Olfactory facilitation of visual categorization in the 4-month-old brain depends on visual demand.

To navigate their environment, infants rely on intersensory facilitation when unisensory perceptual demand is high, a principle known as inverse effectiveness. Given that this principle was mainly documented in the context of audiovisual stimulations, here we aim to determine whether it applies to olfactory-to-visual facilitation. We build on previous evidence that the mother's body odor facilitates face categorization in the 4-month-old brain, and investigate whether this effect depends on visual demand. Scalp electroencephalogram (EEG) was recorded in two groups of 4-month-old infants while they watched 6-Hz streams of visual stimuli with faces displayed every 6th stimulus to tag a face-selective response at 1 Hz. We used variable natural stimuli in one group (Nat Group), while stimuli were simplified in the other group (Simp Group) to reduce perceptual categorization demand. During visual stimulation, infants were alternatively exposed to their mother's versus a baseline odor. For both groups, we found an occipito-temporal face-selective response, but with a larger amplitude for the simplified stimuli, reflecting less demanding visual categorization. Importantly, the mother's body odor enhances the response to natural, but not to simplified, face stimuli, indicating that maternal odor improves face categorization when it is most demanding for the 4-month-old brain. Overall, this study demonstrates that the inverse effectiveness of intersensory facilitation applies to the sense of smell during early perceptual development. RESEARCH HIGHLIGHTS: Intersensory facilitation is a function of unisensory perceptual demand in infants (inverse effectiveness). This inverse relation between multisensory and unisensory perception has been mainly documented using audiovisual stimulations. Here we show that olfactory-to-visual facilitation depends on visual demand in 4-month-old infants. The inverse effectiveness of intersensory facilitation during early perceptual development applies to the sense of smell.

Olfactory-to-visual facilitation in the infant brain declines gradually from 4 to 12 months.

During infancy, intersensory facilitation declines gradually as unisensory perception develops. However, this trade-off was mainly investigated using audiovisual stimulations. Here, fifty 4- to 12-month-old infants (26 females, predominately White) were tested in 2017-2020 to determine whether the facilitating effect of their mother's body odor on neural face categorization, as previously observed at 4 months, decreases with age. In a baseline odor context, the results revealed a face-selective electroencephalographic response that increases and changes qualitatively between 4 and 12 months, marking improved face categorization. At the same time, the benefit of adding maternal odor fades with age (R2 = .31), indicating an inverse relation with the amplitude of the visual response, and generalizing to olfactory-visual interactions previous evidence from the audiovisual domain.

Voice categorization in the four-month-old human brain.

Voices are the most relevant social sounds for humans and therefore have crucial adaptive value in development. Neuroimaging studies in adults have demonstrated the existence of regions in the superior temporal sulcus that respond preferentially to voices. Yet, whether voices represent a functionally specific category in the young infant's mind is largely unknown. We developed a highly sensitive paradigm relying on fast periodic auditory stimulation (FPAS) combined with scalp electroencephalography (EEG) to demonstrate that the infant brain implements a reliable preferential response to voices early in life. Twenty-three 4-month-old infants listened to sequences containing non-vocal sounds from different categories presented at 3.33 Hz, with highly heterogeneous vocal sounds appearing every third stimulus (1.11 Hz). We were able to isolate a voice-selective response over temporal regions, and individual voice-selective responses were found in most infants within only a few minutes of stimulation. This selective response was significantly reduced for the same frequency-scrambled sounds, indicating that voice selectivity is not simply driven by the envelope and the spectral content of the sounds. Such a robust selective response to voices as early as 4 months of age suggests that the infant brain is endowed with the ability to rapidly develop a functional selectivity to this socially relevant category of sounds.

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.

Smell what you hardly see: Odors assist visual categorization in the human brain.

Visual categorization is the brain ability to rapidly and automatically respond to a certain category of inputs. 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 has long been considered as poorly functional in humans, is well placed to disambiguate visual information.

Rapid neural categorization of facelike objects predicts the perceptual awareness of a face (face pareidolia).

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.

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.

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.

An ecological measure of rapid and automatic face-sex categorization.

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.

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.

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.