Differential modulations of reward expectation on implicit facial emotion processing: ERP evidence

Implicit emotional processing refers to the preferential processing of emotional content even if it is task irrelevant. Given that motivation enhances executive control by biasing attentional resources toward target stimuli, here we investigated the effects of reward expectation on implicit facial emotional processing in two experiments using ERPs. A precue signaling additional monetary reward for fast and accurate response for the upcoming trial (incentive condition; relative to a cue indicating no such additional reward, i.e., nonincentive condition) was followed by the presentation of a happy, angry, or neutral face. Participants had to determine the gender of the face in Experiment 1 and decide whether a number superimposed on the face was even or odd in Experiment 2. In both experiments, incentive cues elicited larger P3 and contingent negative variation responses, and the targets following incentive cues elicited more positive‐going ERPs (200–700 ms), compared with the nonincentive condition. Importantly, the N2 responses (200–280 ms) to the target exhibited differential patterns of Reward × Emotion interaction: relative to the nonincentive condition, the N2 amplitude differences between emotional (i.e., happy and/or angry) and neutral faces increased in the incentive condition in Experiment 1, but diminished in Experiment 2. These results indicate that reward expectation can differentially modulate implicit processing of facial expressions, with increased sensitivity to emotions when the processing of whole faces is required, but with reduced sensitivity when the processing of faces is distractive. This study enriches the evidence for interactions between reward‐related executive control and implicit emotional processing.     

Crossmodal transfer of emotion by music

Music is one of the most powerful elicitors of subjective emotion, yet it is not clear whether emotions elicited by music are similar to emotions elicited by visual stimuli. This leads to an open question: can music-elicited emotion be transferred to and/or influence subsequent vision-elicited emotional processing? Here we addressed this question by investigating processing of emotional faces (neutral, happy and sad) primed by short excerpts of musical stimuli (happy and sad). Our behavioural experiment showed a significant effect of musical priming: prior listening to a happy (sad) music enhanced the perceived happiness (sadness) of a face irrespective of facial emotion. Further, this musical priming-induced effect was largest for neutral face. Our electrophysiological experiment showed that such crossmodal priming effects were manifested by event related brain potential components at a very early (within 100 ms post-stimulus) stages of neuronal information processing. Altogether, these results offer new insight into the crossmodal nature of music and its ability to transfer emotion to visual modality.     

Effects of attention and emotion on repetition priming and their modulation by cholinergic enhancement

We examined whether behavioral and neural effects of repeating faces are modulated by independent factors of selective attention, emotion, and cholinergic enhancement, during functional MRI. Face repetition occurred either between task-relevant (spatially attended) or task-irrelevant (unattended) stimuli; faces could be fearful or neutral; subjects received either placebo or physostigmine. Under placebo, a reaction time advantage occurred with repetition (i.e., priming) that did not differ between levels of attention, but was attenuated with emotion. Inferior temporo-occipital cortex demonstrated repetition decreases to both attended and unattended faces, and showed either equivalent or greater repetition decreases with emotional compared with neutral faces. By contrast, repetition decreases were attenuated for emotional relative to neutral faces in lateral orbitofrontal cortex. These results distinguish automatic repetition effects in sensory cortical regions from repetition effects modulated by emotion in orbitofrontal cortex, which parallel behavioral effects. Under physostigmine, unlike placebo, behavioral repetition effects were seen selectively for attended faces only, whereas emotional faces no longer impaired priming. Physostigmine enhanced repetition decreases in inferior occipital cortex selectively for attended faces, and reversed the emotional interaction with repetition in lateral orbitofrontal cortex. Thus we show that cholinergic enhancement both augments a neural signature of priming and modulates the effects of attention and emotion on behavioral and neural consequences of repetition.     

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.     

Modulation of facial reactions to avatar emotional faces by nonconscious competition priming

To investigate whether subliminally priming for competition influences facial reactions to facial emotional displays, 49 participants were either subliminally competition primed or neutrally primed. Thereafter, they viewed computer generated avatar faces with happy, neutral, and sad expressions while Corrugator supercilii and Zygomaticus major reactions were recorded. Results revealed facial mimicry to happy and sad faces in the neutrally primed group but not the competition primed group. Furthermore, subliminal competition priming enhanced Corrugator supercilii activity after an initial relaxation while viewing happy faces. An impression formation task revealed counter empathic effects confirming successful competition priming. Overall, results indicate that nonconscious processes influence a presumably nonconscious behavior.     

Neural and behavioral measures suggest that cognitive and affective functioning interactions mediate risk for psychosis‐proneness symptoms in youth with chromosome 22q11.2 deletion syndrome

Behavioral components of chromosome 22q11.2 deletion syndrome (22q), caused by the most common human microdeletion, include cognitive and adaptive functioning impairments, heightened anxiety, and an elevated risk of schizophrenia. We investigated how interactions between executive function and the largely overlooked factor of emotion regulation might relate to the incidence of symptoms of psychotic thinking in youth with 22q. We measured neural activity with event‐related potentials (ERPs) in variants of an inhibitory function (Go/No‐Go) experimental paradigm that presented affective or non‐affective stimuli. The study replicated inhibition impairments in the 22q group that were amplified in the presence of stimuli with negative, more than positive affective salience. Importantly, the anterior N2 conflict monitoring ERP significantly increased when youth with 22q viewed angry and happy facial expressions, unlike the typically developing participants. This suggests that youth with 22q may require greater conflict monitoring resources when controlling their behavior in response to highly salient social signals. This evidence of both behavioral and neurophysiological differences in affectively influenced inhibitory function suggests that frequently anxious youth with 22q may struggle more with cognitive control in emotionally charged social settings, which could influence their risk of developing symptoms of psychosis.     

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.     

Emotional misattribution: Facial muscle responses partially mediate behavioral responses in the emotion misattribution procedure

There is ongoing debate regarding the degree to which, and the conditions under which, physiological, affect‐related (i.e., embodied) processes contribute to emotion information processing. Whereas most studies focus on clearly visible and intentional processing conditions, the present study targeted this issue by studying the implicit processing of emotional (angry, fearful, joyful, neutral) faces in a masked emotion misattribution procedure. That is, participants had to categorize neutral‐looking faces with regard to the allegedly felt emotion, which were preceded by a very briefly presented emotional expression. In addition to behavioral measures, facial muscle responses were obtained as an index of physiological, affect‐related processes. Linear mixed‐model mediation analyses confirmed that facial muscle responses partially mediated the behavioral responses to the masked primes in the misattribution task.     

P3b reflects maltreated children's reactions to facial displays of emotion

Processing of emotion information by maltreated and control children was assessed with event-related brain potentials (ERPs). Maltreated children, for whom negative facial displays may be especially salient, and demographically comparable peers were tested to increase knowledge of differential processing of emotion information. ERPs were measured while children responded to pictures depicting facial displays of anger, fear, and happiness. Maltreated children showed larger P3b amplitude when angry faces appeared as targets than did control children; the two groups did not differ when targets were either happy or fearful facial expressions or for nontargets of any emotional content. These results indicate that aberrant emotional experiences associated with maltreatment may alter the allocation of attention and sensitivity that children develop to process specific emotion information.     

On the resistance to extinction of fear conditioned to angry faces

The present study investigated whether, like fear conditioned to pictures of snakes and spiders, fear conditioned to angry faces resists extinction even after verbal instruction and removal of the shock electrode. Participants were trained in a differential Pavlovian fear conditioning procedure with angry face or happy face conditional stimuli (CSs). Prior to extinction, half the participants in each group were informed that no more unconditional stimuli would be presented and the shock electrode was removed. In the absence of this manipulation, participants showed resistance to extinction after training with angry face CSs, but not after training with happy face CSs. Instructed extinction and electrode removal abolished fear conditioning regardless of the emotion expressed by the CS faces. This finding suggests that fear conditioned to angry faces, like fear conditioned to racial out-group faces, is more malleable than fear conditioned to snakes and spiders.     

Facial reactions, autonomic activity and experienced emotion: a three component model of emotional conditioning

The present study was designed to evaluate whether aversively conditioned responses to facial stimuli are detectable in all three components of the emotional response system, i.e. the expressive/behavioral, the physiological/autonomic and the cognitive/experienced component of emotion. Two groups of subjects were conditioned to angry or happy facial expression stimuli using a 100 dB noise as UCS in a differential aversive conditioning paradigm. The three components of the emotional response system were measured as: Facial-EMG reactions (corrugator and zygomatic muscle regions); autonomic activity (skin conductance, SCR; SCR half recovery time, T/2; heart rate, HR); and ratings of experienced emotion. It was found that responses in all components of the emotional response system were detectable in the angry group as greater EMG and autonomic resistance to extinction and greater self-reported fear. More specifically the angry group showed a resistant conditioning effect for the facial-EMG corrugator muscle that was accompanied by resistant conditioning for SCR frequency, slower SCR recovery, resistant conditioning in HR and a higher self-reported fear than the happy group. Thus, aversive conditioning to angry facial stimuli induce a uniform negative emotional response pattern as indicated by all three components of the emotional response system. These data suggest that a negative 'affect program' triggers responses in the different emotional components. The results suggest that human subjects are biologically prepared to react with a negative emotion to angry facial stimuli.     

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.     

Enhanced neural reactivity and selective attention to threat in anxiety

Attentional bias towards threat is implicated in the etiology and maintenance of anxiety disorders. We examined the neural correlates of threat bias in anxious and nonanxious participants to shed light on the neural chronometry of this cognitive bias. In this study, event-related potentials (ERPs) were recorded while anxious (n = 23) and nonanxious (n = 23) young adults performed a probe-discrimination task measuring attentional bias towards threat (angry) and positive (happy) face stimuli. Results showed an attention bias towards threat among anxious participants, but not among nonanxious participants. No bias to positive faces was found. ERP data revealed enhanced C1 amplitude (∼80 ms following threat onset) in anxious relative to nonanxious participants when cue displays contained threat faces. Additionally, P2 amplitude to the faces display was higher in the anxious relative to the nonanxious group regardless of emotion condition (angry/happy/neutral). None of the ERP analyses associated with target processing were significant. In conclusion, our data suggest that a core feature of threat processing in anxiety lies in functional perturbations of a brain circuitry that reacts rapidly and vigorously to threat. It is this over-activation that may set the stage for the attention bias towards threat observed in anxious individuals.     

Current status of the anger superiority hypothesis: A meta‐analytic review of N2pc studies

Numerous investigators have tested contentions that angry faces capture early attention more completely than happy faces do in the context of other faces. However, syntheses of studies on early event‐related potentials related to the anger superiority hypothesis have yet to be conducted, particularly in relation to the N200 posterior‐contralateral (N2pc) component which provides a reliable electrophysiological index related to orienting of attention suitable for testing this hypothesis. Fifteen samples (N = 534) from 13 studies featuring the assessment of N2pc amplitudes during exposure to angry‐neutral and/or happy‐neutral facial expression arrays were included for meta‐analysis. Moderating effects of study design features and sample characteristics on effect size variability were also assessed. N2pc amplitudes elicited by affectively valenced expressions (angry and happy) were significantly more pronounced than those elicited by neutral expressions. However, the mean effect size difference between angry and happy expressions was ns. N2pc effect sizes were moderated by sample age, number of trials, and nature of facial images used (schematic vs. real) with larger effect sizes observed when samples were comparatively younger, more task trials were presented and schematic face arrays were used. N2pc results did not support anger superiority hypothesis. Instead, attentional resources allocated to angry versus happy facial expressions were similar in early stages of processing. As such, possible adaptive advantages of biases in orienting toward both anger and happy expressions warrant consideration in revisions of related theory.     

Schizophrenia patients' perceptual biases in response to positively and negatively valenced emotion chimeras

BACKGROUND: In a prior study, we observed that schizophrenia patients display atypical perceptual biases in response to emotional (happy/neutral) facial chimeras. METHODS: The present study was an attempt to replicate and extend those findings, using emotional stimuli with negative affective valence (angry/neutral chimeras) as well as positive valence, and including more than one type of non-affective facial comparison task. We compared schizophrenia patients (N = 37) and controls (N = 48) on free-vision tasks that typically yield left spatial field biases indicative of right hemisphere activation. There were six chimera tasks, including two emotion (happy, angry) chimeras, two non-emotion (gender, age) chimeras and two non-face (dots, gradients) chimeras. RESULTS: We observed a Group x Task interaction, with schizophrenia patients displaying significantly less of the expected left spatial perceptual bias in response to the happy/neutral chimeras and the angry/neutral chimeras relative to the controls. In contrast, the patients and controls did not differ in terms of their response to the Gender, Age, Dots, or Gradients tasks. CONCLUSIONS: These findings are consistent with the assertion that, compared with healthy controls individuals with schizophrenia perceive emotion differently.     

Attention bias to faces in Asperger Syndrome: a pictorial emotion Stroop study

BACKGROUND: Emotional Stroop tasks have shown attention biases of clinical populations towards stimuli related to their condition. Asperger Syndrome (AS) is a neuropsychiatric condition with social and communication deficits, repetitive behaviours and narrow interests. Social deficits are particularly striking, including difficulties in understanding others. METHOD: We investigated colour-naming latencies of adults with and without AS to name colours of pictures containing angry facial expressions, neutral expressions or non-social objects. We tested three hypotheses: whether (1) controls show longer colour-naming latencies for angry versus neutral facial expressions with male actors, (2) people with AS show differential latencies across picture types, and (3) differential response latencies persist when photographs contain females. RESULTS: Controls had longer latencies to pictures of male faces with angry compared to neutral expressions. The AS group did not show longer latencies to angry versus neutral expressions in male faces, instead showing slower latencies to pictures containing any facial expression compared to objects. When pictures contained females, controls no longer showed longer latencies for angry versus neutral expressions. However, the AS group still showed longer latencies to all facial picture types, compared to objects, providing further evidence that faces produce interference effects for this clinical group. CONCLUSIONS: The pictorial emotional Stroop paradigm reveals normal attention biases towards threatening emotional faces. The AS group showed Stroop interference effects to all facial stimuli regardless of expression or sex, suggesting that faces cause disproportionate interference in AS.     

Selective attention to threatening faces in delusion‐prone individuals

Introduction. Selective attention to threat‐related information has been associated with clinical delusions in schizophrenia and nonclinical delusional ideation in healthy individuals. However, it is unclear whether biased attention for threat reflects early engagement effects on selective attention, or later difficulties in disengaging attention from perceived threat. The present study examined which of these processes operate in nonclinical delusion‐prone individuals.

Methods. A total of 100 psychologically healthy participants completed the Peters et al. () Delusions Inventory (PDI). Twenty‐two scoring in the upper quartile (high‐PDI group) and 22 scoring in the lower quartile (low‐PDI group) completed a modified dot‐probe task. Participants detected dot‐probes appearing 200, 500, or 1250 ms after an angry‐neutral face pair or a happy‐neutral face pair.

Results. High‐PDI individuals responded faster to dot‐probes presented in the same location as angry compared to happy faces at the short 200 ms stimulus onset asynchrony (SOA), but only when the emotional faces were presented to the left visual field. At the two longer SOAs (500 ms, 1250 ms), the high‐PDI group were also faster to respond to dot‐probes presented in the same location as angry compared to happy faces and slower to respond to dot‐probes presented in different spatial locations to angry (vs. happy) faces. The latter effects were seen whether emotional faces were presented to the left or the right visual field.

Conclusions. Results support the operation of emotion‐selective engagement and defective disengagement for threat‐related facial expressions (i.e., anger) in delusion‐prone individuals.     

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.     

Emotion regulation of the affect‐modulated startle reflex during different picture categories

Previous studies on emotion regulation of the startle reflex found an increase in startle amplitude from down‐, to non‐, to up‐regulation for pleasant and unpleasant stimuli. We wanted to clarify whether this regulation effect remains stable for different picture categories within pleasant and unpleasant picture sets. We assessed startle amplitude of 31 participants during down‐, non‐, or up‐regulation of feelings elicited by pleasant erotic and adventure and unpleasant victim and threat pictures. Startle amplitude was smaller during adventure and erotic compared to victim and threat pictures and increased from down‐, to non‐, to up‐regulation independently of the picture category. Results indicate that the motivational priming effect on startle modulation elicited by different picture categories is independent of emotion regulation instructions. In addition, the emotion regulation effect is independent of motivational priming effects.     

Event-related delta and theta synchronization during explicit and implicit emotion processing

Emotion information processing may occur in two modes which are differently represented in conscious awareness. Fast online processing involves coarse-grained analysis of salient features, and is not represented in conscious awareness; offline processing takes hundreds of milliseconds to generate fine-grained analysis, and is represented in conscious awareness. These processing modes may be studied using event-related electroencephalogram theta and delta synchronization as a marker of emotion processing. Two experiments were conducted, which differed on the mode of emotional information presentation. In the explicit mode subjects were explicitly instructed to evaluate the emotional content of presented stimuli; in the implicit mode they performed a gender discrimination task. Firstly, we show that in both experiments theta and delta synchronization is stronger upon presentation of “emotional” than “neutral” stimuli, and in subjects who are more sensitive, or experience higher emotional involvement than in less sensitive or detached subjects. Secondly, we show that in the implicit mode theta and delta synchronization is more pronounced in an early (before 250 ms post-stimulus) processing stage, whereas in the explicit mode it is more pronounced in a later processing stage. Source localization analysis showed that implicit processing of angry and happy (relative to neutral) faces is associated with higher early (before 250 ms) theta synchronization in the right parietal cortex and the right insula, respectively. Explicit processing of angry and happy faces is associated with higher late (after 250 ms) theta synchronization in the left temporal lobe and bilateral prefrontal cortex, respectively.