Karine Durand

During infant development, intersensory facilitation declines gradually as unisensory perception improves. However, this developmental trade-off has been mainly investigated using audiovisual stimulations. Here, fifty 4- to 12-month-old infants were tested 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, results revealed a face-selective electroencephalographic (EEG) 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 gradually with age, indicating an inverse relation with the strength of the sole visual response, and generalizing to olfactory-visual interactions previous evidence from the audiovisual domain.

Visual categorization is the brain ability to rapidly and automatically respond to widely variable visual inputs in a category-selective manner (i.e., distinct responses between categories and similar responses within categories). 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 9 ^th 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 is generally considered as poorly functional in humans, is well placed to disambiguate visual information.

Significance: The adult human brain is organized in unimodal regions responding selectively to categories of environmental sensory stimuli. Here, we document the origin of category-selective visual brain responses in infancy, demonstrating the key contribution of other senses. Visual categorization is recorded neurally in 4-mo-old infants presented with rapid trains of natural images of nonface objects. A concurrent maternal odor initiates the neural response to periodically presented face-like objects categorized as faces in the specialized right hemisphere. This observation provides invaluable clues to understand how the developing visual system builds upon multisensory experience to start categorizing ambiguous and complex unimodal sensory inputs.

Objectives: Colostrum is the initial milk secretion which ingestion by neonates warrants their adaptive start in life. Colostrum is accordingly expected to be attractive to newborns. The present study aims to assess whether colostrum is olfactorily attractive for 2‐day‐old newborns when presented against mature milk or a control.Methods: The head‐orientation of waking newborns was videotaped in three experiments pairing the odors of: (a) colostrum (sampled on postpartum day 2, not from own mother) and mature milk (sampled on average on postpartum day 32, not from own mother) (n tested newborns = 15); (b) Colostrum and control (water; n = 9); and (c) Mature milk and control (n = 13).Results: When facing the odors of colostrum and mature milk, the infants turned their nose significantly longer toward former (32.8 vs 17.7% of a 120‐s test). When exposed to colostrum against the control, they responded in favor of colostrum (32.9 vs 16.6%). Finally, when the odor of mature milk was presented against the control, their response appeared undifferentiated (26.7 vs 28.6%).Conclusions: These results indicate that human newborns can olfactorily differentiate conspecific lacteal fluids sampled at different lactation stages. They prefer the odor of the mammary secretion ‐ colostrum ‐ collected at the lactation stage that best matches the postpartum age of their own mother. These results are discussed in the context of the earliest mother‐infant chemo‐communication. Coinciding maternal emission and offspring reception of chemosignals conveyed in colostrum may be part of the sensory precursors of attunement between mothers and infants.

Little is known about the effects of olfaction on visual processing during infancy. We investigated whether and how an infant's own mother's body odor or another mother's body odor affects 4‐month‐old infants’ looking at their mother's face when it is paired with a stranger's face. In Experiment 1, infants were exposed to their mother's body odor or to a control odor, while in Experiment 2, infants were exposed to a stranger mother's body odor while their visual preferences were recorded. Results revealed that infants looked more at the stranger's female face in presence of the control odor but that they looked more at their mother's face in the context of any mother's body odors. This effect was due to a reduction of looking at the stranger's face. These findings suggest that infants react similarly to the body odor of any mother and add to the growing body of evidence indicating that olfactory stimulation represents a pervasive aspect of infant multisensory perception.

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 vs. 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.

To interact with an unlabeled rich visual world, the human developing brain learns to differentiate visual events and to generalize across some of them despite their physical variability. Although this perceptual categorization process has been traditionally investigated from a unisensory perspective, the early development of visual categorization is inherently constrained by multisensory inputs. In particular, the visual system being largely immature in infancy, early-maturing sensory systems such as olfaction are ideally suited to support and refine visual development. Odors are relevant cues for young infants providing stability and familiarity within a rapidly changing complex visual environment. Here we provide evidence that perceptual categorization of one of the earliest and most salient visual category for the young infant brain, human faces, is shaped by a familiar odor already learned in utero, the maternal odor. We recorded scalp electroencephalogram (EEG) from 18 four-month-old infants exposed to the maternal or a control odor condition during rapid 6 Hz stream of widely variable natural images, with faces inserted every 6^th image (i.e., at 1 Hz). We replicate the infant brain ability to categorize at a glance various faces embedded in a fast train of natural images, with a significant face categorization response at 1 Hz over right posterior cortical regions (de Heering & Rossion, 2015). Strikingly, this visual categorization response is enhanced by concomitant maternal odor inputs, with every single infant brain showing a larger face categorization response in the maternal odor context. The lack of difference between odor conditions for the 6 Hz visual response common to all images excludes a mere enhancement of visual attention in the maternal odor context. Overall, these observations support a multisensory view of category learning and have important implications for our understanding of the development of perceptual categorization in the human brain. Meeting abstract presented at VSS 2018

The Cambridge Encyclopedia of Child Development - edited by Brian Hopkins October 2017