Pinpointing the optimal spatial frequency range for automatic neural facial fear processing.

Faces convey an assortment of emotional information via low and high spatial frequencies (LSFs and HSFs). However, there is no consensus on the role of particular spatial frequency (SF) information during facial fear processing. Comparison across studies is hampered by the high variability in cut-off values for demarcating the SF spectrum and by differences in task demands. We investigated which SF information is minimally required to rapidly detect briefly presented fearful faces in an implicit and automatic manner, by sweeping through an entire SF range without constraints of predefined cut-offs for LSFs and HSFs. We combined fast periodic visual stimulation with electroencephalography. We presented neutral faces at 6 â€‹Hz, periodically interleaved every 5th image with a fearful face, allowing us to quantify an objective neural index of fear discrimination at exactly 1.2 â€‹Hz. We started from a stimulus containing either only very low or very high SFs and gradually increased the SF content by adding higher or lower SF information, respectively, to reach the full SF spectrum over the course of 70 â€‹s. We found that faces require at least SF information higher than 5.93 cycles per image (cpi) to implicitly differentiate fearful from neutral faces. However, exclusive HSF faces, even in a restricted SF range between 94.82 and 189.63 cpi already carry the critical information to extract the emotional expression of the faces.

EEG frequency-tagging demonstrates increased left hemispheric involvement and crossmodal plasticity for face processing in congenitally deaf signers.

In humans, face-processing relies on a network of brain regions predominantly in the right occipito-temporal cortex. We tested congenitally deaf (CD) signers and matched hearing controls (HC) to investigate the experience dependence of the cortical organization of face processing. Specifically, we used EEG frequency-tagging to evaluate: (1) Face-Object Categorization, (2) Emotional Facial-Expression Discrimination and (3) Individual Face Discrimination. The EEG was recorded to visual stimuli presented at a rate of 6 Hz, with oddball stimuli at a rate of 1.2 Hz. In all three experiments and in both groups, significant face discriminative responses were found. Face-Object categorization was associated to a relative increased involvement of the left hemisphere in CD individuals compared to HC individuals. A similar trend was observed for Emotional Facial-Expression discrimination but not for Individual Face Discrimination. Source reconstruction suggested a greater activation of the auditory cortices in the CD group for Individual Face Discrimination. These findings suggest that the experience dependence of the relative contribution of the two hemispheres as well as crossmodal plasticity vary with different aspects of face processing.

Consistent behavioral and electrophysiological evidence for rapid perceptual discrimination among the six human basic facial expressions.

The extent to which the six basic human facial expressions perceptually differ from one another remains controversial. For instance, despite the importance of rapidly decoding fearful faces, this expression often is confused with other expressions, such as Surprise in explicit behavioral categorization tasks. We quantified implicit visual discrimination among rapidly presented facial expressions with an oddball periodic visual stimulation approach combined with electroencephalography (EEG), testing for the relationship with behavioral explicit measures of facial emotion discrimination. We report robust facial expression discrimination responses bilaterally over the occipito-temporal cortex for each pairwise expression change. While fearful faces presented as repeated stimuli led to the smallest deviant responses from all other basic expressions, deviant fearful faces were well discriminated overall and to a larger extent than expressions of Sadness and Anger. Expressions of Happiness did not differ quantitatively as much in EEG as for behavioral subjective judgments, suggesting that the clear dissociation between happy and other expressions, typically observed in behavioral studies, reflects higher-order processes. However, this expression differed from all others in terms of scalp topography, pointing to a qualitative rather than quantitative difference. Despite this difference, overall, we report for the first time a tight relationship of the similarity matrices across facial expressions obtained for implicit EEG responses and behavioral explicit measures collected under the same temporal constraints, paving the way for new approaches of understanding facial expression discrimination in developmental, intercultural, and clinical populations.

Rapid neural categorization of angry and fearful faces is specifically impaired in boys with autism spectrum disorder.

BACKGROUND: Difficulties with facial expression processing may be associated with the characteristic social impairments in individuals with autism spectrum disorder (ASD). Emotional face processing in ASD has been investigated in an abundance of behavioral and EEG studies, yielding, however, mixed and inconsistent results. METHODS: We combined fast periodic visual stimulation (FPVS) with EEG to assess the neural sensitivity to implicitly detect briefly presented facial expressions among a stream of neutral faces, in 23 boys with ASD and 23 matched typically developing (TD) boys. Neutral faces with different identities were presented at 6 Hz, periodically interleaved with an expressive face (angry, fearful, happy, sad in separate sequences) every fifth image (i.e., 1.2 Hz oddball frequency). These distinguishable frequency tags for neutral and expressive stimuli allowed direct and objective quantification of the expression-categorization responses, needing only four sequences of 60 s of recording per condition. RESULTS: Both groups show equal neural synchronization to the general face stimulation and similar neural responses to happy and sad faces. However, the ASD group displays significantly reduced responses to angry and fearful faces, compared to TD boys. At the individual subject level, these neural responses allow to predict membership of the ASD group with an accuracy of 87%. Whereas TD participants show a significantly lower sensitivity to sad faces than to the other expressions, ASD participants show an equally low sensitivity to all the expressions. CONCLUSIONS: Our results indicate an emotion-specific processing deficit, instead of a general emotion-processing problem: Boys with ASD are less sensitive than TD boys to rapidly and implicitly detect angry and fearful faces. The implicit, fast, and straightforward nature of FPVS-EEG opens new perspectives for clinical diagnosis.

Tuning functions for automatic detection of brief changes of facial expression in the human brain.

Efficient decoding of even brief and slight intensity facial expression changes is important for social interactions. However, robust evidence for the human brain ability to automatically detect brief and subtle changes of facial expression remains limited. Here we built on a recently developed paradigm in human electrophysiology with full-blown expressions (Dzhelyova et al., 2017), to isolate and quantify a neural marker for the detection of brief and subtle changes of facial expression. Scalp electroencephalogram (EEG) was recorded from 18 participants during stimulation of a neutral face changing randomly in size at a rapid rate of 6 Hz. Brief changes of expression appeared every five stimulation cycle (i.e., at 1.2 Hz) and expression intensity increased parametrically every 20 s in 20% steps during sweep sequences of 100 s. A significant 1.2 Hz response emerged in the EEG spectrum already at 40% of facial expression-change intensity for most of the 5 emotions tested (anger, disgust, fear, happiness, or sadness in different sequences), and increased with intensity steps, predominantly over right occipito-temporal regions. Given the high signal-to-noise ratio of the approach, thresholds for automatic detection of brief changes of facial expression could be determined for every single individual brain. A time-domain analysis revealed three components, the two first increasing linearly with increasing intensity as early as 100 ms after a change of expression, suggesting gradual low-level image-change detection prior to visual coding of facial movements. In contrast, the third component showed abrupt sensitivity to increasing expression intensity beyond 300 ms post expression-change, suggesting categorical emotion perception. Overall, this characterization of the detection of subtle changes of facial expression and its temporal dynamics open promising tracks for precise assessment of social perception ability during development and in clinical populations.

At a Single Glance: Fast Periodic Visual Stimulation Uncovers the Spatio-Temporal Dynamics of Brief Facial Expression Changes in the Human Brain.

Detecting brief changes of facial expression is vital for social communication. Yet, how reliably, how fast these changes are detected and how long they are processed in the human brain remain unknown. High-density electroencephalogram (EEG) was recorded in 18 participants presented with a neutral-expression face at a rate of 5.88 Hz (F) for 80 s. Every five faces, the face changed expression to fear, disgust or happiness (different stimulation sequences). The resulting 1.18 Hz (F/5) EEG response and its harmonics objectively indexed detection of a brief change of facial expression. This response was recorded in every participant in a few minutes but was largely reduced for inverted faces, indicating that it reflects high-level processes. Although this response focused on occipito-temporal sites, different expression changes evoked reliably distinct topographical maps, pointing to partly distinct neural generators. These effects were also observed at a faster 12 Hz frequency rate and a lower ratio of expression change (1/9). Time-domain analysis showed that a brief change of expression inserted in a dynamic stimulation sequence elicits specific occipito-temporal responses between 100 and 310 ms, indicating a rapid change detection process followed by a long integration period of facial expression information in the human brain.

The effect of parametric stimulus size variation on individual face discrimination indexed by fast periodic visual stimulation.

BACKGROUND: The human brain is frequently exposed to individual faces across a wide range of different apparent sizes, often seen simultaneously (e.g., when facing a crowd). Here we used a sensitive and objective fast periodic visual stimulation approach while recording scalp electroencephalogram (EEG) to test the effect of size variation on neural responses reflecting individual face discrimination. METHODS: EEG was recorded in ten observers presented with the same face identity at a fixed rate (5.88 Hz, frequency F) and different oddball face identities appearing every five faces (F/5, i.e., 1.18 Hz). Stimulus size was either constant (6.5 × 4 degrees of visual angle) or changed randomly at each stimulation cycle, by 2:1 ratio increasing values from 10% to 80% size variation in four conditions. Absolute stimulus size remained constant across conditions. RESULTS: The base rate 5.88 Hz EEG response increased with image size variation, particularly over the right occipito-temporal cortex. In contrast, size variation decreased the oddball response marking individual face discrimination over the right occipito-temporal cortex. At constant stimulus size, the F/5 change of identity generated an early (about 100 ms) oddball response reflecting individual face discrimination based on image-based cues. This early component disappeared with a relatively small size variation (i.e., 20%), leaving a robust high-level index of individual face discrimination. CONCLUSIONS: Stimulus size variation is an important manipulation to isolate the contribution of high-level visual processes to individual face discrimination. Nevertheless, even for relatively small stimuli, high-level individual face discrimination processes in the right occipito-temporal cortex remain sensitive to stimulus size variation.

Supra-additive contribution of shape and surface information to individual face discrimination as revealed by fast periodic visual stimulation.

Face perception depends on two main sources of information--shape and surface cues. Behavioral studies suggest that both of them contribute roughly equally to discrimination of individual faces, with only a small advantage provided by their combination. However, it is difficult to quantify the respective contribution of each source of information to the visual representation of individual faces with explicit behavioral measures. To address this issue, facial morphs were created that varied in shape only, surface only, or both. Electrocephalogram (EEG) were recorded from 10 participants during visual stimulation at a fast periodic rate, in which the same face was presented four times consecutively and the fifth face (the oddball) varied along one of the morphed dimensions. Individual face discrimination was indexed by the periodic EEG response at the oddball rate (e.g., 5.88 Hz/5 = 1.18 Hz). While shape information was discriminated mainly at right occipitotemporal electrode sites, surface information was coded more bilaterally and provided a larger response overall. Most importantly, shape and surface changes alone were associated with much weaker responses than when both sources of information were combined in the stimulus, revealing a supra-additive effect. These observations suggest that the two kinds of information combine nonlinearly to provide a full individual face representation, face identity being more than the sum of the contribution of shape and surface cues.

Monitoring the effect of oxytocin on the neural sensitivity to emotional faces via frequency-tagging EEG: A double-blind, cross-over study.

The neuropeptide oxytocin (OXT) is suggested to exert an important role in human social behaviors by modulating the salience of social cues. To date, however, there is mixed evidence whether a single dose of OXT can improve the behavioral and neural sensitivity for emotional face processing. To overcome difficulties encountered with classic event-related potential studies assessing stimulus-saliency, we applied frequency-tagging EEG to implicitly assess the effect of a single dose of OXT (24 IU) on the neural sensitivity for positive and negative facial emotions. Neutral faces with different identities were presented at 6 Hz, periodically interleaved with an expressive face (angry, fearful, and happy, in separate sequences) every fifth image (i.e., 1.2 Hz oddball frequency). These distinctive frequency tags for neutral and expressive stimuli allowed direct and objective quantification of the neural expression-categorization responses. The study involved a double-blind, placebo-controlled, cross-over trial with 31 healthy adult men. Contrary to our expectations, we did not find an effect of OXT on facial emotion processing, neither at the neural, nor at the behavioral level. A single dose of OXT did not evoke social enhancement in general, nor did it affect social approach-avoidance tendencies. Possibly ceiling performances in facial emotion processing might have hampered further improvement.

A neural marker of rapid discrimination of facial expression in 3.5- and 7-month-old infants.

Infants' ability to discriminate facial expressions has been widely explored, but little is known about the rapid and automatic ability to discriminate a given expression against many others in a single experiment. Here we investigated the development of facial expression discrimination in infancy with fast periodic visual stimulation coupled with scalp electroencephalography (EEG). EEG was recorded in eighteen 3.5- and eighteen 7-month-old infants presented with a female face expressing disgust, happiness, or a neutral emotion (in different stimulation sequences) at a base stimulation frequency of 6 Hz. Pictures of the same individual expressing other emotions (either anger, disgust, fear, happiness, sadness, or neutrality, randomly and excluding the expression presented at the base frequency) were introduced every six stimuli (at 1 Hz). Frequency-domain analysis revealed an objective (i.e., at the predefined 1-Hz frequency and harmonics) expression-change brain response in both 3.5- and 7-month-olds, indicating the visual discrimination of various expressions from disgust, happiness and neutrality from these early ages. At 3.5 months, the responses to the discrimination from disgust and happiness expressions were located mainly on medial occipital sites, whereas a more lateral topography was found for the response to the discrimination from neutrality, suggesting that expression discrimination from an emotionally neutral face relies on distinct visual cues than discrimination from a disgust or happy face. Finally, expression discrimination from happiness was associated with a reduced activity over posterior areas and an additional response over central frontal scalp regions at 7 months as compared to 3.5 months. This result suggests developmental changes in the processing of happiness expressions as compared to negative/neutral ones within this age range.

Frequency-Tagging EEG of Superimposed Social and Non-Social Visual Stimulation Streams Provides No Support for Social Salience Enhancement after Intranasal Oxytocin Administration.

The social salience hypothesis proposes that the neuropeptide oxytocin (OT) can impact human social behavior by modulating the salience of social cues. Here, frequency-tagging EEG was used to quantify the neural responses to social versus non-social stimuli while administering a single dose of OT (24 IU) versus placebo treatment. Specifically, two streams of faces and houses were superimposed on one another, with each stream of stimuli tagged with a particular presentation rate (i.e., 6 and 7.5 Hz or vice versa). These distinctive frequency tags allowed unambiguously disentangling and objectively quantifying the respective neural responses elicited by the different streams of stimuli. This study involved a double-blind, placebo-controlled, cross-over trial with 31 healthy adult men. Based on four trials of 60 s, we detected robust frequency-tagged neural responses in each individual, with entrainment to faces being more pronounced in lateral occipito-temporal regions and entrainment to houses being focused in medial occipital regions. However, contrary to our expectation, a single dose of OT did not modulate these stimulus-driven neural responses, not in terms of enhanced social processing nor in terms of generally enhanced information salience. Bayesian analyses formally confirmed these null findings. Possibly, the baseline ceiling level performance of these neurotypical adult participants as well as the personal irrelevance of the applied stimulation streams might have hindered the observation of any OT effect.

Event-related repetitive TMS reveals distinct, critical roles for right OFA and bilateral posterior STS in judging the sex and trustworthiness of faces.

Judging the sex of faces relies on cues related to facial morphology and spatial relations between features, whereas judging the trustworthiness of faces relies on both structural and expressive cues that signal affective valence. The right occipital face area (OFA) processes structural cues and has been associated with sex judgments, whereas the posterior STS processes changeable facial cues related to muscle movements and is activated when observers judge trustworthiness. It is commonly supposed that the STS receives inputs from the OFA, yet it is unknown whether these regions have functionally dissociable, critical roles in sex and trustworthiness judgments. We addressed this issue using event-related, fMRI-guided repetitive transcranial magnetic stimulation (rTMS). Twelve healthy volunteers judged the sex of individually presented faces and, in a separate session, whether those same faces were trustworthy or not. Relative to sham stimulation, RTs were significantly longer for sex judgments when rTMS was delivered over the right OFA but not the right or left STS, and for trustworthiness judgments on male but not female faces when rTMS was delivered over the right STS or left STS but not the right OFA. Nonetheless, an analysis of the RT distributions revealed a possible critical role also for the right OFA in trustworthiness judgments, limited to faces with longer RTs, perhaps reflecting the later, ancillary use of structural cues related to the sex of the face. On the whole, our findings provide evidence that evaluations of the trustworthiness and sex of faces rely on functionally dissociable cortical regions.

The rapid and automatic categorization of facial expression changes in highly variable natural images.

Emotional expressions are quickly and automatically read from human faces under natural viewing conditions. Yet, categorization of facial expressions is typically measured in experimental contexts with homogenous sets of face stimuli. Here we evaluated how the 6 basic facial emotions (Fear, Disgust, Happiness, Anger, Surprise or Sadness) can be rapidly and automatically categorized with faces varying in head orientation, lighting condition, identity, gender, age, ethnic origin and background context. High-density electroencephalography was recorded in 17 participants viewing 50 s sequences with natural variable images of neutral-expression faces alternating at a 6 Hz rate. Every five stimuli (1.2 Hz), variable natural images of one of the six basic expressions were presented. Despite the wide physical variability across images, a significant F/5 = 1.2 Hz response and its harmonics (e.g., 2F/5 = 2.4 Hz, etc.) was observed for all expression changes at the group-level and in every individual participant. Facial categorization responses were found mainly over occipito-temporal sites, with distinct hemispheric lateralization and cortical topographies according to the different expressions. Specifically, a stronger response was found to Sadness categorization, especially over the left hemisphere, as compared to Fear and Happiness, together with a right hemispheric dominance for categorization of Fearful faces. Importantly, these differences were specific to upright faces, ruling out the contribution of low-level visual cues. Overall, these observations point to robust rapid and automatic facial expression categorization processes in the human brain.

Investigating automatic emotion processing in boys with autism via eye tracking and facial mimicry recordings.

Difficulties in automatic emotion processing in individuals with autism spectrum disorder (ASD) might remain concealed in behavioral studies due to compensatory strategies. To gain more insight in the mechanisms underlying facial emotion recognition, we recorded eye tracking and facial mimicry data of 20 school-aged boys with ASD and 20 matched typically developing controls while performing an explicit emotion recognition task. Proportional looking times to specific face regions (eyes, nose, and mouth) and face exploration dynamics were analyzed. In addition, facial mimicry was assessed. Boys with ASD and controls were equally capable to recognize expressions and did not differ in proportional looking times, and number and duration of fixations. Yet, specific facial expressions elicited particular gaze patterns, especially within the control group. Both groups showed similar face scanning dynamics, although boys with ASD demonstrated smaller saccadic amplitudes. Regarding the facial mimicry, we found no emotion specific facial responses and no group differences in the responses to the displayed facial expressions. Our results indicate that boys with and without ASD employ similar eye gaze strategies to recognize facial expressions. Smaller saccadic amplitudes in boys with ASD might indicate a less exploratory face processing strategy. Yet, this slightly more persistent visual scanning behavior in boys with ASD does not imply less efficient emotion information processing, given the similar behavioral performance. Results on the facial mimicry data indicate similar facial responses to emotional faces in boys with and without ASD. LAY SUMMARY: We investigated (i) whether boys with and without autism apply different face exploration strategies when recognizing facial expressions and (ii) whether they mimic the displayed facial expression to a similar extent. We found that boys with and without ASD recognize facial expressions equally well, and that both groups show similar facial reactions to the displayed facial emotions. Yet, boys with ASD visually explored the faces slightly less than the boys without ASD.

Combined frequency-tagging EEG and eye-tracking measures provide no support for the "excess mouth/diminished eye attention" hypothesis in autism.

BACKGROUND: Scanning faces is important for social interactions. Difficulty with the social use of eye contact constitutes one of the clinical symptoms of autism spectrum disorder (ASD). It has been suggested that individuals with ASD look less at the eyes and more at the mouth than typically developing (TD) individuals, possibly due to gaze aversion or gaze indifference. However, eye-tracking evidence for this hypothesis is mixed. While gaze patterns convey information about overt orienting processes, it is unclear how this is manifested at the neural level and how relative covert attention to the eyes and mouth of faces might be affected in ASD. METHODS: We used frequency-tagging EEG in combination with eye tracking, while participants watched fast flickering faces for 1-min stimulation sequences. The upper and lower halves of the faces were presented at 6 Hz and 7.5 Hz or vice versa in different stimulation sequences, allowing to objectively disentangle the neural saliency of the eyes versus mouth region of a perceived face. We tested 21 boys with ASD (8-12 years old) and 21 TD control boys, matched for age and IQ. RESULTS: Both groups looked longer at the eyes than the mouth, without any group difference in relative fixation duration to these features. TD boys looked significantly more to the nose, while the ASD boys looked more outside the face. EEG neural saliency data partly followed this pattern: neural responses to the upper or lower face half were not different between groups, but in the TD group, neural responses to the lower face halves were larger than responses to the upper part. Face exploration dynamics showed that TD individuals mostly maintained fixations within the same facial region, whereas individuals with ASD switched more often between the face parts. LIMITATIONS: Replication in large and independent samples may be needed to validate exploratory results. CONCLUSIONS: Combined eye-tracking and frequency-tagged neural responses show no support for the excess mouth/diminished eye gaze hypothesis in ASD. The more exploratory face scanning style observed in ASD might be related to their increased feature-based face processing style.

Frequency-Tagging Electroencephalography of Superimposed Social and Non-Social Visual Stimulation Streams Reveals Reduced Saliency of Faces in Autism Spectrum Disorder.

Individuals with autism spectrum disorder (ASD) have difficulties with social communication and interaction. The social motivation hypothesis states that a reduced interest in social stimuli may partly underlie these difficulties. Thus far, however, it has been challenging to quantify individual differences in social orientation and interest, and to pinpoint the neural underpinnings of it. In this study, we tested the neural sensitivity for social versus non-social information in 21 boys with ASD (8-12 years old) and 21 typically developing (TD) control boys, matched for age and IQ, while children were engaged in an orthogonal task. We recorded electroencephalography (EEG) during fast periodic visual stimulation (FPVS) of social versus non-social stimuli to obtain an objective implicit neural measure of relative social bias. Streams of variable images of faces and houses were superimposed, and each stream of stimuli was tagged with a particular presentation rate (i.e., 6 and 7.5 Hz or vice versa). This frequency-tagging method allows disentangling the respective neural responses evoked by the different streams of stimuli. Moreover, by using superimposed stimuli, we controlled for possible effects of preferential looking, spatial attention, and disengagement. Based on four trials of 60 s, we observed a significant three-way interaction. In the control group, the frequency-tagged neural responses to faces were larger than those to houses, especially in lateral occipito-temporal channels, while the responses to houses were larger over medial occipital channels. In the ASD group, however, faces and houses did not elicit significantly different neural responses in any of the regions. Given the short recording time of the frequency-tagging paradigm with multiple simultaneous inputs and the robustness of the individual responses, the method could be used as a sensitive marker of social preference in a wide range of populations, including younger and challenging populations.

Combined frequency-tagging EEG and eye tracking reveal reduced social bias in boys with autism spectrum disorder.

Developmental accounts of autism spectrum disorder (ASD) state that infants and children with ASD are spontaneously less attracted by and less proficient in processing social stimuli such as faces. This is hypothesized to partly underlie social communication difficulties in ASD. While in some studies a reduced preference for social stimuli has been shown in individuals with ASD, effect sizes are moderate and vary across studies, stimuli, and designs. Eye tracking, often the methodology of choice to study social preference, conveys information about overt orienting processes but conceals covert attention, possibly resulting in an underestimation of the effects. In this study, we recorded eye tracking and electroencephalography (EEG) during fast periodic visual stimulation to address this issue. We tested 21 boys with ASD (8-12 years old) and 21 typically developing (TD) control boys, matched for age and IQ. Streams of variable images of faces were presented at 6 Hz alongside images of houses presented at 7.5 Hz or vice versa, while children were engaged in an orthogonal task. While frequency-tagged neural responses were larger in response to faces than simultaneously presented houses in both groups, this effect was much larger in TD boys than in boys with ASD. This group difference in saliency of social versus non-social processing is significant after 5 sec of stimulus presentation and holds throughout the entire trial. Although there was no interaction between group and stimulus category for simultaneously recorded eye-tracking data, eye tracking and EEG measures were strongly correlated. We conclude that frequency-tagging EEG, allowing monitoring of both overt and covert processes, provides a fast, objective and reliable measure of decreased preference for social information in ASD.

A robust implicit measure of facial attractiveness discrimination.

Decisions of attractiveness from the human face are made instantly and spontaneously, but robust implicit neural measures of facial attractiveness discrimination are currently lacking. Here we applied fast periodic visual stimulation coupled with electroencephalography (EEG) to objectively measure the neural coding of facial attractiveness. We presented different pictures of faces at 6 Hz, i.e. six faces/second, for a minute while participants attended to a central fixation cross and indicated whether the cross shortly changed color. Every other face in the stimulation was attractive and was replaced by a relatively less attractive face. This resulted in alternating more/less attractive faces at a 3 Hz rate, eliciting a significant increase in occipito-temporal EEG amplitude at 3 Hz both at the group and the individual participant level. This response was absent in two control conditions where either only attractive or only less attractive faces were presented. These observations support the view that face-sensitive visual areas discriminate attractiveness implicitly and rapidly from the human face.

Rapid and automatic discrimination between facial expressions in the human brain.

Automatic responses to brief expression changes from a neutral face have been recently isolated in the human brain using fast periodic visual stimulation (FPVS) coupled with scalp electroencephalography (EEG). Based on these observations, here we isolate specific neural signatures for the rapid categorization of each of 5 basic expressions, i.e., when they are directly discriminated from all other facial expressions. Scalp EEG was recorded in 15 participants presented with pictures alternating at a rapid 6 Hz rate (i.e., one fixation/face, backward- and forward-masked). In different stimulation sequences, an expressive (angry, disgusted, happy, fearful, or sad) or a neutral face arose every 5 pictures (i.e., at 6/5 = 1.2 Hz), among pictures of the same individual expressing the other emotions randomly. Frequency-domain analysis indicated a robust (i.e., recorded in every individual participant) and objective (i.e., at the predefined 1.2 Hz frequency and its harmonics) expression-specific brain response over occipito-temporal sites for each emotion and neutrality. In this context of variable expressions, while neural responses to the different expressions (Anger, Disgust, Happiness, Sadness) were dissimilar qualitatively, a much larger specific signature for neutral faces as compared to facial expressions was found. Interestingly, Fear also elicited a strong contrasted response with other facial expressions, associated with a specific neural signature over ventral occipito-temporal sites. Collectively, these findings reveal that specific EEG signatures for different facial expressions can be isolated in the human brain, pointing to partially different neural substrates. In addition, they provide support for a strong and highly selective neural response to fear at the system-level, in line with the importance of this emotional expression for biological survival.