Abstract
While humans are usually considered as overly visual, human vision is poor at the beginning of life. In contrast, olfaction is an early-developing sense that promotes adaptive responses and may support visual development. Accordingly, this chapter reviews recent studies that we conducted showing that the mother’s body odor selectively facilitates face categorization in the 4-month-old human brain. We also reveal that as infants grow up, their ability to categorize faces improves until 12 months of age and becomes progressively independent of the influence of maternal odor. We open with findings in adults, demonstrating that odor-driven visual categorization is still observed for ambiguous stimuli, aligning with the inverse effectiveness principle of multisensory integration. Overall, this body of research exposes the powerful impact of odors on visual categorization, especially how social chemical cues emanating from the mother can drive the categorization of conspecifics from visual inputs in the developing human brain. These findings suggest that odors act as disambiguating cues fostering visual categorization as an inverse function of its effectiveness and point toward a critical role of multisensory inputs for the acquisition of categories in humans, relying on the ordered development across the senses.
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Notes
- 1.
ERPs suffer from a low signal-to-noise ratio and are constrained by their sensitivity to (e.g., muscular) artifacts in awake infant studies. ERPs also use post-hoc subtraction between absolute brain responses to transient stimuli, such that face-selective neural activity is indirectly obtained and can be masked by large noise in the subtracted responses, or driven by a subset of stimuli. In addition, the time-windows of ERP components are often difficult to define objectively from brain responses that are heterogenous in terms of shape, latency and polarity across individuals and age groups. Finally, ERP studies generally use a limited set of homogenous and edited stimuli (i.e., segmented from their natural background with identical exposure conditions across category exemplars; see footnote 2), and compare faces to only a few nonface categories.
- 2.
Naturalistic stimuli depict the main item of each stimulus embedded in the original background the photography was taken in, without controlling for viewpoints, luminance, contrast, colors, etc. This is opposed to edited (sometimes referred to as standardized) stimuli which are commonly used in visual experiments, where the item is isolated from its background and generally homogenized across the different exemplars to control for inter-stimulus variability.
- 3.
It should be also noted that with frequency-tagging EEG, infants are tested under the same conditions and using the same stimuli as for adults, making infants’ data comparable to that of adults but increasing categorization difficulty at such an early stage of development. The maternal odor effect could thus have been also favored by this demanding paradigm for their immature visual system. More generally, one may question the ecological validity of our paradigm since infants rarely see faces so rapidly in their everyday experience. However, while slower modes of visual display better match the natural timing of exposure to a conspecifics’ face, they are rather limited in terms of measurement validity, especially for visual categorization, as they often rely on a limited set of edited visual stimuli depicting only a few visual categories (see Sect. 2.1 for a discussion of this issue; see also Kominsky et al., 2022, for a recent discussion about the difficult balance between ecological and measurement validity in infant research). Moreover, as mentioned above, we aimed to investigate the development of face categorization using adult performance as reference. Neurotypical adults reach a plateau for categorizing natural views of faces after only a short exposure of about 80 ms (≈ 12 Hz of fast periodic visual stimulation; see e.g., Retter et al., 2020). Hence, despite its limitations in ecological terms, our paradigm is well designed to measure the development of adult-like rapid face categorization in the infant brain. Admittedly, future studies should investigate odor-driven visual categorization in other experimental and/or natural designs to further improve the generalizability of our findings.
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Acknowledgments
The studies presented in this chapter have received financial support from the Centre National de la Recherche Scientifique (CNRS), the “Conseil Régional Bourgogne Franche-Comté” (PARI grant), the FEDER (European Funding for Regional Economic Development), the French ‘Investissements d’Avenir’ program, project ISITE-BFC (contract ANR-15-IDEX-03) and the French National Research Agency (contract ANR-19-CE28-0009). The authors wish to thank the co-authors of the original papers of the studies described here (in alphabetical order: J.-Y. Baudouin, F. Damon, K. Durand, F. Poncet, B. Rossion & B. Schaal), along with Sylviane Martin for her help in recruiting participants and Vincent Gigot for his assistance in preprocessing the EEG signals.
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Rekow, D., Leleu, A. (2023). Tips from the Nose: Odor-Driven Visual Categorization in the Developing Human Brain. In: Schaal, B., Rekow, D., Keller, M., Damon, F. (eds) Chemical Signals in Vertebrates 15. CSiV 2021. Springer, Cham. https://doi.org/10.1007/978-3-031-35159-4_18
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