Humans are inclined to perceive conspecifics

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Which neural mechanisms could subtend the odor effect?

In line with the role of intersensory congruency in perceptual development (Bahrick and Lickliter, 2000), the repeated co-occurrence of odor and visual cues in the social niche of the developing infant could increase the likelihood of a face in the visual environment when the infant smells a (maternal) body odor. At the neural level, this would be reflected by a strengthened connectivity between the olfactory and visual systems through reentrant signaling (Edelman, 1993), such that maternal odor would be able to pre-activate face-selective regions in the ventral visual pathway, thereby tuning their responsiveness when a face(like) visual input appears. This interpretation is consistent with findings in adults showing that body odors alone activate the lateral fusiform gyrus (Zhou and Chen, 2008), a well-known category-selective visual region, and downstream recipient of the primary olfactory cortex (Zhou et al., 2019). This is more broadly in line with a large-scale connectivity between distinct ―unisensory‖ brain regions dedicated to the same semantic domain (Mahon and Caramazza, 2011). Interestingly, it has been recently shown that the functional layout of the category-selective occipito-temporal cortex can be constrained by auditory inputs in people who are born blind (Mattioni et al., 2020). In this context, we are tempted to speculate that this mechanism also applies in infancy because face-selective regions are too immature to readily categorize face(like) stimuli from the sole visual input. Despite the difficulty of setting neuroimaging studies with young infants, recent advances in this endeavor (Deen et al., 2017; Kamps et al., 2020) offer a promising avenue for the future investigation of the mechanisms at stake in odor-driven category-selective neural responses.
It is worth noting that intersensory effects in the infant brain are not limited to social information (Werchan et al., 2018), and evidence obtained in adults shows that non-social odor cues actively modulate visual perception (Hörberg et al., 2020; Seigneuric et al., 2010; Zhou et al., 2010). However, social stimuli are arguably the most relevant and familiar cues in early development, in both visual (Fausey et al., 2016) and olfactory (Schaal et al., 2020) domains. This makes social information the best candidate to evidence potent intersensory effects during the first months of life, and, more generally, to demonstrate that the developing brain takes advantage of multisensory inputs for category acquisition. In this regard, one could inquire whether body odors that do not belong to the infant‘s own mother would be able to shape face(like) categorization. Body odors are mixtures of cues conveying nested information about people and their internal states (de Groot et al., 2017), and which influence on the perception of congruent facial information has been described in adults (Kamiloğlu et al., 2018; Wudarczyk et al., 2016). However, previous infant studies investigating this question have used maternal odors for their powerful effectiveness on infant behavior and cognition (Durand et al., 2020, 2013; Jessen, 2020; Leleu et al., 2020; Rekow et al., 2020b). Whether and how different ―social chemosignals‖ interact with face perception in infancy is yet to be explored.

Moving to adulthood

Altogether, these three studies have first confirmed the impressive ability of infants to rapidly process information in order to categorize objects independently of their viewpoint, exposure, stimulus-driven specificities. Importantly, we have also described to what extent maternal odor influences visual categorization in early infancy: in the form of a congruent intersensory association, particularly effective when visual processing appears challenging. Indeed, maternal odor, a reliable and almost omnipresent cue in the sensory bubble of the young infant (Schaal and Durand, 2012), embodies a powerful role in bonding early in life (Schaal et al., 2020), and previous studies have evidenced its apparent effect on visual behavior in neonates (Doucet et al., 2007) and young infants (Durand et al., 2020, 2013). We here reveal the maternal odor effect on visual categorization in individual infant brains, shaping the categorization of visual information provided it bears congruency, here the social dimension brought by the face – admittedly one of the most relevant visual object for infants.
These observations take root in a broader mechanism of multisensory integration, whereby concurrent sensory inputs contribute to a common representation (Ernst and Bülthoff, 2004), and are thus not limited to social (face) categories associated with (maternal) body odor, selected for their relevance in early stages of development. Moreover, by revealing that the odor effect was the strongest when the baseline response was the lowest at the individual level, our findings strongly suggest an inverse effectiveness mechanism on perceptual abilities, at stake in early stages of cognitive development (Bahrick and Lickliter, 2012; Holmes, 2007).
Considering that face knowledge and abilities is rapidly growing during the first months, that adults are reputed face experts, but that literature still report several cases in which odor effects on adult visual perception is observable, how could body odor effect over face categorization manifest with development?
On the ―short term‖ of cognitive development, we predict that maternal odor will gradually loose its effect along with 1) the maturation of the visual system and the development of face perception abilities in the visual realm; 2) motor development bringing forth a new relationship to other individuals (more distal and less oriented toward the face, e.g., Fausey et al., 2016) and 3) the fading of the physiological changes characterizing the ―maternal‖ quality of the mother‘s body odor. These elements will be further discussed in the perspective section (part VIII), supported by preliminary data from older infants (4-to-12-month-olds).
In adults, the rationale is that odors could have an effect on visual categorization provided the neural response is not saturated. If it were, the odor effect would become measurable by increasing the difficulty of the task, i.e., ensuring the neural response can be enhanced. A proposition on tackling this issue is presented in Study 4, corresponding to chapter two.

Odors still exert a tuning function on visual categorization for the adult visual system

In adults, scientific knowledge about visual categorization is much advanced as compared to that of infants, especially using the FPVS-(i)EEG approach. In addition to faces, the neural signature to houses (scalp: Jacques et al., 2016a; iEEG: Hagen et al., 2020), body parts (Jacques et al., 2016a) and facelike objects (Rekow et al., in prep., Appendix 5), were also isolated and quantified.
This last study combines the three infant studies into one, with some adaptations. Instead of maternal odor, we used adult body odor, sampled from unfamiliar individuals (i.e., axillary sweat, see Methods and Appendix 6: Supporting information of Study 4, for more details). It was implicitly diffused alternatively with another odorant (i.e., gasoline) and a baseline odor (i.e., scentless mineral oil) during the visual stimulation, which consisted in all three visual categories (faces, cars, facelikes, same material as in Study 1 to 3), alternated across sequences. How can odor help in categorizing these categories, considering that the typical adult visual system is extremely efficient?
Interestingly, adults are not equal at face pareidolia and individual differences are often reported. This is due to the intrinsic ambiguity of the illusory face to be perceived from a common object. It represents an interesting challenge for the visual system, since the source of the illusion is a proper object, and face pareidolia corresponds to a dominant face bias. Therefore, the facelike category can be described as ambiguous and could thus constitute an interesting category to investigate the odor effect in adults, since face pareidolia is not systematic despite a mature and typically efficient visual system.

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Procedure d.

EEG was recorded in a sound and light-attenuated cabin equipped with an air-vacuum. To reduce additional olfactory noise, the non-smoker experimenter used scentless soap and avoided consuming coffee, tea, or any odorant product prior to testing. In the cabin, participants were seated at a 57-cm distance from the screen with their head on a chinrest. The screen (24-inch LED) displayed images with a refresh rate of 60 Hz and a resolution of 1920 × 1080 pixels on a uniform grey background (i.e., 128/255 in greyscale). To diffuse the odorants, we used an odor-delivering device adapted from previous studies (Leleu et al., 2015b; Poncet et al., 2021). The three odor flasks were connected to a device delivering a constant flow of scentless air originating from a tank of pressured air purified by charcoal filters and set at room temperature. The airflow was delivered at an undetectable pressure (i.e., 0.5 bar) to avoid the mechanical sensation of air on the skin and to ensure unawareness of olfactory stimulation throughout the experiment. The airflow was directed to one of the three flasks by a hand-activated valve from where a tube was connected to the chinrest to diffuse odors directly under the nose of the participants in the cabin. The flasks and the odor diffusing system were hidden from the participants.
We used a fast periodic visual stimulation (FPVS) coupled with an EEG frequency-tagging approach (Norcia et al., 2015) to measure rapid (i.e., single glance) and automatic (i.e., without explicit intention) visual categorization in the brain. The design was adapted from previous studies which successfully isolated visual categorization responses at different levels of brain organization in adults (e.g., Gao et al., 2018; Hagen et al., 2020; Jacques et al., 2016a), and infants (de Heering and Rossion, 2015; Leleu et al., 2020; Rekow et al., 2020b, in revision). Base objects were presented without inter-stimulus interval at a rapid 12-Hz base rate (i.e., 12 images / second, ≈ 83 ms per image, Figure V-1B) and images of either human faces, cars, or facelike objects (one target category per sequence) were periodically interspersed every 9th stimulus, corresponding to a category-selective rate of 1.33 Hz (i.e., 12 / 9; 750 ms between each category exemplar). Thanks to this frequency-tagging approach, we isolate two distinct brain responses in the EEG frequency spectrum: (1) a general visual response at 12 Hz and harmonics (i.e., integer multiples) elicited by the information rapidly changing 12 times per second (e.g., local contrast) and (2) a category-selective response at 1.33 Hz and harmonics reflecting the visual categorization of the target category. The latter response is elicited by populations of neurons that selectively respond to this category in the VOTC (Gao et al., 2018; Hagen et al., 2020; Jonas et al., 2016).

Table of contents :

I. Through a multisensory journey
A. Making sense of our senses
1. An adaptive perceptual experience
2. Categorization as a perceptual tool
3. The role of context
B. Sensory development
1. Neuro-anatomy and neuro-functionality of olfaction
2. Neuro-anatomy and neuro-functionality of vision
3. Differences in sensory functions
C. Multisensory integration
1. Views on multisensory perceptual development in infancy
2. Subtending mechanisms
3. Theoretical perspectives
II. Humans are inclined to perceive conspecifics
A. Conspecifics in the visual realm: seeing faces
1. Generic face categorization
Behavioral evidence for the categorization of faces
Brain activity corresponding to face categorization
A recent approach to measure direct, automatic and implicit face categorization
2. Neural architecture subtending face perception Dedicated pathways
A right hemispheric specialization for face perception
B. Conspecifics in the chemical realm: body odor
1. Body odor production
2. Perceiving body odor
Particularities of maternal odor
Pre- and post-natal perception of maternal odor
From childhood to adolescence
In adulthood
3. A dedicated neural network subtending body odor processing
III. Body odors and faces intertwined
A. What your nose tells your eyes when you see faces
1. In adulthood
2. In infancy
B. Hypotheses, prediction and proposed methodology
1. Mechanisms and hypotheses
2. Methodological considerations
Chapter one
IV. Delineating the maternal odor influence over visual categorizations in the developing brain Study 1: Maternal odor shapes rapid face categorization in the infant brain
Abstract
1. Introduction
2. Materials and Methods
Participants
Visual stimuli
Odor stimuli
Procedure
EEG recording and analysis
3. Results
Rapid face categorization in the infant brain
Maternal odor shapes the neural signature of face categorization
Common visual processes elicited by all images are immune to maternal odor influence
4. Discussion
Study 2: Categorization of objects and faces in the infant brain and its sensitivity to maternal odor: further evidence for the role of intersensory con
Abstract
1. Introduction
2. Materials and methods
Participants
Visual stimuli
Odor stimuli
Procedure
EEG recording and preprocessing
Frequency-domain analysis
3. Results
Car categorization and general visual responses in the 4-month-old infant brain No effect of maternal odor on both car categorization and general visual responses Maternal odor effect on the visual categorization of cars and faces
4. Discussion
Study 3: Smells like real faces: odor-driven categorization of illusory faces in the infant brain
Abstract
1. Introduction
2. Materials and methods
Participants
Visual stimuli
Odor stimuli
Design and procedure
EEG recording and analysis

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