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International audience; Sex categorization is essential for mate choice and social interactions in many animal species. In humans, sex categorization is readily performed from the face. However, clear neural markers of face-sex categorization, i.e., common responses to widely variable individuals from one sex, have not been identified so far in humans. To isolate a direct signature of rapid and automatic face-sex categorization generalized across a wide range of variable exemplars, we recorded scalp electroencephalogram (EEG) from 32 participants (16 females) while they were exposed to variable natural face images from one sex alternating at a rapid rate of 6 Hz (i.e., 6 images per second). Images from the other sex were inserted every 6th stimulus (i.e., at a 1-Hz rate). A robust categorization response to both sex contrasts emerged at 1 Hz and harmonics in the EEG frequency spectrum over the occipito-temporal cortex of most participants. The response was larger for female faces presented among male faces than the reverse, suggesting that the two sex categories are not equally homogenous. This asymmetrical response pattern disappeared for upside-down faces, ruling out the contribution of low-level physical variability across images. Overall, these observations demonstrate that sex categorization occurs automatically after a single glance at natural face images and can be objectively isolated and quantified in the human brain within a few minutes.

Visual categorization is the brain ability to rapidly and automatically respond to widely variable visual inputs in a category-selective manner (i.e., distinct responses between categories and similar responses within categories). Whether category-selective neural responses are purely visual or can be influenced by other sensory modalities remains unclear. Here, we test whether odors modulate visual categorization, expecting that odors facilitate the neural categorization of congruent visual objects, especially when the visual category is ambiguous. Scalp electroencephalogram (EEG) was recorded while natural images depicting various objects were displayed in rapid 12-Hz streams (i.e., 12 images / second) and variable exemplars of a target category (either human faces, cars, or facelike objects in dedicated sequences) were interleaved every 9th stimulus to tag category-selective responses at 12/9 = 1.33 Hz in the EEG frequency spectrum. During visual stimulation, participants (N = 26) were implicitly exposed to odor contexts (either body, gasoline or baseline odors) and performed an orthogonal cross-detection task. We identify clear category-selective responses to every category over the occipito-temporal cortex, with the largest response for human faces and the lowest for facelike objects. Critically, body odor boosts the response to the ambiguous facelike objects (i.e., either perceived as nonface objects or faces) over the right hemisphere, especially for participants reporting their presence post-stimulation. By contrast, odors do not significantly modulate other category-selective responses, nor the general visual response recorded at 12 Hz, revealing a specific influence on the categorization of congruent ambiguous stimuli. Overall, these findings support the view that the brain actively uses cues from the different senses to readily categorize visual inputs, and that olfaction, which is generally considered as poorly functional in humans, is well placed to disambiguate visual information.

International audience; Understanding how the young infant brain starts to categorize the flurry of ambiguous sensory inputs coming in from its complex environment is of primary scientific interest. Here, we test the hypothesis that senses other than vision play a key role in initiating complex visual categorizations in 20 4-mo-old infants exposed either to a baseline odor or to their mother’s odor while their electroencephalogram (EEG) is recorded. Various natural images of objects are presented at a 6-Hz rate (six images/second), with face-like object configurations of the same object categories (i.e., eliciting face pareidolia in adults) interleaved every sixth stimulus (i.e., 1 Hz). In the baseline odor context, a weak neural categorization response to face-like stimuli appears at 1 Hz in the EEG frequency spectrum over bilateral occipitotemporal regions. Critically, this face-like–selective response is magnified and becomes right lateralized in the presence of maternal body odor. This reveals that nonvisual cues systematically associated with human faces in the infant’s experience shape the interpretation of face-like configurations as faces in the right hemisphere, dominant for face categorization. At the individual level, this intersensory influence is particularly effective when there is no trace of face-like categorization in the baseline odor context. These observations provide evidence for the early tuning of face-(like)–selective activity from multisensory inputs in the developing brain, suggesting that perceptual development integrates information across the senses for efficient category acquisition, with early maturing systems such as olfaction driving the acquisition of categories in later-developing systems such as vision.

The human brain rapidly and automatically categorizes faces vs. other visual objects. However, whether face-selective neural activity predicts the subjective experience of a face – perceptual awareness – is debated. To clarify this issue, here we use face pareidolia, i.e., the illusory perception of a face, as a proxy to relate the neural categorization of a variety of facelike objects to conscious face perception. In Experiment 1, scalp electroencephalogram (EEG) is recorded while pictures of human faces or facelike objects – in different stimulation sequences – are interleaved every second (i.e., at 1 Hz) in a rapid 6-Hz train of natural images of nonface objects. Participants do not perform any explicit face categorization task during stimulation, and report whether they perceived illusory faces post-stimulation. A robust categorization response to facelike objects is identified at 1 Hz and harmonics in the EEG frequency spectrum with a facelike occipito-temporal topography. Across all individuals, the facelike categorization response is of about 20% of the response to human faces, but more strongly right-lateralized. Critically, its amplitude is much larger in participants who report having perceived illusory faces. In Experiment 2, facelike or matched nonface objects from the same categories appear at 1 Hz in sequences of nonface objects presented at variable stimulation rates (60 Hz to 12 Hz) and participants explicitly report after each sequence whether they perceived illusory faces. The facelike categorization response already emerges at the shortest stimulus duration (i.e., 17 ms at 60 Hz) and predicts the behavioral report of conscious perception. Strikingly, neural facelike-selectivity emerges exclusively when participants report illusory faces. Collectively, these experiments characterize a neural signature of face pareidolia in the context of rapid categorization, supporting the view that face-selective brain activity reliably predicts the subjective experience of a face from a single glance at a variety of stimuli.Highlights- EEG frequency-tagging measures the rapid categorization of facelike objects- Facelike objects elicit a facelike neural categorization response- Neural face categorization predicts conscious face perception across variable inputs

International audience; The influence of odor valence on expressive-face perception remains unclear. Here, three "valenced" odor contexts (pleasant, unpleasant, control) were diffused while scalp electroencephalogram (EEG) was recorded in 18 participants presented with expressive faces alternating at a 6-Hz rate. One facial expression (happiness, disgust or neutrality) repeatedly arose every 6 face pictures to isolate its discrimination from other expressions at 1 Hz and harmonics in the EEG spectrum. The amplitude of the brain response to neutrality was larger in the pleasant vs. control odor context, and fewer electrodes responded in the unpleasant odor context. The number of responding electrodes was reduced for disgust in both odor contexts. The response to happiness was unchanged between odor conditions. Overall, these observations suggest that valenced odors influence the neural discrimination of facial expressions depending on both face and odor hedonic valence, especially for the emotionally ambiguous neutral expression.

International audience; According to recent evidence, rapid categorization of natural face images in the infant brain is enhanced by concomitant maternal odor (Leleu et al., 2029). To test whether this effect is selective to faces, we recorded scalp electroencephalogram (EEG) in 4-month-old infants presented with variable exemplars of a nonface visual category - cars - appearing every 6 stimuli in 6-Hz streams of natural object images. At the same time, infants were exposed to the maternal or to a control odor context. A relatively weak neural categorization response to cars (i.e., a differential response to cars that generalizes across exemplars) was observed at 1 Hz over the right occipital cortex in both odor conditions, revealing rapid categorization of an unfamiliar object in the infant brain. However, the car categorization response was not modulated by maternal odor, suggesting that odors selectively prime neural activity in the infant visual cortex to categorize congruent incoming inputs.

International audience; Humans exhibit a marked specialization to process the most experienced facial morphologies. In particular, nonhuman primate faces are poorly discriminated compared to human faces in behavioral tasks. So far however, a clear and consistent marker that quantifies our expertise in human over monkey face discrimination directly from brain activity is lacking. Here, using scalp electroencephalography (EEG), we isolate a direct signature of individuation abilities for human and nonhuman (i.e., macaque faces) primate faces. Human or monkey faces were rapidly presented at a base rate of 12Hz in upright or inverted orientations while participants performed an orthogonal behavioral task. In each stimulation sequence, eight face images of one individual were used as base stimuli, while images of other individuals were briefly introduced every 9th stimulus to quantify an identity-change response at 1.33Hz and harmonics (i.e., integer multiples) in the EEG frequency spectrum. The brain response to upright human faces was twice as large as to monkey faces, and reduced following picture-plane inversion for human faces only. This reflects the disruption of high-level face identity discrimination developed for the canonical upright human face. No difference was observed between upright monkey faces and inverted human faces, suggesting non-expert visual processes for those two face formats associated with little experience. In addition, the size of the inversion effect for human, but not monkey faces, was predictive of the expertise effect (i.e., difference between upright human and monkey faces) at the individual level. This result suggests a selective ability to discriminate human faces that does not contribute to the individuation of other unexperienced face morphologies such as monkey faces. Overall, these findings indicate that human expertise for conspecific face discrimination can be isolated and quantified in individual human brains.

Although various psychiatric disorders present with social-cognitive impairment, a measure assessing social-cognitive processes implicitly and reliably, with high selectivity and with enough signal-to-noise ratio (SNR) for individual evaluation of any population at any age, is lacking. Here we isolate a neural marker quantifying impaired visual coding of facial expression in individuals with 22q11.2 deletion syndrome (22q11DS) using frequency-tagging with electroencephalography (EEG). Twenty-two 22q11DS participants and 22 healthy controls were presented with changes of facial expression displayed at low, moderate, and high intensities every five cycles in a stream of one neutral face repeating 6 times per second (i.e., at a 6 Hz base rate). The brain response to expression changes tagged at the 1.2 Hz (i.e., 6 Hz/5) predefined frequency was isolated over occipito-temporal regions in both groups of participants for moderate- and high-intensity facial expressions. Neural sensitivity to facial expression was reduced by about 36% in 22q11DS, revealing impaired visual coding of emotional facial signals. The significance of the expression-change response was estimated for each single participant thanks to the high SNR of the approach. Further analyses revealed the high reliability of the response and its immunity from other neurocognitive skills. Interestingly, response magnitude was associated with the severity of positive symptoms, pointing to a potential endophenotype for psychosis risk. Overall, the present study reveals an objective, selective, reliable, and behavior-free signature of impaired visual coding of facial expression implicitly quantified from brain activity with high SNR. This novel tool opens avenues for clinical practice, providing a potential early biomarker for later psychosis onset and offering an alternative for individual assessment of social-cognitive functioning in even difficult-to-test participants.

Variation in facial emotion processing abilities may contribute to variability in penetrance for psychotic symptoms in 22q11.2DS. However, the precise nature of the social cognitive dysfunction (i.e., facial expression perception vs. emotion recognition), the potential additional roles of genetic and environmental variabilities, and consequently the possibility of using this neurocognitive marker in clinical monitoring remain unclear. The present case study aimed at testing the hypothesis that when confounding factors are controlled, the presence of psychotic symptoms in 22q11.2DS is associated, at the individual level, with a neural marker of facial expression perception rather than explicit emotional face recognition. Two monozygotic twins with 22q11.2DS discordant for psychiatric manifestations performed (1) a classical facial emotion labelling task and (2) an implicit neural measurement of facial expression perception using a frequency-tagging approach in electroencephalography (EEG). Analysis of the periodic brain response elicited by a change of facial expression from neutrality indicated that the twin with psychotic symptoms did not detect emotion among neutral faces while the twin without the symptoms did. In contrast, both encountered difficulties labelling facial emotion. The results from this exploratory twin study support the idea that impaired facial expression perception rather than explicit recognition of the emotion expressed might be a neurocognitive endophenotype of psychotic symptoms that could be reliable at a clinical level. Although confirmatory studies should be required, it facilitates further discussion on the etiology of the clinical phenotype in 22q11.2DS., Highlights • Study design is a privileged opportunity to highlight reliable endophenotypes of psychiatric symptoms at an individual level • Impaired facial expression perception rather than explicit recognition might be an endophenotype of psychotic symptoms • Further discussion on the etiology of the incomplete penetrance for psychotic symptoms in 22q11.2DS

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.

Open access article; International audience; Rare neurodevelopmental syndromes often present social cognitive deficits that may underlie difficulties in social interactions and increase the risk of psychosis or autism spectrum disorders. However, little is known regarding the specificities of social cognitive impairment across syndromes while it remains a major challenge for the care. Our review provides an overview of social cognitive dysfunctions in rare diseases associated with psychiatric symptoms (with a prevalence estimated between 1 in 1,200 and 1 in 25,000 live births: 22q11.2 deletion syndrome, Angelman syndrome, Fragile X syndrome, Klinefelter syndrome, Prader-Willi syndrome, Rett syndrome, Smith-Magenis syndrome, Turner syndrome, and Williams syndrome) and shed some light on the specific mechanisms that may underlie these skills in each clinical presentation. We first detail the different processes included in the generic expression "social cognition" before summarizing the genotype, psychiatric phenotype, and non-social cognitive profile in each syndrome. Then, we offer a systematic review of the social cognitive abilities and the disturbed mechanisms they are likely associated with. We followed the PRISMA process, including the definition of the relevant search terms, the selection of studies based on clear inclusion, and exclusion criteria and the quality appraisal of papers. We finally provide insights that may have considerable influence on the development of adapted therapeutic interventions such as social cognitive training (SCT) therapies specifically designed to target the psychiatric phenotype. The results of this review suggest that social cognition impairments share some similarities across syndromes. We propose that social cognitive impairments are strongly involved in behavioral symptoms regardless of the overall cognitive level measured by intelligence quotient. Better understanding the mechanisms underlying impaired social cognition may lead to adapt therapeutic interventions. The studies targeting social cognition processes offer new thoughts about the development of specific cognitive training programs, as they highlight the importance of connecting neurocognitive and SCT techniques.

International audience; Difficulties in the recognition of emotions in expressive faces have been reported in people with 22q11.2 deletion syndrome (22q11.2DS). However, while low-intensity expressive faces are frequent in everyday life, nothing is known about their ability to perceive facial emotions depending on the intensity of expression. Through a visual matching task, children and adolescents with 22q11.2DS as well as gender- and age-matched healthy participants were asked to categorise the emotion of a target face among six possible expressions. Static pictures of morphs between neutrality and expressions were used to parametrically manipulate the intensity of the target face. In comparison to healthy controls, results showed higher perception thresholds (i.e. a more intense expression is needed to perceive the emotion) and lower accuracy for the most expressive faces indicating reduced categorisation abilities in the 22q11.2DS group. The number of intrusions (i.e. each time an emotion is perceived as another one) and a more gradual perception performance indicated smooth boundaries between emotional categories. Correlational analyses with neuropsychological and clinical measures suggested that reduced visual skills may be associated with impaired categorisation of facial emotions. Overall, the present study indicates greater difficulties for children and adolescents with 22q11.2DS to perceive an emotion in low-intensity expressive faces. This disability is subtended by emotional categories that are not sharply organised. It also suggests that these difficulties may be associated with impaired visual cognition, a hallmark of the cognitive deficits observed in the syndrome. These data yield promising tracks for future experimental and clinical investigations.

Resume La microdeletion 22q11.2 est le syndrome microdeletionnel le plus frequent de la population generale. Le phenotype associe des anomalies de l’appareil pharynge embryonnaire a un phenotype neurocomportemental. La presentation clinique du syndrome est extremement variable d’un individu a l’autre, quelle que soit la taille de la deletion, et plus de 180 manifestations ont ete decrites, aucune n’etant pathognomonique. Les symptomes psychiatriques, particulierement de nature psychotique, sont frequents dans la microdeletion 22q11.2 et de nombreux psychiatres sont amenes a rencontrer ces patients. La prise en charge doit tenir compte des particularites du syndrome. L’evaluation de la neurocognition, de la cognition sociale et la recherche de symptomes psychiatriques dans le contexte medical general sont une etape fondamentale. Concernant le phenotype neurocomportemental, les soins de remediation cognitive doivent etre combines a une prescription mesuree de psychotropes pour aboutir a une meilleure qualite de vie de ces patients.

We studied the time course of the cerebral integration of olfaction in the visual processing of emotional faces during an orthogonal task asking for detection of red-colored faces among expressive faces. Happy, angry, disgust, fearful, sad, and neutral faces were displayed in pleasant, aversive or no odor control olfactory contexts while EEG was recorded to extract event-related potentials (ERPs). Results indicated that the expressive faces modulated the cerebral responses at occipito-parietal, central and central-parietal electrodes from around 100 ms and until 480 ms after face onset. The response was divided in different successive stages corresponding to different ERP components (P100, N170, P200 and N250 (EPN), and LPP). The olfactory contexts influenced the ERPs in response to facial expressions in two phases. First, regardless of their emotional content, the response to faces was enhanced by both odors compared with no odor approximately 160 ms after face-onset at several central, centro-parietal and left lateral electrodes. The topography of this effect clearly depended on the valence of odors. Then, a second phase occurred, but only in the aversive olfactory context, which modulated differentially the P200 at occipital sites (starting approximately 200 ms post-stimulus) by amplifying the differential response to expressions, especially between emotional neutrality and both happiness and disgust. Overall, the present study suggests that the olfactory context first elicits an undifferentiated effect around 160 ms after face onset, followed by a specific modulation at 200 ms induced by the aversive odor on neutral and affectively congruent/incongruent expressions.

Sex-related hemispheric lateralization and interhemispheric transmission times (IHTTs) were examined in twenty-four participants at the level of the first visual ERP components (P1 and N170) during face identity encoding in a divided visual-field paradigm. While no lateralization-related and sex-related differences were reflected in the P1 characteristics, these two factors modulated the N170. Indeed, N170 amplitudes indicated a right hemisphere (RH) dominance in men (and a more bilateral functioning in women). N170 latencies and the derived IHTTs confirmed the RH advantage in men but showed the reverse asymmetry in women. Altogether, the results of this study suggest a clear asymmetry in men and a more divided work between the hemispheres in women, with a tendency toward a left hemisphere (LH) advantage. Thus, by extending the pattern to the right-sided face processing, our results generalize previous findings from studies using other materials and indicating longer transfers from the specialized to the non-specialized hemisphere, especially in the male brain. Because asymmetries started from the N170 component, the first electrophysiological index of high-level perceptual processing on face representations, they also suggest a functional account for hemispheric lateralization and sex-related differences rather than a structural one. (c) 2013 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved.