! Charon, the grim ferryman, his fearful eyes aglare. Shades of men and heroes thronging the phantom shores. Ghosts and monsters, and yet more ghosts. Aye, and older legends too. Silver-footed Thetis dipping her babe, and the gods themselves swearing dread oaths on its waters. But how many of you, I wonder, when you read those stories at school, realized that the Styx actually existed? Well, it does; and I decided that if ever I had the good fortune to go to Greece, I would endeavour to visit it.