Odor-driven face-like categorization in the human infant brain.

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.

Expertise for conspecific face individuation in the human brain.

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 12 Hz 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 1.33 Hz 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.

Maternal odor shapes rapid face categorization in the infant brain.

To successfully interact with a rich and ambiguous visual environment, the human brain learns to differentiate visual stimuli and to produce the same response to subsets of these stimuli despite their physical difference. Although this visual categorization function is traditionally investigated from a unisensory perspective, its early development is inherently constrained by multisensory inputs. In particular, an early-maturing sensory system such as olfaction is ideally suited to support the immature visual system in infancy by providing stability and familiarity to a rapidly changing visual environment. Here, we test the hypothesis that rapid visual categorization of salient visual signals for the young infant brain, human faces, is shaped by another highly relevant human-related input from the olfactory system, the mother's body odor. We observe that a right-hemispheric neural signature of single-glance face categorization from natural images is significantly enhanced in the maternal versus a control odor context in individual 4-month-old infant brains. A lack of difference between odor conditions for the common brain response elicited by both face and non-face images rules out a mere enhancement of arousal or visual attention in the maternal odor context. These observations show that face-selective neural activity in infancy is mediated by the presence of a (maternal) body odor, providing strong support for multisensory inputs driving category acquisition in the developing human brain and having important implications for our understanding of human perceptual development.

Task-related modulation of facial expression processing: An FPVS-EEG study.

In the current study, we examined the role of task-related top-down mechanisms in the recognition of facial expressions. An expression of increasing intensity was displayed at a frequency of 1.5 Hz among the neutral faces of the same model that was displayed at a frequency of 12 Hz (i.e., 12 frames per second, with the expression occurring every eight frames). Twenty-two participants were asked either to recognize the emotion at the expression-specific frequency (1.5 Hz) or to perform an orthogonal task in separate blocks, while a scalp electroencephalogram (EEG) was recorded. A significant 1.5 Hz response emerged with the increase in expressive intensity over the medial occipital, right and left occipitotemporal, and centro-frontal regions. In these three regions, the magnitude of this response was greater when participants were involved in expression recognition, especially when the intensity of expression was low and ambiguous. Time-domain analysis revealed that engagement in the explicit recognition of facial expression caused a modulation of the response even before the onset of the expression over centro-frontal regions. The response was then amplified over the medial occipital and right and left occipitotemporal regions. Overall, the procedure developed in the present study allowed us to document different stages of the voluntary recognition of facial expressions, from detection to recognition, through the implementation of task-related top-down mechanisms that modulated the incoming information flow. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

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.

Odor-evoked hedonic contexts influence the discrimination of facial expressions in the human brain.

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.

The spatial distribution of eye movements predicts the (false) recognition of emotional facial expressions.

Recognizing facial expressions of emotions is a fundamental ability for adaptation to the social environment. To date, it remains unclear whether the spatial distribution of eye movements predicts accurate recognition or, on the contrary, confusion in the recognition of facial emotions. In the present study, we asked participants to recognize facial emotions while monitoring their gaze behavior using eye-tracking technology. In Experiment 1a, 40 participants (20 women) performed a classic facial emotion recognition task with a 5-choice procedure (anger, disgust, fear, happiness, sadness). In Experiment 1b, a second group of 40 participants (20 women) was exposed to the same materials and procedure except that they were instructed to say whether (i.e., Yes/No response) the face expressed a specific emotion (e.g., anger), with the five emotion categories tested in distinct blocks. In Experiment 2, two groups of 32 participants performed the same task as in Experiment 1a while exposed to partial facial expressions composed of actions units (AUs) present or absent in some parts of the face (top, middle, or bottom). The coding of the AUs produced by the models showed complex facial configurations for most emotional expressions, with several AUs in common. Eye-tracking data indicated that relevant facial actions were actively gazed at by the decoders during both accurate recognition and errors. False recognition was mainly associated with the additional visual exploration of less relevant facial actions in regions containing ambiguous AUs or AUs relevant to other emotional expressions. Finally, the recognition of facial emotions from partial expressions showed that no single facial actions were necessary to effectively communicate an emotional state. In contrast, the recognition of facial emotions relied on the integration of a complex set of facial cues.

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.