Humans detect angry faces more efficiently than other emotional expressions
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The literature presents mixed findings regarding the efficiency of detecting angry faces compared to other emotional expressions. Some studies report faster motor responses or greater physiological arousal for angry faces, while other evidence indicates that fearful or happy expressions can elicit stronger attentional bias or faster saccadic choices.
Efficiently responding to others’ emotions, especially threatening expressions such as anger and fear, can have great survival value. Previous research has shown that humans have a bias toward threatening stimuli. Most of these studies focused on facial expressions, yet emotions are expressed by the whole body, and not just by the face. Body language contains a direct action component, and activates action preparation areas in the brain more than facial expressions. Hence, biases toward threat may be larger following threatening bodily expressions as compared to facial expressions. The current study investigated reaction times of movements directed toward emotional bodies and faces. For this purpose, a new task was developed where participants were standing in front of a computer screen on which angry, fearful, and neutral faces and bodies were presented which they had to touch as quickly as possible. Results show that participants responded faster to angry than to neutral stimuli, regardless of the source (face or body). No significant difference was observed between fearful and neutral stimuli, demonstrating that the threat bias was not related to the negativity of the stimulus, but likely to the directness of the threat in relation to the observer. Whereas fearful stimuli might signal an environmental threat that requires further exploration before action, angry expressions signal a direct threat to the observer, asking for immediate action. This study provides a novel and implicit method to directly test the speed of actions toward emotions from the whole body.
The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Efficiently responding to others’ emotions, especially threatening expressions such as anger and fear, can have great survival value. Previous research has shown that humans have a bias toward threatening stimuli. Most of these studies focused on facial expressions, yet emotions are expressed by the whole body, and not just by the face.
Body language contains a direct action component, and activates action preparation areas in the brain more than facial expressions. Hence, biases toward threat may be larger following threatening bodily expressions as compared to facial expressions. The current study investigated reaction times of movements directed toward emotional bodies and faces. For this purpose, a new task was developed where participants were standing in front of a computer screen on which angry, fearful, and neutral faces and bodies were presented which they had to touch as quickly as possible. Results show that participants responded faster to angry than to neutral stimuli, regardless of the source (face or body).
For example, fearful and angry as compared to neutral facial expressions induce larger peak amplitudes on early face-related components such as the N170 and VPP (120–220 ms post-stimulus; Williams et al., 2006 ; Hinojosa et al., 2015 ), but also boost later potentials reflecting decision making processes ( Lang et al., 1990 ; Liddell et al., 2004 ). There is an extensive literature on the implicit (i.e., non-conscious) processing of facial expressions.
Moreover, the perception of facial expressions is strongly influenced by body language and the other way around, i.e., the interpretation of a face (body) can change, depending on the emotion expressed by the body ( Meeren et al., 2005 ; Van den Stock et al., 2007 ; Willis et al., 2011 ; Van den Stock and de Gelder, 2012 , 2014 ; Kret et al., 2013a , b ; Martinez et al., 2015 ). Eye-tracking studies have shown that when humans are observing whole-body images of other individuals, they generally spend more time looking at the face than at the posture ( Kret et al., 2013a , b ).
However, when the observed individuals display conflicting messages through the face and the body (for example, a happy face above an angry body), then visual attention immediately allocates toward the threat, whether expressed by the face or by the body ( Kret et al., 2013a , b ). Other studies have shown that recognition of emotional bodies is facilitated (or hindered) by simultaneous presentation of task-irrelevant congruent (or incongruent) emotional facial expressions, respectively ( Willis et al., 2011 ; Gu et al., 2013 ).
Merely looking at fearful faces does not evoke an autonomic response ( Dunsmoor et al., 2009 ) or subjective fear ( Davis and Whalen, 2001 ). Rather, fearful faces are important signals for a potential threat in one’s environment, leading to increased vigilance for the source of danger without concomitant defensive mobilization ( Whalen, 1998 ; Whalen et al., 1998 ). Pichon et al. (2009) directly compared brain activity during the perception of fearful and angry body expressions. They observed that angry body expressions activated the premotor cortex more than fearful expressions.
Significant effects were followed up by Bonferroni-corrected pairwise comparisons. Results A 3 (Emotion: Angry/Fear/Neutral) × 2 (Source: Face/Body) repeated measures ANOVA showed a main effect of emotion F (2,64) = 7.173, p = 0.002, η p 2 = 0.183 1 , 1 – β = 0.922, with faster (log-transformed) reaction times following angry ( M = 2.624, SE = 0.005) as compared to neutral expressions ( M = 2.633, SE = 0.006, p = 0.004), independent from the source [face or body: F (2,64) = 0.225, p = 0.799, η p 2 = 0.007].
Results showed a threat bias for angry faces and bodies, which is in line with previous studies showing that threat cues are prioritized over neutral cues. There was no threat bias for fearful stimuli, suggesting that the directness of the threat in case of anger sped up reaction times, rather than the negativity of a stimulus. Also, no difference was found
Rapid detection and recognition of another individual’s emotional state plays a pivotal role for humans and, most likely, other social species. Proper reactions contribute to an individual’s survival in potentially dangerous situations; this is ensured by a preferential attention towards salient cues. The predisposition to attend to certain categories of affectively salient stimuli– also referred to as affect-biased attention - is likely shared with other species, since fast detection of and appropriate reaction to threats is crucial to survival. We compared human children and one of our close relatives, Sumatran orangutans (Pongo abelii), and predicted that both look more attentively and longer at emotionally salient facial expressions of their own and corresponding other species, compared to neutral faces. However, in contrast to a bias towards emotions providing relevant information by indicating a threat, both species preferentially looked at the fear-related, but not the angry faces of humans and consistently preferred the silent-bared teeth espressions in orangutans. The differential attention towards certain expressions might derive from their social function and the need to detect a potential threat in the environment. Our findings are consistent with claims rooting this affect-biased attention characteristic of human perception in our evolutionary history.
However, in contrast to a bias towards emotions providing relevant information by indicating a threat, both species preferentially looked at the fear-related, but not the angry faces of humans and consistently preferred the silent-bared teeth espressions in orangutans. The differential attention towards certain expressions might derive from their social function and the need to detect a potential threat in the environment. Our findings are consistent with claims rooting this affect-biased attention characteristic of human perception in our evolutionary history.
Since it is difficult to assign specific emotional states to facial expressions of nonhuman primates, we focused on those facial expressions, which are likely to occur in orangutans in similar contexts as in humans (silent-bared teeth display in insecure, potentially fearful situations; bulging lip display in agonistic interactions or in case of high tension; relaxed open mouth face in playful situations; and neutral expression; Study 2). We used two facial expressions of negative emotions with comparable characteristics, i.e. high arousal and threat-related, but which occur in two different contexts.
Figure 1 Visualizations (heat maps) of fixation durations. ( A , B ) Humans ( A ) and orangutans ( B ) fixate human facial expressions (fear vs. anger). While the color red marks those areas that are fixated
For humans, our findings show an attentional bias that is modulated by the affective value of the stimuli, with fearful expressions being fixated most and longest. Like humans, orangutans also fixated fearful faces longer (but not more often) than angry faces (χ 2 = 4.93, df = 1, p = 0.026) and showed a trend to fixate them more frequently than neutral faces (fear vs. neutral: χ 2 = 2.91, df = 1, p = 0.088), but none of the other comparisons revealed significant differences.
Together these results indicate that both species preferentially look at fearful facial expressions compared to angry and neutral faces, but unlike orangutans, humans also fixated angry facial expressions more and longer than happy faces, thus revealing an attentional bias towards affective stimuli expressing negative valence. Our findings for the perception of human facial expressions point to a particular attentional bias for the expression of fear, since humans as well as orangutans responded faster to and looked longer at fearful expressions. Figure 3 Fixation rates at specific pairs of human facial expressions.
Equally, both species looked longer at the silent bared-teeth face but not at the bulging lip face (Study 2). When looking at human facial expressions, human children also preferentially looked at angry faces compared to positive and neutral information. However, angry faces were still fixated for significantly shorter intervals and less often than fearful expressions. Furthermore, both species looked in general less at neutral compared to positive or negative faces.
Together these findings support our assumption that increased attention to emotional faces is an adaptive trait, since it is present in humans and orangutans and it is not limited to looking at emotional facial expressions of their respective own species. The finding that in humans fear is preferentially processed compared to anger can be explained by the fact that each of these two emotions and their corresponding expressions convey different information, which requires different responses and most importantly, is of different relevance for the individual 42 .
Hence, informed consent was obtained for all human subjects in accordance with the Declaration of Helsinki. Stimuli Study 1 - Human facial expressions Stimuli were obtained from the FACES Database, a set of photographs of humans from different age classes performing various facial expressions. Photographs were standardized in size, color and background, and have been extensively rated as regards their emotional content before being published 63 . To create our stimuli, we selected a subset of 14 young Caucasian adults (seven males, seven females) performing happy, fearful, angry, and neutral faces.
We selected pictures of facial expressions that orangutans show in comparable emotional situations as those underlying the human facial expressions: the silent-bared teeth display occurs in contexts of insecurity, submissive/affiliative behavior or fear 39 , 64 ; the bulging lip face is shown in contexts of frustration, similar to the angry facial expression in humans 65 ; the relaxed open mouth face, which occurs in playful interactions 41 ; and a neutral face.
<h4>Introduction</h4>Understanding how emotions are encoded at the neural level remains a central challenge in human neuroscience. Facial expressions are among the most powerful and frequently used stimuli to study emotion processing. Face perception itself is a complex function supported by a core network-including bilateral occipito-fusiform and superior temporal regions-and an extended network involving anterior structures such as the bilateral amygdalae. However, previous findings on how emotional content modulates these networks have been inconsistent.<h4>Methods</h4>To disentangle perceptual and affective components of face emotion processing, we combined high-frequency pupillometry with functional magnetic resonance imaging (fMRI). Pupillary dilation serves as a sensitive index of two distinct processes: perceptual load, reflecting the informational complexity of a face, and arousal, indicating its immediate sensory impact. In our study, 25 participants (13 female) viewed faces expressing anger, fear, happiness, or neutrality as well as luminance-matched houses serving as control stimuli. A one-back task unrelated to emotion masked the true experimental purpose.<h4>Results</h4>Relative to houses, faces elicited stronger pupillary dilations as well as enhanced blood-oxygen-level-dependent (BOLD) activity in bilateral occipital and fusiform cortices as well as in both amygdalae. Among facial expressions, angry faces evoked the largest pupillary dilations, while fearful faces elicited the strongest neural responses within a right-lateralized network centered on the superior temporal sulcus (rSTS). Across all faces>houses (conjunction minimum-statistic inference), pupil size correlated positively with BOLD activity in the right fusiform gyrus (rFFG), left inferior occipital gyrus (lIOG), bilateral calcarine cortex, and bilateral lingual gyrus.<h4>Discussion</h4>These findings indicate that emotional faces impose a higher perceptual load than matched control stimu
Among facial expressions, angry faces evoked the largest pupillary dilations, while fearful faces elicited the strongest neural responses within a right-lateralized network centered on the superior temporal sulcus (rSTS). Across all faces>houses (conjunction minimum-statistic inference), pupil size correlated positively with BOLD activity in the right fusiform gyrus (rFFG), left inferior occipital gyrus (lIOG), bilateral calcarine cortex, and bilateral lingual gyrus. Discussion These findings indicate that emotional faces impose a higher perceptual load than matched control stimuli, engaging a distributed network spanning early visual and attention-related areas.
Across cultures, observers reliably categorize a limited set of basic emotions from facial expressions ( Ekman, 1992 ). Yet it remains an open question whether the human brain performs a similar classification of facial emotions—and which neural regions integrate emotional quality into perceptual and experiential representations. FMRI studies have established that face processing engages a core network, encompassing the bilateral occipital and fusiform gyri as well as the superior temporal cortex, and an extended network, including anterior structures such as the bilateral amygdalae ( Haxby et al., 2000 , 2002 ; Fairhall and Ishai, 2007 ).
We hypothesized that angry faces, as direct threat signals, would evoke greater pupil dilation, reflecting heightened arousal, whereas fearful faces, which indicate environmental alarm, would preferentially engage the right superior temporal sulcus (rSTS)—a region implicated in the integration of social and motion cues. To ensure balanced emotional valence, happy and neutral expressions were included as comparison conditions ( Uljarevic and Hamilton, 2013 ). Luminance-matched house images served as non-social control stimuli.
In addition, all stimuli were already luminance-matched and have been validated in previous work; further SF manipulation would likely have introduced distortions that run counter to the aim of presenting perceptually natural emotional stimuli. Example stimuli are shown in Figure 1 . Experimental Procedure is shown in Figure 2 . Figure 1 Example stimuli. Faces displaying neutral (top left), happy (top middle), angry (top right), and fearful (bottom left) expressions, alongside luminance-matched houses as a control condition (bottom middle). Faces reproduced with permission from Langner et al. (2010) . Five black and white images arranged in a grid.
Faces reproduced with permission from Langner et al. (2010) . A sequential series of grayscale images shows a person’s different facial expressions, from fearful to neutral, then angry, followed by a house, and finally smiling. Time intervals between these images are labeled as twelve seconds, three to seven seconds, and various short times. Below, overlapping images of people with neutral or emotional expressions change quickly, marked by intervals of 0.35 seconds and 0.15 seconds. An icon of a hand clicking is shown at the end.
A sensitivity power analysis conducted in G*Power 3.1 for a within-subjects ANOVA with five measurements, using a sample size of 25, α = 0.05, and 80% power, determined that this design could detect effects of size f ≥ 0.22, which is below our observed effect size. Notably, ranksum test revealed that angry faces elicited a significantly greater increase over time than all other face conditions ( Figure 4 , dark stars).
Redilation was significantly larger for faces than for houses (light stars). Among face conditions, angry faces elicited a significantly greater increase over time compared with the other expressions (dark stars). Line graph showing normalized mean pupil size over time in milliseconds for different emotional expressions: neutral, happy, angry, fearful, and a control condition of houses. Pupil size initially drops then differentiates, with lines for each expression showing distinct trends and error bars.
Hemispheric asymmetry in conditioning to facial emotional expressions. In the present experiment, we report a right hemisphere advantage for autonomic conditioning to facial emotional expressions. Specifically, angry, but not happy, facial expressions showed significantly more resistance to extinction when presented initially to the right as compared to the left hemisphere. Slides of happy and angry faces were used as conditioned stimuli (CS+ and CS-) with shock as the unconditioned stimulus (UCS). Half of the subjects (n = 15) had the angry face as CS+ (and the happy face as CS-), the other half had the happy face as CS+ (and the angry face as CS-). During acquisition, the CSs were presented foveally. During extinction, using the Visual Half-Field (VHF) technique, half of the CS+ and CS- trials were randomly presented in the right visual half-field (initially to the left hemisphere), and half of the trials were presented in the left half-field (initially to the right hemisphere). Stimuli were presented for 210 ms during acquisition, and for 30 ms during extinction. Bilateral skin conductance responses (SCRs) were recorded.
Brain asymmetry and human electrodermal conditioning. Two experiments are reviewed that demonstrate effects of brain laterality on human classical conditioning. Pictures of facial emotional expressions were used as conditioned stimuli (CSs) together with shock as unconditioned stimulus (UCS). Bilateral electrodermal responses were recorded as dependent measures. In the first experiment, one group was conditioned to an angry face, and one group to a happy face. During extinction, the face-CSs were presented to the right hemisphere on half of the trials and to the left hemisphere on the other half of the trials. Results showed that the right hemisphere was superior in showing persisting effects of learning, and especially to the angry CS+. In the second experiment, lateralized presentations of the angry and happy faces were made during acquisition, with foveal presentations during extinction. Once again, the angry face elicited greater skin conductance responses (SCRs) during extinction in the group that had this stimulus presented to the right hemisphere during acquisition. It is concluded that emotional conditioning is differentially regulated by the two hemispheres of the brain.
Previous studies have shown that the human visual system can detect a face and elicit a saccadic eye movement toward it very efficiently compared to other categories of visual stimuli. In the first experiment, we tested the influence of facial expressions on fast face detection using a saccadic choice task. Face-vehicle pairs were simultaneously presented and participants were asked to saccade toward the target (the face or the vehicle). We observed that saccades toward faces were initiated faster, and more often in the correct direction, than saccades toward vehicles, regardless of the facial expressions (happy, fearful, or neutral). We also observed that saccade endpoints on face images were lower when the face was happy and higher when it was neutral. In the second experiment, we explicitly tested the detection of facial expressions. We used a saccadic choice task with emotional-neutral pairs of faces and participants were asked to saccade toward the emotional (happy or fearful) or the neutral face. Participants were faster when they were asked to saccade toward the emotional face. They also made fewer errors, especially when the emotional face was happy. Using computational modeling, we showed that this happy face advantage can, at least partly, be explained by perceptual factors. Also, saccade endpoints were lower when the target was happy than when it was fearful. Overall, we suggest that there is no automatic prioritization of emotional faces, at least for saccades with short latencies, but that salient local face features can automatically attract attention.
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