Threat Signals Research Articles

Finding the Angry Face in the Crowd: A Comparison Between Preadolescents and Adolescents with an Emotional Visual Search Task

The facial expression of anger is considered a salient signal of threat that elicits preferential allocation of attention as expected on the basis of an evolved module of fear. Though not explicitly stated in the model, an evolved threat -detection bias should operate across different ages. However, developmental data on such an advantage of anger with photographic stimuli is limited to preschoolers. The current study compares the speed of preadolescents to those of adolescents when detecting angry and happy faces in a visual search task with photos of 9 individuals. Angry faces were detected more efficiently compared to happy ones, across the two age groups. Additionally, for adolescents, the anger advantage was modulated by face gender. These results offer among the first evidence of an anger advantage in attention processing across development.

Neural predictors and mechanisms of cognitive behavioral therapy on threat processing in social anxiety disorder

Cognitive behavioral therapy (CBT) is "gold standard" psychotherapy for social anxiety disorder (SAD). Cognitive models posit that preferential processing of threat mediates excessive forms of anxiety, which is supported by exaggerated amygdala, insula, and cortical reactivity to threatening socio-emotional signals in SAD. However, little is known about neural predictors of CBT success or the mechanisms by which CBT exerts its therapeutic effects. Functional magnetic resonance imaging (fMRI) was conducted during responses to social signals of threat (fearful/angry faces) against positive signals (happy faces) in 14 patients with SAD before and after 12 weeks of CBT. For comparison, 14 healthy control (HC) participants also underwent two fMRI scans, 12 weeks apart. Whole-brain voxel-wise analyses showed therapeutic success was predicted by enhanced pre-treatment activation to threatening faces in higher-order visual (superior and middle temporal gyrus), cognitive, and emotion processing areas (dorsal anterior cingulate cortex, dorsomedial prefrontal cortex). Moreover, a group by time interaction was revealed in prefrontal regions (dorsomedial, medial gyrus) and insula. The interaction was driven by relatively greater activity during threat processing in SAD, which significantly reduced after CBT but did not significantly predict response to CBT. Therefore, pre-treatment cortical hyperactivity to social threat signals may serve as a prognostic indicator of CBT success in SAD. Collectively, CBT-related brain changes involved a reduction in activity in insula, prefrontal, and extrastriate regions. Results are consistent with cognitive models, which associate decreases in threat processing bias with recovery.

Influence of the BDNF Genotype on Amygdalo-Prefrontal White Matter Microstructure is Linked to Nonconscious Attention Bias to Threat

Cognitive processing biases, such as increased attention to threat, are gaining recognition as causal factors in anxiety. Yet, little is known about the anatomical pathway by which threat biases cognition and how genetic factors might influence the integrity of this pathway, and thus, behavior. For 40 normative adults, we reconstructed the entire amygdalo-prefrontal white matter tract (uncinate fasciculus) using diffusion tensor weighted MRI and probabilistic tractography to test the hypothesis that greater fiber integrity correlates with greater nonconscious attention bias to threat as measured by a backward masked dot-probe task. We used path analysis to investigate the relationship between brain-derived nerve growth factor genotype, uncinate fasciculus integrity, and attention bias behavior. Greater structural integrity of the amygdalo-prefrontal tract correlates with facilitated attention bias to nonconscious threat. Genetic variability associated with brain-derived nerve growth factor appears to influence the microstructure of this pathway and, in turn, attention bias to nonconscious threat. These results suggest that the integrity of amygdalo-prefrontal projections underlie nonconscious attention bias to threat and mediate genetic influence on attention bias behavior. Prefrontal cognition and attentional processing in high bias individuals appear to be heavily influenced by nonconscious threat signals relayed via the uncinate fasciculus.

Song type matching is an honest early threat signal in a hierarchical animal communication system

Aggressive encounters between animals often involve significant amounts of signalling before or in lieu of physical fights. When, as is often the case, these apparent threat signals are neither inherently costly nor inherently indicative of fighting ability, we should ask whether they are in fact honest signals, i.e. do they predict that escalation is imminent? While signalling theories have indicated that such 'conventional' threat signals can honestly predict escalation, attempts to gather supporting empirical evidence have mostly failed. For example, recent studies in songbirds of song type matching (replying to an opponent's song with the same song type he has just sung) have failed to confirm that it predicts an eventual attack by the signaller. In the present study of song sparrows (Melospiza melodia), we tested the hypothesis that song type matching is an early threat signal in a hierarchical signalling system. We used an improved model-playback design that simulated an escalating intrusion onto the subject's territory: the simulated opponent first sang in hiding from the boundary before moving to the centre of the territory, where he revealed himself and continued to sing. We found that type matching beginning in the boundary phase and continuing into the escalation phase, or beginning immediately after the escalation, reliably predicted both subsequent escalated signalling (soft songs and wing waves) and subsequent attack on the model, supporting the hypothesis that type matching is a reliable early threat signal.

Have No Fear: The Neural Basis of Anxiolytic Drug Action in Generalized Social Phobia

Selective serotonin reuptake inhibitors (SSRIs) are first-line pharmacological treatments for anxiety disorders such as social phobia. Despite widespread use of SSRIs over the last 20 years, our understanding of how these treatments correct the disabling psychological symptoms seen in anxiety disorders is still in its infancy. Neuropsychological models highlight a key role for corticolimbic neural circuitry in anxiety, in which excessive reactivity to threat at the level of the amygdala is left unchecked by cortical systems, which usually regulate excessive or inappropriate responses to these cues. This model has been widely supported by experimental evidence across a number of anxiety disorders, shown as an imbalance in activity and/or reduced connectivity across amygdala-medial prefrontal cortex networks believed to govern our responses to a potential environmental threat ( 1 Kim M.J. Loucks R.A. Palmer A.L. Brown A.C. Solomon K.M. Marchante A.N. Whalen P.J. The structural and functional connectivity of the amygdala: from normal emotion to pathological anxiety. Behav Brain Res. 2011; 223: 403-410 Crossref PubMed Scopus (597) Google Scholar ). In this issue of Biological Psychiatry, Phan et al. ( 2 Phan KL, Coccaro EF, Angstadt M, Kreger KJ, Mayberg HS, Liberzon I, Stein MB (2013): Corticolimbic brain reactivity to social signals of threat before and after sertraline treatment in generalized social phobia. Biol Psychiatry 73:329–336. Google Scholar ) present evidence that a 12 week SSRI treatment with sertraline normalizes aberrant threat responses in this corticolimbic circuit in generalized social phobia, revealing a potentially relevant neuropsychological mechanism of anxiolytic drug action. Corticolimbic Brain Reactivity to Social Signals of Threat Before and After Sertraline Treatment in Generalized Social PhobiaBiological PsychiatryVol. 73Issue 4PreviewGeneralized social phobia (gSP), also known as generalized social anxiety disorder, is characterized by excessive fear of scrutiny by others and pervasive avoidance of social interactions. Pathophysiologic models of gSP implicate exaggerated reactivity of the amygdala and insula in response to social evaluative threat, making them plausible targets for treatment. Although selective serotonin reuptake inhibitor (SSRI) treatment is known to be an effective treatment, little is known about the mechanism through which these agents exert their anxiolytic effects at a brain level in gSP. Full-Text PDF

The social modulation of pain: others as predictive signals of salience - a systematic review.

Several studies in cognitive neuroscience have investigated the cognitive and affective modulation of pain. By contrast, fewer studies have focused on the social modulation of pain, despite a plethora of relevant clinical findings. Here we present the first review of experimental studies addressing how interpersonal factors, such as the presence, behavior, and spatial proximity of an observer, modulate pain. Based on a systematic literature search, we identified 26 studies on experimentally induced pain that manipulated different interpersonal variables and measured behavioral, physiological, and neural pain-related responses. We observed that the modulation of pain by interpersonal factors depended on (1) the degree to which the social partners were active or were perceived by the participants to possess possibility for action; (2) the degree to which participants could perceive the specific intentions of the social partners; (3) the type of pre-existing relationship between the social partner and the person in pain, and lastly, (4) individual differences in relating to others and coping styles. Based on these findings, we propose that the modulation of pain by social factors can be fruitfully understood in relation to a recent predictive coding model, the free energy framework, particularly as applied to interoception and social cognition. Specifically, we argue that interpersonal interactions during pain may function as social, predictive signals of contextual threat or safety and as such influence the salience of noxious stimuli. The perception of such interpersonal interactions may in turn depend on (a) prior beliefs about interpersonal relating and (b) the certainty or precision by which an interpersonal interaction may predict environmental threat or safety.

Drawn into the vortex: The facing-past encounter and combat in lekking male greater sage-grouse (Centrocercus urophasianus)

Lekking male greater sage-grouse (Centrocercus urophasianus) compete with neighbours not only by strutting to attract females but also by directly challenging other males. These challenges include approaching another male and adopting an anti-parallel orientation at close quarters (‘facing past encounter’) and fighting, in which the birds strike one another with their wings. Facing past encounters and facing past encounters that led to fights in free-living sage-grouse were videotaped and analysed to test predictions arising from two sets of hypotheses to account for the features of such encounters. They could be used to assess or threaten opponents (index signal or threat signal hypotheses) or they may be the result of a stalemate in which one bird’s attempts to gain an vantage point for attack are neutralised by counter moves by the other bird (combat hypothesis). Frame-by-frame analyses of both facing past encounters and fights were used to extract data to test specific predictions arising from the three hypotheses. The results, overall, support the hypothesis that the facing past orientation arises from combat. However, the results also suggest that, once in the anti-parallel orientation, opportunities emerge for communication to take place.

Reappraisal of Threat Value: Loss of Blocking in Human Aversive Conditioning

Non-specificity of fear is a core aspect of what makes anxiety disorders so impairing: Fear does not remain specific to a single stimulus paired with danger, but generalizes to a broad set of stimuli, resulting in a snowballing of threat signals. The blocking procedure can provide a valuable laboratory model for gaining insight into such threat appraisal and generalization processes. We report two experiments in which we induced selective threat appraisal by using a blocking procedure in human aversive conditioning. We subsequently assessed to what extent such selective threat appraisal is sensitive to different kinds of interference. Results illustrate that the maintenance of selective threat appraisal is not guaranteed: Stimuli present during an aversive conditioning event that are initially tagged with a low threat value, can come to be tagged with a higher threat value later on, without additional experience with these stimuli. We argue that such interference in selective threat appraisal might be one of the mechanisms underlying the pathogenesis of non-specific fear.

In the face of danger: Exploring the attentional blink to emotional facial expressions in PTSD

There is a wealth of evidence demonstrating an attentional bias to threat-related information in posttraumatic stress disorder (PTSD) and other anxiety disorders. However, there is an ongoing debate whether an enhanced identification of threatening information or rather difficulties to disengage from such signals of danger constitute this bias. The present study used a dual target rapid visual presentation paradigm to examine the temporal allocation of attention to facial expressions of anger and happiness in 16 Palestinian victims of torture with PTSD and 16 control subjects. Findings revealed that signals of threat seem to interfere with already processed information in individuals suffering from PTSD. In contrast, PTSD does not facilitate attention to threatening information. The data provide support for detrimental disengagement as an underlying mechanism of the attentional bias toward threat in PTSD, possibly contributing to symptom development and maintenance.

What Are We So Afraid of? How Early Attention Shapes Our Most Common Fears

AbstractFear is one of our most salient emotions, and one that is shared among humans and nonhumans alike. Traditional and modern views of how we acquire fear suggest that it is learned through conditioning or observation. However, an interesting aspect of human fears is that they are not all created equal—some fears are more likely to be experienced than others. In this article, I discuss some recent developmental research that sheds new light on why we are more likely to experience certain fears over others, and how attention and learning might work together to produce some of our most common fears and anxieties.

ABERRANT AMYGDALA-FRONTAL CORTEX CONNECTIVITY DURING PERCEPTION OF FEARFUL FACES AND AT REST IN GENERALIZED SOCIAL ANXIETY DISORDER

Generalized social anxiety disorder (gSAD) is characterized by exaggerated amygdala reactivity to social signals of threat, but if and how the amygdala interacts with functionally and anatomically connected prefrontal cortex (PFC) remains largely unknown. Recent evidence points to aberrant amygdala connectivity to medial PFC in gSAD at rest, but it is difficult to attribute functional relevance without the context of threat processing. Here, we address this by studying amygdala-frontal cortex connectivity during viewing of fearful faces and at rest in gSAD patients. Twenty patients with gSAD and 17 matched healthy controls (HCs) participated in functional magnetic resonance imaging of an emotional face matching task and a resting state task. Functional connectivity and psychophysiological interaction analysis were used to assess amygdala connectivity. Compared to HCs, gSAD patients exhibited less connectivity between amygdala and the rostral anterior cingulate cortex (ACC) and dorsolateral prefrontal cortex (DLPFC) while viewing fearful faces. gSAD patients also showed less connectivity between amygdala and rostral ACC at rest in the absence of fearful faces. DLPFC connectivity was negatively correlated with LSASFear (where LSAS is Liebowitz Social Anxiety Scale). Task and rest paradigms provide unique and important information about discrete and overlapping functional networks. In particular, amygdala coupling to DLPFC may be a phasic abnormality, emerging only in the presence of a social predictor of threat, whereas amygdala coupling to the rostral ACC may reflect both phasic and tonic abnormalities. These findings prompt further studies to better delineate intrinsic and externally evoked brain connectivity in anxiety and depression in relation to amygdala dysfunction.

When do people cooperate? The neuroeconomics of prosocial decision making

Understanding the roots of prosocial behavior is an interdisciplinary research endeavor that has generated an abundance of empirical data across many disciplines. This review integrates research findings from different fields into a novel theoretical framework that can account for when prosocial behavior is likely to occur. Specifically, we propose that the motivation to cooperate (or not), generated by the reward system in the brain (extending from the striatum to the ventromedial prefrontal cortex), is modulated by two neural networks: a cognitive control system (centered on the lateral prefrontal cortex) that processes extrinsic cooperative incentives, and/or a social cognition system (including the temporo-parietal junction, the medial prefrontal cortex and the amygdala) that processes trust and/or threat signals. The independent modulatory influence of incentives and trust on the decision to cooperate is substantiated by a growing body of neuroimaging data and reconciles the apparent paradox between economic versus social rationality in the literature, suggesting that we are in fact wired for both. Furthermore, the theoretical framework can account for substantial behavioral heterogeneity in prosocial behavior. Based on the existing data, we postulate that self-regarding individuals (who are more likely to adopt an economically rational strategy) are more responsive to extrinsic cooperative incentives and therefore rely relatively more on cognitive control to make (un)cooperative decisions, whereas other-regarding individuals (who are more likely to adopt a socially rational strategy) are more sensitive to trust signals to avoid betrayal and recruit relatively more brain activity in the social cognition system. Several additional hypotheses with respect to the neural roots of social preferences are derived from the model and suggested for future research.

Corticolimbic Brain Reactivity to Social Signals of Threat Before and After Sertraline Treatment in Generalized Social Phobia

Generalized social phobia (gSP), also known as generalized social anxiety disorder, is characterized by excessive fear of scrutiny by others and pervasive avoidance of social interactions. Pathophysiologic models of gSP implicate exaggerated reactivity of the amygdala and insula in response to social evaluative threat, making them plausible targets for treatment. Although selective serotonin reuptake inhibitor (SSRI) treatment is known to be an effective treatment, little is known about the mechanism through which these agents exert their anxiolytic effects at a brain level in gSP. We acquired functional magnetic resonance imaging data of brain response to social signals of threat (fearful/angry faces) in 21 gSP patients before and after they completed 12 weeks of open-label treatment with the SSRI sertraline. For comparison, 19 healthy control (HC) subjects also underwent two functional magnetic resonance imaging scans, 12 weeks apart. Whole-brain voxelwise analysis of variance revealed significant Group×Time interactions in the amygdala and the ventral medial prefrontal cortex. Follow-up analyses showed that treatment in gSP subjects reduced amygdala reactivity to fearful faces (which was exaggerated relative to HCs before treatment) and enhanced ventral medial prefrontal cortex activation to angry faces (which was attenuated relative to HCs before treatment). However, these brain changes were not significantly related to social anxiety symptom improvement. SSRI treatment response in gSP is associated with changes in a discrete limbic-paralimbic brain network, representing a neural mechanism through which SSRIs may exert their actions.

Affective Signals of Threat Increase Perceived Proximity

Do stimuli appear to be closer when they are more threatening? We tested people’s perceptions of distance to stimuli that they felt were threatening relative to perceptions of stimuli they felt were disgusting or neutral. Two studies demonstrated that stimuli that emitted affective signals of threat (e.g., an aggressive male student) were seen as physically closer than stimuli that emitted affective signals of disgust (e.g., a repulsive male student) or no affective signal. Even after controlling for the direct effects of physiological arousal, object familiarity, and intensity of the negative emotional reaction, we found that threatening stimuli appeared to be physically closer than did disgusting ones (Study 2). These findings highlight the links among biased perception, action regulation, and successful navigation of the environment.

Oxytocin differentially modulates eye gaze to naturalistic social signals of happiness and anger

A number of previous studies has shown that oxytocin (OT) promotes facial emotion recognition and enhances eye gaze to facial stimuli in humans. Other studies report valence-specific effects of OT, supporting the proposed prosocial role of OT in social interactions. In the present study, we tested the hypothesis whether OT might selectively enhance eye gaze to positive, approach-related, but not to negative, threat-related social cues. In a placebo-controlled, double-blind, between-subject design, we assessed the effects of intranasal OT administration (24 IU) in 62 healthy male volunteers on eye gaze toward the eyes of neutral, positive (happy) and negative (angry) facial expressions compared with placebo. In order to capture the dynamics of facial expressions, we used video sequences showing neutral faces gradually displaying a specific emotion. In line with previous studies, OT increased eye gaze toward neutral facial expressions. Moreover, under OT treatment, eye gaze remained increased when the face showed a happy facial expression, but in contrast decreased when the face displayed an angry expression. These results support the notion that OT differentially modulates visual attention toward social signals of positive approach and threat and thereby contributes to the modulation of non-verbal interpersonal communication.

Onset and offset of aversive events establish distinct memories requiring fear and reward networks

Two things are worth remembering about an aversive event: What made it happen? What made it cease? If a stimulus precedes an aversive event, it becomes a signal for threat and will later elicit behavior indicating conditioned fear. However, if the stimulus is presented upon cessation of the aversive event, it elicits behavior indicating conditioned "relief." What are the neuronal bases for such learning? Using functional magnetic resonance imaging (fMRI) in humans we found that a fear-conditioned stimulus activates amygdala but not striatum, whereas a relief-conditioned stimulus activates striatum but not amygdala. Correspondingly, acute inactivation of amygdala or of ventral striatum in rats respectively abolished only conditioned fear or only conditioned relief. Thus, the behaviorally opponent memories supported by onset and offset of aversive events engage and require fear and reward networks, respectively. This may explain attraction to stimuli associated with the cessation of trauma or of panic attacks.

Social behavior of dwarf geckos (Sphaerodactylus): a comparative repertoire

Variation in sexual dichromatism of dwarf geckos may affect the ability to use visual signals in sex recognition. Social interactions of nine species of dwarf geckos, covering the range of color pattern variation, were staged and videotaped in captivity. Sequential and nonsequential behavioral data allowed comparing species repertoires, uncovering associations between behavioral traits and variation in dichromatism, exploring potential sex recognition cues, and exploring potential functions of the most common courtship and threat signals. Males and females shared a similar social behavioral repertoire but some homotypical behaviors and different behavioral profiles were common to all species. A correlation between the use of threat signals and variation in sexual dichromatism was the most noticeable behavioral correlate among species. Whereas males from dimorphic species restricted the use of threat signals to agonistic contexts, males from monochromatic species displayed threat signals in agonistic and sexual contexts. All species seemed able to recognize conspecifics' sex through visual cues, but semiochemicals seemed to provide the most reliable sex recognition cues. Contextual and sequential data reinforced the previous suggestion that headbobs and stiff are the main courtship and threat signals, respectively. Stiff in monochromatic species, however, may have been co-opted to play a role in courtship as well.

The Scorn of Status: A Bias Toward Perceiving Anger on High-Status Faces

The expression of anger is an important signal of both danger and threat to social relationships. Furthermore, anger expressed by high-status people should be especially apparent due to the fact that high-status people may be perceived as more able to act on their intentions than low-status people. In the current research, we test the hypothesis that a perceiver will be biased toward anger appearing on the face of a high-status compared to a low-status face. Using an emotion detection task across two experiments, our findings revealed that White participants perceived anger to persist longer (Study 1) and appear sooner (Study 2) on the faces of high-status compared to low-status targets. This suggests that social context, in general, and social status (as indicated by occupation), in particular, can influence the perception of anger.

Trust at first sight: evidence from ERPs

We used event-related potentials (ERPs) to tap the temporal dynamics of first impressions based on face appearance. Participants were asked to evaluate briefly presented faces for trustworthiness and political choice. Behaviorally, participants were better at discriminating faces that were pre-rated as untrustworthy. The ERP results showed that the P100 component was enhanced for untrustworthy faces, consistently with the view that signals of potential threat are given precedence in neural processing. The enhanced ERP responses to untrustworthy faces persisted throughout the processing sequence and the amplitude of early posterior negativity (EPN), and subsequent late positive potential (LPP) was increased with respect to trustworthy faces which, in contrast, elicited an enhanced positivity around 150 ms on frontal sites. These ERP patterns were found specifically for the trustworthiness evaluation and not for the political decision task. Political decision yielded an increase in the N170 amplitude, reflecting a more demanding and taxing structural encoding. Similar ERP responses, as previously reported in the literature for facial expressions processing, were found throughout the entire time course specifically elicited by faces explicitly judged as untrustworthy. One possibility might be that evolution has provided the brain with a 'special toolkit' for trust evaluation that is fast and triggers ERPs related to emotional processing.

Testosterone administration in women increases amygdala responses to fearful and happy faces

Data from both rodents and humans show that testosterone reduces fear. This effect is hypothesized to result from testosterone's down regulating effects on the amygdala, a key region in the detection of threat and instigator of fight-or-flight behavior. However, neuroimaging studies employing testosterone administration in humans have consistently shown increased amygdala responsivity. Yet, no study to date has investigated specifically how testosterone affects the amygdala response to fearful emotional expressions. Such stimuli signal the presence of environmental threat and elicit robust amygdala responses that have consistently been associated with anxious traits. In the present study, we therefore used functional magnetic resonance imaging combined with a single administration of 0.5mg testosterone in 12 healthy women to assess testosterone's effects on amygdala responses to dynamic fearful (and happy control) faces. Our results show that both stimuli activate the amygdala. Notably, testosterone increased the amygdala response to both stimuli, and to an equal degree. Thus, testosterone appears not to reduce fear by attenuating the amygdala response toward signals of threat. Data further show that testosterone selectively increases activation of the superficial amygdala (SFA) and, to a lesser extent, the basolateral amygdala (BLA). No effect was found in the central nucleus, which is involved in the generation of autonomic fear responses. Both the SFA and BLA are considered input regions, and enhanced activation by testosterone might reflect the role of this hormone in adaptive responding to socially relevant stimuli. Furthermore, literature on the distinct roles of the SFA and BLA in fear processing show that increased activation of these subregions of the amygdala is consistent with a fear reducing effect of testosterone.