I focus only when I see your fear-fearful faces are not prioritized by attention when processed outside of awareness.

The defensive reaction to threats consists of two components: non-specific physiological arousal and specific attentional prioritization of the threatening stimulus, both of which are assumed by the so-called "low-road" hypothesis to be induced automatically and unconsciously. Although ample evidence indicates that non-specific arousal can indeed be caused by unconscious threatening stimuli, data regarding the involvement of the attentional selection mechanism remain inconclusive. Therefore, in the present study we used ERPs to compare the potential engagement of attention in the perception of subliminal and supraliminal fearful facial expressions to that of neutral ones. In the conscious condition, fearful faces were preferentially encoded (as indicated by the N170 component) and prioritized by bottom-up (EPN) and spatial attention (N2pc) in an automatic, task-independent manner. Furthermore, consciously perceived fearful expressions engaged cognitive resources (SPCN, P3) when face stimuli were task-relevant. In the unconscious condition, fearful faces were still preferentially encoded (N170), but we found no evidence for any type of attentional prioritization. Therefore, by showing that threatening stimuli engage attention only when perceived consciously, our findings challenge the "low road" hypothesis and point to the limits of unconscious attentional selection.

Neural processing of lateralised task-irrelevant fearful faces under different awareness conditions.

The neural fate of task-irrelevant emotional faces under different awareness conditions is poorly understood. Here, we examined the electrophysiological activity during an experiment where the location of target information (contrast-induced line) was manipulated orthogonally to the location of task-irrelevant fearful faces, under subliminal or supraliminal viewing conditions. We found that only target lines elicited an N2-posterior-contralateral (N2pc), indexing spatial attention shifting, in the supraliminal condition. No N2pc was found for the targets in the subliminal condition or for task-irrelevant fearful faces in either conditions. However, the mere presence of a fearful face enhanced early neural activity between 200 and 300 ms only in the subliminal condition. Additionally, the presence of a target line, but not a fearful face, enhanced the P3. Our results suggest that the N2pc is dependent on visual awareness and task-relevancy of the information and that laterally-presented task-irrelevant fearful expressions can be processed without awareness during early visual processing.

A randomized trial shows dose-frequency and genotype may determine the therapeutic efficacy of intranasal oxytocin.

BACKGROUND: The neuropeptide oxytocin is proposed as a promising therapy for social dysfunction by modulating amygdala-mediated social-emotional behavior. Although clinical trials report some benefits of chronic treatment, it is unclear whether efficacy may be influenced by dose frequency or genotype. METHODS: In a randomized, double-blind, placebo-controlled pharmaco-functional magnetic resonance imaging trial (150 male subjects), we investigated acute and different chronic (every day or on alternate days for 5 days) intranasal oxytocin (24 international units) effects and oxytocin receptor genotype-mediated treatment sensitivity on amygdala responses to face emotions. We also investigated similar effects on resting-state functional connectivity between the amygdala and prefrontal cortex. RESULTS: A single dose of oxytocin-reduced amygdala responses to all face emotions but for threatening (fear and anger) and happy faces, this effect was abolished after daily doses for 5 days but maintained by doses given every other day. The latter dose regime also enhanced associated anxious-arousal attenuation for fear faces. Oxytocin effects on reducing amygdala responses to face emotions only occurred in AA homozygotes of rs53576 and A carriers of rs2254298. The effects of oxytocin on resting-state functional connectivity were not influenced by either dose-frequency or receptor genotype. CONCLUSIONS: Infrequent chronic oxytocin administration may be therapeutically most efficient and its anxiolytic neural and behavioral actions are highly genotype-dependent in males.

The spatial effect of fearful faces in the autonomic response.

Peripersonal space (PPS) corresponds to the space around the body and it is defined by the location in space where multimodal inputs from bodily and external stimuli are integrated. Its extent varies according to the characteristics of external stimuli, e.g., the salience of an emotional facial expression. In the present study, we investigated the psycho-physiological correlates of the extension phenomenon. Specifically, we investigated whether an approaching human face showing either an emotionally negative (fearful) or positive (joyful) facial expression would differentially modulate PPS representation, compared to the same face with a neutral expression. To this aim, we continuously recorded the skin conductance response (SCR) of 27 healthy participants while they watched approaching 3D avatar faces showing fearful, joyful or neutral expressions, and then pressed a button to respond to tactile stimuli delivered on their cheeks at three possible delays (visuo-tactile trials). The results revealed that the SCR to fearful faces, but not joyful or neutral faces, was modulated by the apparent distance from the participant's body. SCR increased from very far space to far and then to near space. We propose that the proximity of the fearful face provided a cue to the presence of a threat in the environment and elicited a robust and urgent organization of defensive responses. In contrast, there would be no need to organize defensive responses to joyful or neutral faces and, as a consequence, no SCR differences were found across spatial positions. These results confirm the defensive function of PPS.

Attentional allocation to task-irrelevant fearful faces is not automatic: experimental evidence for the conditional hypothesis of emotional selection.

A growing body of research indicates that attentional biases toward emotional stimuli are not automatic, but may depend on the relevance of emotion to the top-down search goals of the observer. To determine whether and how this relevance factor modulates attentional allocation to irrelevant fearful faces, four spatial cueing tasks were designed, in which the goal-relevance of completely task-irrelevant (neutral or fearful) cue faces was systematically manipulated by changing the target defining feature. No attentional capture by cue faces (be they neutral or fearful) was observed when the cue faces were completely goal-irrelevant. When faces - but not facial expressions - were goal-relevant, fearful cue faces captured attention, but so did neutral cue faces to a similar extent. Only when facial expressions were explicitly goal-relevant did we observe a difference between attentional allocation to fearful and neutral cue faces, with larger cueing effects for neutral cue faces in the Neutral task, and for fearful cue faces in the Fearful task. Therefore, rather than automatic, attentional allocation to irrelevant fearful faces proved conditional to the explicit relevance of fearful expressions to top-down search goals.

Fear leads to a deficit of prepulse inhibition of blink reflex in healthy humans.

OBJECTIVE: We aimed to analyze whether or not fear conditioning exerts an effect on prepulse inhibition (PPI) of blink reflex (BR). To create fear conditioning, we used fearful faces. Since fearful faces lead to a specific set of fear conditioning, we hypothesized PPI of BR would change under the observation of fearful faces. METHOD: We included 17 healthy subjects with a mean age of 30.8 ± 6.9 years and seven healthy subjects with a mean age of 57.7 ± 7.3 years between January 2018 and June 2018 and recorded PPI of BR. The recordings were done before observation of any image, during observation of images, and immediately after observation of images. Observation of images included observation of fearful faces for 30 s and a neutral image of a white screen for 30 s (in a randomized order). RESULTS: There was a R2-PPI deficit during observation of fearful faces in each group whereas R2-PPI fully developed at other time points. R1 amplitude and R2 magnitude were lower during observation of any image compared with baseline and post-observation time points. CONCLUSION: In conclusion, a deficit of R2-PPI develops during observation of fearful faces in humans which is probably related to activation of the amygdala.

Attentional avoidance of fearful facial expressions following early life stress is associated with impaired social functioning.

BACKGROUND: Early life stress is associated with poorer social functioning. Attentional biases in response to threat-related cues, linked to both early experience and psychopathology, may explain this association. To date, however, no study has examined attentional biases to fearful facial expressions as a function of early life stress or examined these biases as a potential mediator of the relation between early life stress and social problems. METHODS: In a sample of 154 children (ages 9-13 years) we examined the associations among interpersonal early life stressors (i.e., birth through age 6 years), attentional biases to emotional facial expressions using a dot-probe task, and social functioning on the Child Behavior Checklist. RESULTS: High levels of early life stress were associated with both greater levels of social problems and an attentional bias away from fearful facial expressions, even after accounting for stressors occurring in later childhood. No biases were found for happy or sad facial expressions as a function of early life stress. Finally, attentional biases to fearful faces mediated the association between early life stress and social problems. CONCLUSIONS: Attentional avoidance of fearful facial expressions, evidenced by a bias away from these stimuli, may be a developmental response to early adversity and link the experience of early life stress to poorer social functioning.

"Blindsight" and subjective awareness of fearful faces: Inversion reverses the deficits in fear perception associated with core psychopathic traits.

Though emotional faces preferentially reach awareness, the present study utilised both objective and subjective indices of awareness to determine whether they enhance subjective awareness and "blindsight". Under continuous flash suppression, participants localised a disgusted, fearful or neutral face (objective index), and rated their confidence (subjective index). Psychopathic traits were also measured to investigate their influence on emotion perception. As predicted, fear increased localisation accuracy, subjective awareness and "blindsight" of upright faces. Coldhearted traits were inversely related to subjective awareness, but not "blindsight", of upright fearful faces. In a follow-up experiment using inverted faces, increased localisation accuracy and awareness, but not "blindsight", were observed for fear. Surprisingly, awareness of inverted fearful faces was positively correlated with coldheartedness. These results suggest that emotion enhances both pre-conscious processing and the qualitative experience of awareness, but that pre-conscious and conscious processing of emotional faces rely on at least partially dissociable cognitive mechanisms.

Emotion perception and executive control interact in the salience network during emotionally charged working memory processing.

Processing of emotional stimuli can either hinder or facilitate ongoing working memory (WM); however, the neural basis of these effects remains largely unknown. Here we examined the neural mechanisms of these paradoxical effects by implementing a novel emotional WM task in an fMRI study. Twenty-five young healthy participants performed an N-back task with fearful and neutral faces as stimuli. Participants made more errors when performing 0-back task with fearful versus neutral faces, whereas they made fewer errors when performing 2-back task with fearful versus neutral faces. These emotional impairment and enhancement on behavioral performance paralleled significant interactions in distributed regions in the salience network including anterior insula (AI) and dorsal cingulate cortex (dACC), as well as in emotion perception network including amygdala and temporal-occipital association cortex (TOC). The dorsal AI (dAI) and dACC were more activated when comparing fearful with neutral faces in 0-back task. Contrarily, dAI showed reduced activation, while TOC and amygdala showed stronger responses to fearful as compared to neutral faces in the 2-back task. These findings provide direct neural evidence to the emerging dual competition model suggesting that the salience network plays a critical role in mediating interaction between emotion perception and executive control when facing ever-changing behavioral demands.

Rapid fear detection relies on high spatial frequencies.

Signals of threat--such as fearful faces--are processed with priority and have privileged access to awareness. This fear advantage is commonly believed to engage a specialized subcortical pathway to the amygdala that bypasses visual cortex and processes predominantly low-spatial-frequency information but is largely insensitive to high spatial frequencies. We tested visual detection of low- and high-pass-filtered fearful and neutral faces under continuous flash suppression and sandwich masking, and we found consistently that the fear advantage was specific to high spatial frequencies. This demonstrates that rapid fear detection relies not on low- but on high-spatial-frequency information--indicative of an involvement of cortical visual areas. These findings challenge the traditional notion that a subcortical pathway to the amygdala is essential for the initial processing of fear signals and support the emerging view that the cerebral cortex is crucial for the processing of ecologically relevant signals.

Disrupted limbic-prefrontal effective connectivity in response to fearful faces in lifetime depression.

BACKGROUND: Multiple brain imaging studies of negative emotional bias in major depressive disorder (MDD) have used images of fearful facial expressions and focused on the amygdala and the prefrontal cortex. The results have, however, been inconsistent, potentially due to small sample sizes (typically N<50). It remains unclear if any alterations are a characteristic of current depression or of past experience of depression, and whether there are MDD-related changes in effective connectivity between the two brain regions. METHODS: Activations and effective connectivity between the amygdala and dorsolateral prefrontal cortex (DLPFC) in response to fearful face stimuli were studied in a large population-based sample from Generation Scotland. Participants either had no history of MDD (N=664 in activation analyses, N=474 in connectivity analyses) or had a diagnosis of MDD during their lifetime (LMDD, N=290 in activation analyses, N=214 in connectivity analyses). The within-scanner task involved implicit facial emotion processing of neutral and fearful faces. RESULTS: Compared to controls, LMDD was associated with increased activations in left amygdala (PFWE=0.031,kE=4) and left DLPFC (PFWE=0.002,kE=33), increased mean bilateral amygdala activation (ß=0.0715,P=0.0314), and increased inhibition from left amygdala to left DLPFC, all in response to fearful faces contrasted to baseline. Results did not appear to be attributable to depressive illness severity or antidepressant medication status at scan time. LIMITATIONS: Most studied participants had past rather than current depression, average severity of ongoing depression symptoms was low, and a substantial proportion of participants were receiving medication. The study was not longitudinal and the participants were only assessed a single time. CONCLUSIONS: LMDD is associated with hyperactivity of the amygdala and DLPFC, and with stronger amygdala to DLPFC inhibitory connectivity, all in response to fearful faces, unrelated to depression severity at scan time. These results help reduce inconsistency in past literature and suggest disruption of 'bottom-up' limbic-prefrontal effective connectivity in depression.

Faces capture spatial attention only when we want them to: An inattentional blindness EEG study.

Previous research on emotional face processing has shown that emotional faces such as fearful faces may be processed without visual awareness. However, evidence for nonconscious attention capture by fearful faces is limited. In fact, studies using sensory manipulation of awareness (e.g., backward masking paradigms) have shown that fearful faces do not attract attention during subliminal viewings nor when they were task-irrelevant. Here, we used a three-phase inattentional blindness paradigm and electroencephalography to examine whether faces (fearful and neutral) capture attention under different conditions of awareness and task-relevancy. We found that the electrophysiological marker for attention capture, the N2-posterior-contralateral (N2pc), was elicited by face stimuli only when participants were aware of the faces and when they were task-relevant (phase 3). When participants were unaware of the presence of faces (phase 1) or when the faces were irrelevant to the task (phase 2), no N2pc was observed. Together with our previous work, we concluded that fearful faces, or faces in general, do not attract attention unless we want them to.

Decoding neural patterns for the processing of fearful faces under different visual awareness conditions: A multivariate pattern analysis.

Previous studies have provided mixed findings regarding the nonconscious processing of fearful faces. Here, we used multivariate pattern analysis on electroencephalography data from three backward masking experiments to examine the processing of fearful faces under different visual awareness conditions. Three groups of participants were shown pairs of face images presented very briefly (for 16 ms) or for sufficiently long (for 266 ms), and completed tasks where the faces were either relevant to the experimental task (Experiment 1) or not (Experiments 2 and 3). Three main decoding analyses were performed. First, in the visual awareness decoding, the visibility of the faces, and hence participants' awareness of them, was maximally decodable in three time windows: 158-168 ms, 235-260 ms and 400-600 ms where the earlier neural patterns were generalized to the later stage activity. Second, we found that the spatial location of a fearful face in the face pairs was decodable, however only when the faces were consciously seen and task-relevant. Finally, we successfully decoded distinct neural patterns associated with the fearful-face-present conditions, compared to the fearful-face-absent conditions, and these patterns were decodable during both short and long presentations of the faces. Together, our results suggest that, while the processing of the spatial location of fearful faces requires awareness and task-relevancy, the mere presence of fearful faces can be processed even when visual awareness is highly restricted.

Differential modulation on neural activity related to flankers during face processing: A visual crowding study.

In this visual crowding study, we manipulated the perceivability of a central crowded face (a fearful or a neutral face) by varying the similarity between the central face and the surrounding flanker stimuli. We presented participants with pairs of visual clutters and recorded their electroencephalography during an emotion judgement task. In an upright flanker condition where both the central target face and flanker faces were upright faces, participants were less likely to report seeing the target face, and their P300 was weakened, compared to a scrambled flanker condition where scrambled face images were used as flankers. Additionally, at âˆ¼ 120 ms post-stimulus, a posterior negativity was found for the upright compared to scrambled flanker condition, however only for fearful face targets. We concluded that early neural responses seem to be affected by the perceptual characteristics of both target and flanker stimuli whereas later-stage neural activity is associated with post-perceptual evaluation of the stimuli in this visual crowding paradigm.

Erratum: Attentional capture by fearful faces requires consciousness and is modulated by task-relevancy: a dot-probe EEG study.

[This corrects the article DOI: 10.3389/fnins.2023.1152220.].

Attentional capture by fearful faces requires consciousness and is modulated by task-relevancy: A dot-probe EEG study.

In the current EEG study, we used a dot-probe task in conjunction with backward masking to examine the neural activity underlying awareness and spatial processing of fearful faces and the neural processes for subsequent cued spatial targets. We presented face images under different viewing conditions (subliminal and supraliminal) and manipulated the relation between a fearful face in the pair and a subsequent target. Our mass univariate analysis showed that fearful faces elicit the N2-posterior-contralateral, indexing spatial attention capture, only when they are presented supraliminally. Consistent with this, the multivariate pattern analysis revealed a successful decoding of the location of the fearful face only in the supraliminal viewing condition. Additionally, the spatial attention capture by fearful faces modulated the processing of subsequent lateralised targets that were spatially congruent with the fearful face, in both al and electrophysiological data. There was no evidence for nonconscious processing of the fearful faces in the current paradigm. We conclude that spatial attentional capture by fearful faces requires visual awareness and it is modulated by top-down task demands.

Testing stimulus exposure time as the critical factor of increased EPN and LPP amplitudes for fearful faces during perceptual distraction tasks.

Fearful facial expressions are prioritized across different information processing stages, as evident in early, intermediate, and late components of event-related brain potentials (ERPs). Recent studies showed that, in contrast to early N170 modulations, mid-latency (Early Posterior Negativity, EPN) and late (Late Positive Potential, LPP) emotional modulations depend on the attended perceptual feature. Nevertheless, several studies reported significant differences between emotional and neutral faces for the EPN or LPP components during distraction tasks. One cause for these conflicting findings might be that when faces are presented sufficiently long, participants attend to task-irrelevant features of the faces. In this registered report, we tested whether the presentation duration of faces is the critical factor for differences between reported emotional modulations during perceptual distraction tasks. To this end, 48 participants were required to discriminate the orientation of lines overlaid onto fearful or neutral faces, while face presentation varied (100 msec, 300 msec, 1,000 msec, 2,000 msec). While participants did not need to pay attention to the faces, we observed main effects of emotion for the EPN and LPP, but no interaction between emotion and presentation duration. Of note, unregistered exploratory tests per presentation duration showed no significant EPN and LPP emotion differences during short durations (100 and 300 msec) but significant differences with longer durations. While the presentation duration seems not to be a critical factor for EPN and LPP emotion effects, future studies are needed to investigate the role of threshold effects and the applied analytic designs to explain conflicting findings in the literature.

Does a look of fear prompt to act? The effects of gaze and face emotional expression on manipulable objects.

Gaze direction is an important social cue for understanding the intentions of other people. Indeed, interacting with others requires the ability to encode their current focus of attention in order to predict their future actions. Previous studies have showed that when asked to detect or identify a target, people are faster if shown a gaze oriented toward rather than away from that target. Most importantly, there is evidence that the emotion conveyed by the face with the averted gaze matters. We further tested the interplay between gaze and face emotion in the context of manipulable objects to understand whether and to what extent other people's gaze influences our own actions toward objects. Participants judged whether a target graspable object was upright or inverted after viewing a face cue with a central or averted gaze. Importantly, the target's handle could be oriented toward the gazed-at location or the opposite side such that gaze and handle were corresponding or non-corresponding in space. Furthermore, we manipulated the expression of the cue by using neutral and fearful faces. Results showed a handle-response (H-R) compatibility effect (i.e., a facilitation when the response key is on the same side as the object's handle) only with fearful cues with a central gaze.

The role of phase and orientation for ERP modulations of spectrum-manipulated fearful and neutral faces.

Prioritized processing of fearful compared to neutral faces has been proposed to result from evolutionary adaptation of the contrast sensitivity function (CSF) to the features of emotionally relevant faces and/or vice versa. However, it is unknown whether a stimulus merely has to feature the amplitude spectrum of a fearful face to be prioritized or whether the relevant spatial frequencies have to occur with specific phases and orientations. Prioritized processing is indexed by specific increases of Event-Related Potentials (ERPs) of the EEG and occurs throughout different early processing stages, indexed by emotion-related modulations of the P1, N170, and EPN. In this pre-registered study, we manipulated phase and amplitude properties of the Fourier spectra of neutral and fearful faces to test the effect of phase coherence (PC, face vs. scramble) and orientation coherence (OC, original vs. rotational average) and their interactions with differential emotion processing. We found that differential emotion processing was not present at the level of P1 but strongly affected N170 and EPN. In both cases, intact phase coherence was required for enhanced processing of fearful faces. OC did not interact with emotion. While faces produced the typical N170 effect, we observed a reversed effect for scrambles. Additional exploratory independent component analysis (ICA) suggests that this reversal could signal a mismatch between an early "perceptual hypothesis" and feedback of configural information. In line with our expectations, fearful-neutral differences for the N170 and EPN depend on configural information, i.e., recognizable faces.

Enhanced contralateral theta oscillations and N170 amplitudes in occipitotemporal scalp regions underlie attentional bias to fearful faces.

Attending toward fearful faces and other threatening stimuli increase the chance of survival. The dot-probe task is a commonly used measure of spatial attention. Event-related potentials (ERPs) have been found to be a reliable measure of attentional bias. The dot-probe literature suggests that posterior contralateral N170 amplitudes are more enhanced by fearful faces compared to ipsilateral amplitudes. However, ERP methods remove non-phase locked frequencies, which provides additional information about neural activity. Specifically, theta oscillations (5-7 Hz) have been linked to attentional processing. The purpose of this study was to examine the relationship between posterior contralateral theta oscillations and N170 amplitudes in the dot-probe task. A modified dot-probe task was used with fear and neutral facial expressions and EEG data was recorded from 33 electrodes. The ERP and time-frequency data were extracted from the P7 and P8 electrodes (left and right occipitotemporal regions). This study found enhanced N170 amplitude and theta oscillations in the electrodes posterior contralateral to the fearful face. Contralateral N170 amplitudes and theta oscillations were related such that greater N170 amplitudes were associated with greater theta oscillations. The results indicated that increased contralateral N170 and theta oscillations are related to each other and underlie attentional bias to fearful faces.