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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.

International audience; A recent body of research has emerged regarding the interactions between olfaction and other sensory channels to process social information. The current review examines the influence of body odors on face perception, a core component of human social cognition. First, we review studies reporting how body odors interact with the perception of invariant facial information (i.e., identity, sex, attractiveness, trustworthiness, and dominance). Although we mainly focus on the influence of body odors based on axillary odor, we also review findings about specific steroids present in axillary sweat (i.e., androstenone, androstenol, androstadienone, and estratetraenol). We next survey the literature showing body odor influences on the perception of transient face properties, notably in discussing the role of body odors in facilitating or hindering the perception of emotional facial expression, in relation to competing frameworks of emotions. Finally, we discuss the developmental origins of these olfaction-to-vision influences, as an emerging literature indicates that odor cues strongly influence face perception in infants. Body odors with a high social relevance such as the odor emanating from the mother have a widespread influence on various aspects of face perception in infancy, including categorization of faces among other objects, face scanning behavior, or facial expression perception. We conclude by suggesting that the weight of olfaction might be especially strong in infancy, shaping social perception, especially in slow-maturing senses such as vision, and that this early tutoring function of olfaction spans all developmental stages to disambiguate a complex social environment by conveying key information for social interactions until adulthood.

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.

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; Visual categorization is the rapid and automatic ability to provide a similar response to different exemplars of a single category despite widely variable sensory inputs. Whether visual categorization is solely visually-driven or can be influenced by other sensory modalities remains unclear. Here we test whether odor contexts can modulate visual categorization in humans, expecting that congruent odors facilitate the categorization of visual objects as a function of their ambiguity. Scalp electroencephalogram (EEG) was recorded in N = 26 participants while naturalistic object stimuli were displayed in rapid 12-Hz streams (i.e., 12 images / second, leading to a 12-Hz general response in the EEG frequency spectrum). Variable exemplars of a target category (human faces, cars, or facelike objects in different sequences) were interspersed every 9 stimuli to tag category-selective EEG responses at 12/9 = 1.33 Hz. During visual stimulation, odor contexts (body, gasoline or baseline odors) were implicitly diffused. Category-selective responses to every category are clearly isolated over the occipito-temporal cortex, with the largest response for human faces and the lowest for facelike objects. Importantly, body odors enhance the right-hemispheric response to the ambiguous category, i.e., facelike objects, which are either perceived as nonface objects or faces. This odor effect is especially found in participants who noticed the illusory faces during visual stimulation. In contrast, odor contexts do not modulate other category-selective responses, nor the 12-Hz general response, revealing a selective facilitation of the visual categorization of congruent ambiguous stimuli. Altogether, these observations indicate that the visual system can rely on non-visual cues for efficient categorization, and that olfaction, which is often considered as poor in humans, is ideally suited to assist visual categorization.

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.

Recent ERP research has indicated that the processing of faces of other races (OR) and same race (SR) as the perceiver differs at the perceptual level, more precisely for the N170 component. The purpose of the present study was to continue the investigation of the race-of-face processing across multiple orientations. Event-related brain potentials (ERPs) and performance were recorded when Caucasian participants were required to categorize by race Caucasian and African faces presented in eight different angles of orientation. Three main observations were made: (1) the face-sensitive N170 is modulated by the race of faces, being larger in response to OR compared to SR faces; (2) face rotation affected this component in the same pattern for both racial groups; (3) the N170-ORE progressively disappeared as the faces moved away from their canonical orientation at the right hemisphere only. Thus, the current findings suggest that configural/holisitic information is extracted from faces of both racial groups, but that upright OR faces require increased demands.

Models of face processing suggest that facial familiarity and expression processes involve independent visual systems. But under some conditions, the two processes interact, as when selective attention is solicited, and/or when a link is established between consecutive stimuli. To assess these assumptions during perceptual face processing, event-related potentials (ERPs) were used while subjects discriminated either familiarity or expression in a task-switching paradigm. Switched trials were designed with competitor priming, the unattended dimension being previously attended. The results indicate interactions appearing in the right hemisphere during the perceptual encoding stage (N170) when subjects processed either familiarity or expression during switched trials. These interactions gain both hemispheres during memory retrieval (P2) and in terms of accuracy. Altogether, these results confirm the critical role of the right hemisphere in perceiving faces and their expressions. Moreover, they suggest that familiarity and expression can interact in both directions.

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.

Resume L’alteration de la cognition sociale associee a la schizophrenie, dont fait partie la perception des emotions faciales, a fait l’objet d’une recente meta-analyse qui a revele son impact majeur sur l’insertion sociale et professionnelle. Or l’utilisation de programmes de remediation cognitive portant sur le traitement des emotions faciales est freinee par un manque d’outil permettant d’identifier et de quantifier les troubles pour un sujet donne. Le test de reconnaissance des emotions faciales (TREF) permet d’evaluer la capacite a reconnaitre 6 emotions universelles (joie, colere, tristesse, peur, degout et mepris), presentees a neuf intensites d’expression s’etalant de 20 % a 100 %. Les resultats de l’etude comparative realisee aupres d’un echantillon de 64 sujets temoins sains et de 45 personnes souffrant de schizophrenie montrent, de maniere coherente avec les donnees de la litterature, une diminution significative des performances de reconnaissance des emotions faciales dans la schizophrenie. Des scores seuils sont proposes afin de permettre l’utilisation du TREF pour l’identification et la specification de la presence d’un deficit de reconnaissance des emotions faciales chez un sujet donne, et permettre son orientation vers une prise en charge specifique.

The properties of the face-sensitive N170 component of the event-related brain potential (ERP) were explored through an orientation discrimination task using natural faces, objects, and Arcimboldo paintings presented upright or inverted. Because Arcimboldo paintings are composed of non-face objects but have a global face configuration, they provide great control to disentangle high-level face-like or object-like visual processes at the level of the N170, and may help to examine the implication of each hemisphere in the global/holistic processing of face formats. For upright position, N170 amplitudes in the right occipito-temporal region did not differ between natural faces and Arcimboldo paintings but were larger for both of these categories than for objects, supporting the view that as early as the N170 time-window, the right hemisphere is involved in holistic perceptual processing of face-like configurations irrespective of their features. Conversely, in the left hemisphere, N170 amplitudes differed between Arcimboldo portraits and natural faces, suggesting that this hemisphere processes local facial features. For upside-down orientation in both hemispheres, N170 amplitudes did not differ between Arcimboldo paintings and objects, but were reduced for both categories compared to natural faces, indicating that the disruption of holistic processing with inversion leads to an object-like processing of Arcimboldo paintings due to the lack of local facial features. Overall, these results provide evidence that global/holistic perceptual processing of faces and face-like formats involves the right hemisphere as early as the N170 time-window, and that the local processing of face features is rather implemented in the left hemisphere.

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.

Previous studies on face processing have revealed an asymmetric overlap between identity and expression, as identity is processed irrespective of expression while expression processing partly depends on identity. To investigate whether this relative interaction is caused by dominance of identity over expression, participants performed familiarity and expression judgments during task switching. This paradigm reveals task-set dominance with a paradoxical asymmetric switch-cost (i.e., greater difference between switch and repeat trials when switching toward the dominant task). Event-related potentials (ERPs) were recorded to find the neural signature of the asymmetric cost. As expected, greater switch-cost was shown in the familiarity task with respect to response times, indicating its dominance over the expression task. Moreover, a left-sided ERP correlate of this effect was observed at the level of the frontal N2 component, interpreted as an index of modulations in endogenous executive control. Altogether, these results confirm the overlap between identity and expression during face processing and further indicate their relative dominance.