Variations in the serotonin-transporter gene are associated with attention bias patterns to positive and negative emotion faces

Both attention biases to threat and a serotonin-transporter gene polymorphism (5-HTTLPR) have been linked to heightened neural activation to threat and the emergence of anxiety. The short allele of 5-HTTLPR may act via its effect on neurotransmitter availability, while attention biases shape broad patterns of cognitive processing. We examined individual differences in attention bias to emotion faces as a function of 5-HTTLPR genotype. Adolescents (N = 117) were classified for presumed SLC6A4 expression based on 5-HTTLPR—low (SS, SL_G, or L_GL_G), intermediate (SL_A or L_AL_G), or high (L_AL_A). Participants completed the dot-probe task, measuring attention biases toward or away from angry and happy faces. Biases for angry faces increased with the genotype-predicted neurotransmission levels (low > intermediate > high). The reverse pattern was evident for happy faces. The data indicate a linear relation between 5-HTTLPR allelic status and attention biases to emotion, demonstrating a genetic mechanism for biased attention using ecologically valid stimuli that target socioemotional adaptation.     

Neural activation during the processing of ambiguous fearful facial expressions: an ERP study in anxious and nonanxious individuals

Event-related brain potentials (ERPs) were recorded from anxious and nonanxious participants during performance on a fear detection task. Sequential presentation of gradually increasing fear cues from neutral to fearful allowed an examination of anxiety-related differences in the neural activation patterns corresponding to participants' overt detection of fear in ambiguous stimuli as well as the activation patterns corresponding to stages of fear processing preceding overt fear detection. While centro-parietal Late Positive Potential (LPP) amplitude of nonanxious participants was significantly modulated by increases in stimulus fear intensity preceding overt fear detection, no such LPP sensitivity was detected in anxious participants. Additionally, anxiety group differences as well as emotion related modulation were found for earlier ERP components (P1, P2 and EPN). These findings reveal an anxiety-related dissociation between the early and late processing stages of threat processing. Implications are discussed in light of existing theories of cognitive biases in anxiety.     

The effects of cortisol administration on approach–avoidance behavior: An event-related potential study

We investigated the effects of cortisol administration (50 mg) on approach and avoidance tendencies in low and high trait avoidant healthy young men. Event-related brain potentials (ERPs) were measured during a reaction time task, in which participants evaluated the emotional expression of photographs of happy and angry faces by making an approaching (flexion) or avoiding (extension) arm movement. The task consisted of an affect-congruent (approach happy faces and avoid angry faces) and an affect-incongruent (reversed instruction) condition. Behavioral and ERP analyses showed that cortisol enhanced congruency effects for angry faces in highly avoidant individuals only. The ERP effects involved an increase of both early (P150) and late (P3) positive amplitudes, indicative of increased processing of the angry faces in high avoidant subjects after cortisol administration. Together, these results suggest a context-specific effect of cortisol on processing of, and adaptive responses to, motivationally significant threat stimuli, particularly in participants highly sensitive to threat signals.     

Effects of social anxiety and facial expression on habituation of the electrodermal orienting response.

The present research examined electrodermal orienting to happy and angry faces as a function of social anxiety and threat of shock. A preliminary study using 569 undergraduate participants developed an adequate set of normative data of social anxiety for the Willoughby questionnaire (WQ) for use in subject selection. Electrodermal activity was measured in both high and low socially anxious subjects (N = 85) during exposure to 10 presentations of an angry face intermixed with 10 presentations of a happy face. Threat of shock (no-shock, shock work-up only, and shock work-up plus threat) was also manipulated. Skin conductance responses (SCRs) which occurred within 1-4 s of stimulus onset and trials-to-habituation constituted the data of primary interest. Although trials-to-habituation did not differ between angry and happy facial expressions, SCRs were larger to the angry face than to the happy face in both high and low socially anxious subjects. No differences in SCR magnitude were found as a function of threat of shock. The implications of these results for Ohman's functional-evolutionary model of social phobia are discussed, and alternative explanations in terms of prepotency and prior learning are examined.     

The impact of the stimulus features and task instructions on facial processing in social anxiety: An ERP investigation

Social anxiety has been characterized by an attentional bias towards threatening faces. Electrophysiological studies have demonstrated modulations of cognitive processing from 100 ms after stimulus presentation. However, the impact of the stimulus features and task instructions on facial processing remains unclear. Event-related potentials were recorded while high and low socially anxious individuals performed an adapted Stroop paradigm that included a colour-naming task with non-emotional stimuli, an emotion-naming task (the explicit task) and a colour-naming task (the implicit task) on happy, angry and neutral faces. Whereas the impact of task factors was examined by contrasting an explicit and an implicit emotional task, the effects of perceptual changes on facial processing were explored by including upright and inverted faces. The findings showed an enhanced P1 in social anxiety during the three tasks, without a moderating effect of the type of task or stimulus. These results suggest a global modulation of attentional processing in performance situations.     

The effects of cortisol administration on approach-avoidance behavior: an event-related potential study

We investigated the effects of cortisol administration (50 mg) on approach and avoidance tendencies in low and high trait avoidant healthy young men. Event-related brain potentials (ERPs) were measured during a reaction time task, in which participants evaluated the emotional expression of photographs of happy and angry faces by making an approaching (flexion) or avoiding (extension) arm movement. The task consisted of an affect-congruent (approach happy faces and avoid angry faces) and an affect-incongruent (reversed instruction) condition. Behavioral and ERP analyses showed that cortisol enhanced congruency effects for angry faces in highly avoidant individuals only. The ERP effects involved an increase of both early (P150) and late (P3) positive amplitudes, indicative of increased processing of the angry faces in high avoidant subjects after cortisol administration. Together, these results suggest a context-specific effect of cortisol on processing of, and adaptive responses to, motivationally significant threat stimuli, particularly in participants highly sensitive to threat signals.     

Cortisol-induced enhancement of emotional face processing in social phobia depends on symptom severity and motivational context

We investigated the effects of cortisol administration on approach and avoidance tendencies in 20 patients with social anxiety disorder (SAD). Event-related brain potentials (ERPs) were measured during a reaction time task, in which patients evaluated the emotional expression of photographs of happy and angry faces by making an approaching (flexion) or avoiding (extension) arm movement. Patients showed significant avoidance tendencies for angry but not for happy faces, both in the placebo and cortisol condition. Moreover, ERP analyses showed a significant interaction of condition by severity of social anxiety on early positive (P150) amplitudes during avoidance compared to approach, indicating that cortisol increases early processing of social stimuli (in particular angry faces) during avoidance. This result replicates previous findings from a non-clinical sample of high anxious individuals and demonstrates their relevance for clinical SAD. Apparently the cortisol-induced increase in processing of angry faces in SAD depends on symptom severity and motivational context.     

Startle modulation by affective faces

Startle reflex modulation by affective pictures is a well-established effect in human emotion research. However, much less is known about startle modulation by affective faces, despite the growing evidence that facial expressions robustly activate emotion-related brain circuits. In this study, acoustic startle probes were administered to 37 young adult participants (20 women) during the viewing of slides from the Pictures of Facial Affect set including neutral, happy, angry, and fearful faces. The effect of expression valence (happy, neutral, and negative) on startle magnitude was highly significant (p < .001). Startle reflex was strongly potentiated by negative expressions (fearful and angry), however, no attenuation by happy faces was observed. A significant valence by gender interaction suggests stronger startle potentiation effects in females. These results demonstrate that affective facial expressions can produce significant modulation of the startle reflex.     

Emotion in voice matters: Neural correlates of emotional prosody perception

The ability to perceive emotions is imperative for successful interpersonal functioning. The present study examined the neural characteristics of emotional prosody perception with an exploratory event-related potential analysis. Participants were 59 healthy individuals who completed a discrimination task presenting 120 semantically neutral word pairs from five prosody conditions (happy/happy, angry/angry, neutral/neutral, angry/happy, happy/angry). The task required participants to determine whether words in the pair were spoken in same or different emotional prosody. Reflective of an initial processing stage, the word 1 N1 component was found to have greatest amplitude in parietal regions of the hemispheres, and was largest for emotional compared to neutral stimuli, indicating detection of emotion features. A second processing stage, represented by word 1 P2, showed similar topographic effects; however, amplitude was largest for happy in the left hemisphere while angry was largest in the right, illustrating differentiation of emotions. At the third processing stage, word 1 N3 amplitude was largest in frontal regions, indicating later cognitive processing occurs in the frontal cortex. N3 was largest for happy, which had lowest accuracy compared to angry and neutral. The present results support Schirmer and Kotz's (2006) model of vocal emotion perception because they elucidated the function and ERP components by reflecting three primary stages of emotional prosody perception, controlling for semantic influence.     

The effects of social stress and cortisol responses on the preconscious selective attention to social threat

The purpose of the present study was to investigate the effects of social stress and stress-induced cortisol on the preconscious selective attention to social threat. Twenty healthy participants were administered a masked emotional Stroop task (comparing color-naming latencies for angry, neutral and happy faces) in conditions of rest and social stress. Stress was induced by means of the Trier social stress test. Based on the stress-induced increase in cortisol levels, participants were allocated post hoc (median-split) to a high and low responders group. In contrast to low responders, high responders showed a negative or avoidant attentional bias to threat (i.e. shorter latencies for angry than neutral faces) in the rest condition. Most importantly, although low responders became avoidant, the high responders became vigilant to the angry faces after stress induction. There were no such effects for happy faces. Our findings are in line with previous studies in both animals and humans, that associate high glucocorticoid stress-responsiveness with diminished avoidance and prolonged freezing reactions during stress.     

Don't look at me in anger! Enhanced processing of angry faces in anticipation of public speaking

Anxiety is supposed to enhance the processing of threatening information. Here, we investigated the cortical processing of angry faces during anticipated public speaking. To elicit anxiety, a group of participants was told that they would have to perform a public speech. As a control condition, another group was told that they would have to write a short essay. During anticipation of these tasks, participants saw facial expressions (angry, happy, and neutral) while electroencephalogram was recorded. Event‐related potential analysis revealed larger N170 amplitudes for angry compared to happy and neutral faces in the anxiety group. The early posterior negativity as an index of motivated attention was also enhanced for angry compared to happy and neutral faces in participants anticipating public speaking. These results indicate that fear of public speaking influences early perceptual processing of faces such that especially the processing of angry faces is facilitated.     

The N170 to Angry Faces Predicts Anxiety in Typically Developing Children Over a Two-Year Period

Enhanced threat processing has been associated with elevated anxiety in adults, but less is known about how threat processing influences the developmental trajectory of anxiety in children. We used the N170 to measure threat (angry faces) processing in relation to child anxiety over a 2-year period. Participants were 27 typically developing 5-to-7-year-olds (13 females). Higher anxiety when children were aged 5 to 7 was associated with higher anxiety 2 years later, but only for children showing larger N170 amplitudes to angry versus happy faces. The N170 captures individual differences in threat processing that may characterize children at enhanced risk for anxiety.     

Relationship between trait anxiety, prefrontal cortex, and attention bias to angry faces in children and adolescents

Using event-related functional magnetic resonance imaging (fMRI) with a visual-probe task that assesses attention to threat, we investigated the cognitive and neurophysiological correlates of trait anxiety in youth. During fMRI acquisition, 16 healthy children and adolescents viewed angry-neutral face pairs and responded to a probe that was on the same (angry-congruent) or opposite (angry-incongruent) side as the angry face. Attention bias scores were calculated by subtracting participants' mean reaction time for angry-congruent trials from angry-incongruent trials. Trait anxiety was positively associated with attention bias towards angry faces. Neurophysiologically, trait anxiety was positively associated with right dorsolateral prefrontal cortex (PFC) activation on a contrast of trials that reflect the attention bias for angry faces (i.e. angry-incongruent versus angry-congruent trials). Trait anxiety was also positively associated with right ventrolateral PFC activation on trials with face stimuli (vesus baseline), irrespective of their emotional content.     

The role of age and ethnic group in face recognition memory: ERP evidence from a combined own-age and own-race bias study

Young adult participants are known to more accurately remember faces from both their own age- and ethnic groups. The present study examined combined effects of such own-age and own-race biases by asking young Caucasian participants to learn and remember elderly and young Caucasian as well as elderly and young Asian faces. Neural correlates were assessed by recording event-related potentials (ERPs). Behavioral results indicated both an own-race bias for young but not elderly faces, and an own-age bias for Caucasian but not Asian faces. Importantly, no additional decrease in recognition memory for other-race/other-age faces was detected. An early parietal ERP old/new effect (300-500 ms) was most pronounced for young Caucasian “in-group” faces, while the old/new effect in a later time window (500-800 ms) was generally larger for own- as compared to other-race faces. In conclusion, these findings suggest at least partly different neural processes to accompany the own-race and own-age biases.     

An event-related potential study of the processing of affective facial expressions in young children who experienced maltreatment during the first year of life

This investigation examined the effects of maltreatment during the first year of life on the neural correlates of processing facial expressions of emotion at 30 months of age. Event-related potentials (ERPs) in response to children passively viewing standardized pictures of female models posing angry, happy, and neutral facial expressions were examined. Four ERP waveform components were derived: early negative (N150), early positive (P260), negative central (Nc), and positive slow wave (PSW). Differences in these waveforms between a group of 35 maltreated and 24 nonmaltreated children were reported. The groups did not differ on the early perceptual negative component (N150), whereas the maltreated children had greater P260 amplitude at frontal leads compared to the nonmaltreated children in response to viewing angry facial expressions. For the Nc component, the nonmaltreated comparison children exhibited greater amplitude while viewing pictures of happy faces compared to angry and neutral faces, whereas the maltreated children showed greater Nc amplitude at central sites while viewing angry faces. For the PSW, the nonmaltreated group showed a greater area score in the right hemisphere in response to viewing angry facial expressions compared to the maltreated group. The results are discussed in terms of brain development and function, as well as their implications for the design and evaluation of preventive interventions.     

Insula reactivity and connectivity to anterior cingulate cortex when processing threat in generalized social anxiety disorder

Aberrant subcortical-prefrontal connectivity may contribute to insula hyper-reactivity to threat in generalized social anxiety disorder (gSAD). A novel PsychoPhysiological Interaction (PPI) analysis was used to examine functional ‘coupling’ between the insula and prefrontal cortex in gSAD patients and healthy controls (HCs). During fMRI, 29 gSAD and 26 HC volunteers performed an Emotional Face Matching Task, involving the processing of fear, angry, and happy expressions. As expected, compared with HCs, gSAD patients exhibited greater bilateral anterior insula (aINS) reactivity for fear vs. happy faces; this group difference was less robust for angry vs. happy faces. PPI of insula connectivity when processing fearful faces revealed the gSAD group had less right aINS-dorsal anterior cingulate coupling compared to HCs. Findings indicate that aINS hyper-reactivity for fear faces in gSAD, compared to controls, involves reduced connectivity with a prefrontal region implicated in cognitive control and emotion regulation.     

Anxiety and orienting of gaze to angry and fearful faces

Neuroscience research indicates that individual differences in anxiety may be attributable to a neural system for threat-processing, involving the amygdala, which modulates attentional vigilance, and which is more sensitive to fearful than angry faces. Complementary cognitive studies indicate that high-anxious individuals show enhanced visuospatial orienting towards angry faces, but it is unclear whether fearful faces elicit a similar attentional bias. This study compared biases in initial orienting of gaze to fearful and angry faces, which varied in emotional intensity, in high- and low-anxious individuals. Gaze was monitored whilst participants viewed a series of face-pairs. Results showed that fearful and angry faces elicited similar attentional biases. High-anxious individuals were more likely to direct gaze at intense negative facial expressions, than low-anxious individuals, whereas the groups did not differ in orienting to mild negative expressions. Implications of the findings for research into the neural and cognitive bases of emotion processing are discussed.     

Signatures of emotional face processing measured by event-related potentials in 7-month-old infants

The ability to distinguish facial emotions emerges in infancy. Although this ability has been shown to emerge between 5 and 7 months of age, the literature is less clear regarding the extent to which neural correlates of perception and attention play a role in processing of specific emotions. This study's main goal was to examine this question among infants. To this end, we presented angry, fearful, and happy faces to 7-month-old infants (N = 107, 51% female) while recording event-related brain potentials. The perceptual N290 component showed a heightened response for fearful and happy relative to angry faces. Attentional processing, indexed by the P400, showed some evidence of a heightened response for fearful relative to happy and angry faces. We did not observe robust differences by emotion in the negative central (Nc) component, although trends were consistent with previous work suggesting a heightened response to negatively valenced expressions. Results suggest that perceptual (N290) and attentional (P400) processing is sensitive to emotions in faces, but these processes do not provide evidence for a fear-specific bias across components.     

Nonlinear relations between post-traumatic stress symptoms and electrocortical reactivity during emotional face processing in combat-exposed veterans

Combat-related post-traumatic stress symptoms (PTSS) are prevalent among recently deployed veterans, making identification of biomarkers of PTSS in this population a public health priority. Given the link between threat processing neurobiology and PTSS, the threat-related late positive potential (LPP), an ERP reflective of attentional processing sensitive to emotion and its regulation, may have utility as a cost-effective biomarker. Existing PTSS/threat-related LPP findings are mixed, possibly due to variability in PTSS across samples, but this has never been explicitly tested. To address this gap, LPP amplitudes to angry, fearful, and happy emotional face stimuli were recorded among 81 combat-exposed veterans at a VA hospital. A quadratic relationship between self-reported PTSS and LPP amplitude modulation by angry faces emerged such that greater PTSS was related to a decreased LPP response to angry faces among veterans with subthreshold PTSD and an enhanced LPP response to angry faces among veterans with probable PTSD. These results suggest that prior mixed findings may be due to variability in PTSS severity. In addition, exploratory moderation analysis revealed that PTSS was positively associated with late LPP modulation for veterans reporting low cognitive reappraisal use and negatively associated with late LPP modulation for veterans reporting high cognitive reappraisal use. All results were specific to the 1,000–3,000 ms LPP time window. Thus, the functional nature of LPP modulation by direct threat cues may depend upon PTSS severity and/or related variables (e.g., cognitive reappraisal utilization).     

Attentional selectivity for emotional faces: Evidence from human electrophysiology

This study investigated the temporal course of attentional biases for threat-related (angry) and positive (happy) facial expressions. Electrophysiological (event-related potential) and behavioral (reaction time [RT]) data were recorded while participants viewed pairs of faces (e.g., angry face paired with neutral face) shown for 500 ms and followed by a probe. Behavioral results indicated that RTs were faster to probes replacing emotional versus neutral faces, consistent with an attentional bias for emotional information. Electrophysiological results revealed that attentional orienting to threatening faces emerged earlier (early N2pc time window; 180–250 ms) than orienting to positive faces (after 250 ms), and that attention was sustained toward emotional faces during the 250–500-ms time window (late N2pc and SPCN components). These findings are consistent with models of attention and emotion that posit rapid attentional prioritization of threat.