Nasal Chemoreception

The strongest evidence for human prenatal olfactory function comes from studies on newborns in which the odor of amniotic fluid,1 or of flavor compounds (e.g., anise, alcohol, carrot) transferred into it, induce appetitive responses in the newborn.2,3 Thus, from late gestation, the human fetus is able to detect, selectively encode, and retain some odor information in the womb. Near-term fetuses may be as competent as neonates. Sarnat,4 however, found that the proportion of premature newborns detecting mint odor at birth (assessed by sucking or arousal responses) was related to gestational age. While most infants born between 29 and 36 weeks’ gestation responded, less predictable reactions arose before week 29. After gestational week 32, infants born prematurely responded to the mint odor equally to infants born at term. Near-infrared spectroscopy also showed that preterm infants aged 33.7 gestational weeks (tested 12.5 days post birth) evince differential cortical hemodynamic variations when exposed to the odor of colostrum or vanilla or to trigeminal stimuli carried in disinfectants or detergents: after 10 seconds of stimulation, an increase or decrease, respectively, was noted in oxygenated hemoglobin over the parietal region.5

Oral Chemoreception

Taste buds of all types are evident as early as gestational week 10, and by the end of gestational month 4 receptor cells become accessible to potential stimuli through open taste pores. Human fetal responses to sapid agents infused in utero remain equivocal, but functional taste has been established in infants born preterm within gestational months 6 to 9. Sweet, bitter, or acid tastants elicit responses indicating that, from early gestational month 6, taste buds are connected with the central systems controlling behavioral and autonomic (salivation) responses. Sweet solutions lead to mouthing/sucking and positive hedonic responses (sucking, calming, facial expression indicating acceptance) in preterm infants, whereas bitter, acid, and salty stimuli tend to inhibit these responses or do not affect them (e.g., ref. 6).

Nasal Chemoreception

When tested within 12 hours after birth and before any postnatal ingestion, odorants chosen to be pleasant or unpleasant to adults (banana, vanilla, and milky odorants versus fishy and rotten odorants, respectively) elicited typical facial responses.7 When photographs of these responses were evaluated by an adult panel for their hedonic meaning, the odors considered pleasant induced expressions of acceptance (relaxed face, rising mouth corners, licking, sucking), while unpleasant odors provoked rejection expressions (lowering mouth corners, lip/tongue protrusion, gaping) ( Fig. 10.1 ). As one anencephalic newborn reacted with similar facial expressions to odors as normal infants, an “innate” brainstem mechanism controlling hedonic facial reactivity was proposed, and termed the olfactofacial reflex.7 However, it was later shown that prenatal experience with odorants can strongly bias such neonatal responses,3 casting doubt on the innate nature of the “reflex”.

* The human neonatal period is generally considered as extending from birth to the first month.

Oral Chemoreception

Taste stimuli are well discriminated by term-born newborns. Facial and oral movements expressing acceptance (sucking, relaxed and “smiley” face, eye opening, hand–mouth contact) are elicited by water solutions of sweet tastants (sucrose, lactose, or saccharin), or by monosodium glutamate (savory) administered in a soup. In contrast, facial–oral responses expressing avoidance (grimaces, crying, gaping, eye closure) occur with acid and bitter tastants, while salty solutions remain hedonically ambiguous during the first postnatal months.7 Reactivity measured by comparing differential ingestion from bottles containing various taste solutions against a reference bottle (generally water) provided less convincing data, probably because the sucking drive over-rides taste regulation of intake at this early age. While the acceptance for sweet solutions remained, infants consumed salt and bitter (urea) solutions as much as water, suggesting indifference to these latter tastants, while sour tastes were generally rejected.8 Taste can regulate infants’ activation states by inhibiting crying and facilitating calmness. The oral administration of sucrose activates mouthing/licking/sucking motions. This sweetness–calming link appears to fade out after 2 months of age, however.

Nasal Chemoreception

Owing to difficulties in compliance and in designing tests for preverbal children, our understanding of nasal chemosensation remains scanty between the ages of 1 month and 3 years. However, there is no a priori reason why nasal chemosensation should not function well over this period:

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  Below 3 years of age, reactivity to odors is attested by infants’ selective responsiveness to foods and persons9; between 3 and 4 years, rare studies indicate good odor detection abilities; and by age 5 children′s responses become accessible to more systematic psychophysical testing (see pp. 58–75).

  
  
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  The best evidence for infants’ and children′s olfactory responsiveness comes from studies on preferences and aversions, which suggest a generally greater tolerance to unpleasant odors before 5 years of age, and converging hedonic responses in children and adults.10 Early stability in categorizing odors as pleasant or unpleasant occurs, although considerable interindividual differences exist because of exposure and learning effects.

  
  
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  Sensitivity to trigeminal agents in infants and children under 5 years of age has not been clearly established.

  
  
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  Puberty is a period of change in sensitivity and hedonic rating for certain odorant qualities in or resembling body odors (e.g., steroids, musks); thus, boys become increasingly insensitive to androstenone with advancing puberty, while girls become more sensitive to it.11 However, this pubertal variation in olfactory sensitivity and preferences does not seem to affect food odorants.12

Oral Chemoreception

The sense of taste continues to mature until at least 8 years of age, and possibly into adolescence. Measurement of taste detection thresholds indicate that 8-year-old females, but not males, have similar detection thresholds to adults, and 6- to 10-year-olds require larger differences between the concentrations of a tastant to perceive a difference.13 In addition, 8-year-olds cannot perceive tastes in mixtures similarly to adults, and fail to detect both tastes in some two-component mixtures. Adults and children also differ in their taste preferences (e.g., higher levels of sourness are preferred by many children of this age, while 9- to 15-year-olds prefer higher salt concentrations than adults). These behavioral differences are accompanied by anatomical changes in 8-year-olds, with greater numbers of fungiform papillae per unit area occurring on the anterior tongue than in adults, which is reflected in higher taste sensitivity in localized areas of the tongue. Nevertheless, 8-year-olds and adults have similar response functions for suprathreshold sweet stimuli.

Arousal

Odors and tastes can markedly affect an infant′s activation state. Thus, between 2 and 10 days of age, upset infants become less agitated when exposed to the breast odor of a lactating mother, which can also counteract the hyperarousal elicited by acute pain. Attenuation of agitation is even more pronounced when the odors originate from the infant′s own mother.9

Directional Responses

Head orientation is a much used index of olfactory discrimination in infants. A two-choice test was developed that recorded supine newborns’ head-turning responses to two odor stimuli, hanging on each side of their faces.14 It demonstrated that 6-day-old infants spent more time turned toward their mother′s breast odor rather than to another mother′s breast odor. Infants were later shown to orient more insistently to the odor of milk from an unfamiliar woman rather than toward an unfamiliar odor of similar intensity.9 Odors can also motivate infants to crawl toward a distant odor source.

Stimulus Sampling Responses

Volitional sniffing remains poor in infants below 2 years of age, but their respiratory pattern is nevertheless affected by the hedonic nature of an odor. For example, newborns show accelerated and decreased respiratory rates, respectively, to vanilla and butyric acid.15 Maternal odor of very low intensity can also elicit specific patterns of respiration in newborns.16 Thus, infants tend to adjust their nasal airflow depending on whether it carries a pleasant/familiar or unpleasant/unfamiliar odorant. Maternal odors also stimulate oral (chewing) and lingual (licking, sucking) motions that favor stimulation by taste. Four-day-olds display increased oral responses to the odor of their mother′s milk than the odor of another mother′s milk, or when they perceive their amniotic fluid odor. Oral movements do, therefore, express an individual′s motivation to grasp the offered stimulus orally. In addition to the effects of odorants administered orthonasally, infants detect retronasal odorants during feeds, and modulate their ingestive decisions accordingly.17

Physiological Interactions

Odorants and tastants affect various responses controlled by the autonomic nervous system (i.e., heart and respiration rates, endocrine release).15 Conversely, the metabolic state influences infantile responses to odors. When 3-day-old, bottle-fed infants are exposed to the odor of their usual formula milk 1 hour before and 1 hour after a feed, they respond more negatively to it during the post-prandial than during the preprandial stage.18 This fluctuation in hedonic responsiveness of infants resembles the phenomenon of negative alliesthesia* described in adults, and is an important factor of variation to consider in the testing of olfactory or taste abilities.