Anyone who has observed infants for any period of time can testify to the intense activity occurring in and around their mouths-the primary site for learning in the first few months of life. Before they are even able to crawl, infants have learned much about their new sensory world. Through recent research we have begun to explore the impact of these early experiences on infants' acceptance of solid foods and how they explore objects in their environment. We have also begun to focus on the sensory experiences of the formula-fed infant, in particular, how their responses to particular formulas, which are extremely unpalatable to older children and adults, change during infancy. This is a relatively new and exciting area of study, with much research yet to be done. It is clear, however, that infants are not passive receptacles for flavored foods. Parents who offer a variety of foods will provide both a nutritious, well-balanced diet, as well as an opportunity for their children's own personal preferences to develop.
Introduction Anyone who has observed infants for any period of time can testify to the intense activity occurring in and around their mouths-the primary site for learning in the first few months of life. During feeding, or while mouthing objects such as their hands and toys, infants use the sense of touch to discriminate between textures, and the senses of taste and smell to discriminate flavors. Before they are even able to crawl, infants have learned much about their new sensory world.
When we first explored the topic of early flavor experiences in Pediatric Basics (No. 65, Summer 1993), we knew that the sensory world of the infant was different than that of older children and adults. We also knew infants had an ability to detect some tastes and not others, and that breast-fed infants experienced a variety of flavors in their mothers' milk.
Through recent research we have begun to explore the impact of these early experiences on infants' acceptance of solid foods and how they explore objects in their environment. We have also begun to focus on the sensory experiences of formula-fed infants, in particular, how their responses to particular formulas, which are extremely unpalatable to older children and adults, change. Before we discuss infants' early flavor experiences, we must establish a basic understanding of taste and smell, the differences between them, and how they interact and integrate to produce an overall impression of flavor. What Is Flavor? The "flavor" we experience while eating foods is a product of two frequently confused chemical senses: taste and smell. Taste refers to the sensation occurring when chemicals stimulate taste receptors on the tongue and other parts of the oropharynx (Figure 1). The taste stimuli that interact with these receptors are often separated into a small number of "primary" tastes: sweet, salty, bitter, sour, and perhaps savory, the taste of umami or monosodium glutamate.
Smell, on the other hand, occurs when chemicals stimulate olfactory receptors located on a relatively small patch of tissue in the nasal cavity. Unlike the sense of taste, there may be many different classes of odor stimuli, perhaps thousands. Odors can reach their receptors in two ways: they can enter the nostrils during inhalation (orthonasal route) or they can travel from the back of the nasopharynx toward the roof to the nasal cavity (retronasal route) during suckling in infants or chewing and swallowing in older children and adults (Figure 1).
Retronasal olfaction, the aroma of substances we put in our mouths, contributes significantly to the complexity of flavor. This is clearly noted by head cold sufferers who lose the ability to discriminate common foods when olfactory receptors are blocked. Similarly, foods often "taste" better after a person quits smoking perhaps because their sense of smell has improved, ' allowing them to detect more subtleties of flavor. The role of smell in flavor is critical in distinguishing the flavor of strawberry from cherry, and in enjoying foods containing licorice, vanilla, and citrus. It should be noted that other properties of food (e.g., texture, temperature, irritation) are also very important to its perceived flavor. However, little experimental work has been done in this area of infant flavor perception. Therefore, in this article we will focus on the infant's senses of taste and smell.
Developing Sensitivities and Preferences The sensory world of the young infant differs from that of the adult in that the infant's sense of taste develops over time. Specifically, sweet responses are evident prenatally, and major changes are not known to occur postnatally. Similarly, the rejection of sour taste is evidenced from birth onwards, although it is clear that children often come to like very sour substances. How this happens is not known. Salt and bitter sensitivities appear to change postnatally, and the limited research on umami taste suggests that preferences are evident during infancy, but the context in which the tastant is experienced is critical. Less is known about how olfactory perceptions and preferences change over time. Clearly, infants are able to detect and discriminate among a wide variety of odors shortly after birth. Although it is not yet known whether they hedonically respond to differences in odor quality, that is, which odors infants find pleasant, research has shown that newborns appear to be as sensitive to odors as adults, if not more so, and are capable of retaining complex olfactory memories.' When older, they will explore a scented toy differently than an unscented one and the way they respond to the scented toys is influenced by the amount of exposure they have had with that particular scent.3 These findings suggest that infants are able to detect and retain information about the chemical features of their environment. Fetus and Premature Infants Studies on Taste Although amniotic fluid and embryonic membranes provide a series of barriers that protect the fetus from disturbances from the outside world, the fetus is nonetheless exposed to a variety of chemosensory stimuli in utero. The composition of amniotic fluid varies over the course of gestation, particularly as the fetus begins to urinate. By term, the fetus is actively swallowing almost a liter of amniotic fluid a day and has been exposed to a variety of substances including glucose, lactic acids, urea, amino acids, proteins, and salts.4.5 The apparatus needed to detect these stimuli, the taste buds, make their first appearance around the 7th or 8th week of gestation, and by 13 to 15 weeks, they begin to resemble those of the adult.6 Based on anatomical studies and studies on other animal species, they are presumably functional by the third trimester. Studies on taste sensation in the preterm infant are rare, due in part to methodologic limitations. When preterm infants who had been fed exclusively via gastric tubes were presented with minute amounts of either glucose or water solutions intraorally, they exhibited more nonnutritive sucking in response to the glucose than the water.7 In another study using a methodology that embedded taste substances in a nipple-shaped gelatin medium,8 infants born preterm and tested between 33 and 40 weeks postconception produced more frequent, stronger sucking responses when offered a sucrose-sweetened nipple compared with a latex nipple. The results from these studies indicate that, prior to birth, the human infant possesses a sensory apparatus that can detect sweet tastes. Studies on Smell
New research also confirms that the environment in which the fetus lives-the amnion-is indeed odorous. The odor can indicate certain disease states (such as maple syrup disease,9 phenylketonuria,'0 and trimethylaminuria") or the types of foods eaten by the pregnant mother.'2 That the amniotic fluid and the newborn's body can acquire the odor of a spicy meal the mother ingested prior to giving birth suggests that odorous compounds in her diet can be transferred to the amniotic fluid. This has been experimentally demonstrated in a recent study in which amniotic fluid samples were obtained from pregnant women who were undergoing routine amniocentesis and who ingested either garlic or placebo capsules approximately 45 minutes before the procedure.'3 As expected, the odor of amniotic fluid obtained from the women who ingested the garlic, as determined by adult human evaluators, was judged to smell stronger or more like garlic than the amniotic fluid from the women who did not consume the garlic.
Because the normal fetus swallows significant amounts of amniotic fluid during the latter stages of gestation"4 and has open airway passages that are bathed in amniotic fluid,'5 the fetus may be exposed to a unique olfactory environment. Studies on other animals reveal that young and adult animals prefer certain odors that were experienced in utero. 6 Whether similar mechanisms are operating in humans remains unknown. However, a recent study revealed that newborns can detect the odor of amniotic fluid and that they prefer the odor of their own amniotic fluids for at least the first few days of life."s Newborns
Studies on Taste
Facial expressions, which suggest contentment and liking or discomfort and rejection, have been used to assess the newborn's responsiveness to taste stimuli in some of the earliest investigations on human taste development (Figure 2). During the first few hours of life, infants display relatively consistent, quality-specific facial expressions when the sweet tastes of sucrose (facial relaxation, followed by positive mouth gaping), the sour taste of concentrated citric acid (lip pursing and facial grimace), and the bitter taste of concentrated quinine and urea (tongue protrusion and grimace) are presented into the oral cavity.'W2' No distinct facial response is evidenced with salt taste, however. Infants also display distinct positive facial expressions, similar to those observed with sweetness, when tasting soup to which monosodium glutamate (MSG) has been added when compared to the soup diluent alone.zz MSG alone does not appear to elicit those facial responses, however, raising the question of exactly what it is about the MSG-flavored soup that is preferred. Intake studies, which compare how much an infant consumes of a taste solution and a diluent solution during brief presentations, are the most frequent method used to evaluate taste preferences. Generally, intake studies use weaker concentrations of taste stimuli than studies on facial expressions. If an infant ingests more of the taste solution than a diluent, for example, one can infer that (a) the infant can detect the taste and, with less certainty, (b) the infant prefers or likes the tastant more than the diluent.
Consistent with the findings for premature infants, research has repeatedly demonstrated strong acceptance of sweet-tasting sugars by newborn infants. Within days after birth, infants are quite sophisticated sweet connoisseurs. They can detect even dilute sweet solutions and can differentiate varying degrees of sweetness and different kinds of sugars.23 In addition, as was the case for premature infants, newborns will suck more in response to sweet stimuli.s*zq It is of interest to note that one of the most predominant taste qualities of the first food of all mammals, mother's milk, is its sweetness. In addition to a preference for sweet tastes, infants also show physiologic responses to them. A small amount of a sweet-tasting liquid placed on the tongue of a crying newborn exerts a rapid, calming effect which persists for several minutes.25"26 The rapid onset of analgesia, which has been observed during such painful procedures as blood sampling and circumcision, suggests that afferent signals from the mouth, rather than gastric or metabolic changes, are responsible for such effects. In contrast to the innate preference for sweet tastes, newborns reject the sour taste of citric acid." Because only a handful of studies on sour tastes have been conducted with newborn infants, it is not known whether there are developmental changes in sensitivity or preference for sour-tasting fluids.
Conclusions regarding the neonate's response to bitter and salty tastes are more problematic and further research is needed. Newborns respond with highly negative facial expressions to concentrated quinine and urea (Figure 2), but they do not reject moderate concentrations of urea.21 The reason for this difference remains unclear. Perhaps the newborn can detect bitter substances, but the ability to reject a substance or modulate intake will come as the infant matures. With regard to salt taste, studies measuring intake and facial expressions suggest that the newborn infant is indifferent to and may not detect salt. However, salt does appear to suppress some parameters of sucking in newborns. No studies suggest that the taste of salt is attractive to the newborn infant, however. Although each measure has its limitations, the convergence of research findings supports the conclusion that the ability to detect sweets is evident very early in human development and that its hedonic tone-that is, its pleasantnessis also well developed at birth. It is likely that the innate preference for sweets and rejection of bitter tastes in humans is a consequence of selection, favoring animals who consumed high-energy, vitamin-rich fruit and vegetable diets, while avoiding bitter, poisonous fruits and plants. Although the preference for sweet tastes appears to be innate and persists throughout childhood, experience may also play an interacting role in development. However, contrary to popular beliefs, there is no scientific evidence in humans that variations in early exposure to sweets permanently alter the preference for sweet-tasting foods.za Studies on Smell
Odor preferences in newborns are more difficult to assess. However, we do know that, shortly after birth, human infants are able to detect a wide variety of odors, with perhaps the most salient of these odors originating from the mother. Within hours after birth, mothers and infants can recognize each other through the sense of smell alone. Day-old breast-fed infants spend more time orienting toward a breast pad previously worn by their lactating mothers than one worn by an unfamiliar lactating woman.231 They move their head and arms less, suck more, and cry less when they are exposed to their mother's odors.32 33
This ability of breast-fed infants to discriminate the odors of their mothers from those of other lactating women is not limited to odors emanating from the breast region, since they can also discriminate odors originating from their mother's underarms and neck. Interestingly, newborns preferred their mother's breast unwashed as compared to when it had been thoroughly washed and thereby less odorous.34 Before the sense of sight is well developed, the recognition and preference for mother's odors may play an early role in guiding the infant to the nipple area and facilitating early nipple attachment and breast feeding.
Because bottle-fed infants do not discriminate their mothers' odors from those of an unfamiliar bottle-feeding mother,332 it has been suggested that breast-fed infants are able to discriminate these odors because they, unlike bottle-fed infants, have prolonged periods of skin contact with their mothers and their nostrils are in close proximity to their mother's breasts and underarms during feeding. Recent studies, however, suggest that bottle-fed infants also prefer the breast odors of unfamiliar, lactating women.35 Therefore, breast odors, or the volatile components of breast milk, may be particularly attractive to all newborns.
Older Infants Studies on Taste
Babies beyond the neonatal period (one to 24 months) have been most neglected in studies on taste. Nonetheless, a few notable findings suggest that changes in taste responses occur during this time in development.
While newborns rejected concentrated bitter-tasting solutions (urea), more recent studies revealed that relatively low concentrations of urea were not rejected in newborn infants, but rejection was evident among infants who were 14 to 180 days of age.36 This is consistent with the idea that there is an early developmental change in bitter perception or the ability to regulate the intake of bitter solutions. As a practical matter, it could explain why older infants reject bitter-tasting foods, like green vegetables. Parents can expect a "learning period" when introducing these foods, and anticipate a need to introduce them slowly, but consistently. With exposure, eventually these foods may be tolerated and even enjoyed. Developmental shifts in salt acceptability have also been demonstrated in several research studies. While newborn infants are indifferent to or reject salt relative to plain water, the preference for salt water relative to plain water first emerges at approximately 4 months of age.37 Experience with salty tastes does not appear to play a major role in this shift from indifference or rejection of salt at birth to acceptance in later infancy.37 Rather, this change in response may reflect postnatal maturation of central and/or peripheral mechanisms underlying salt taste perception, as has been demonstrated in animal model studies.38 Thus, the preference that emerges at 4 months appears to be largely unlearned.
Research has also revealed that young children undergo another developmental shift in their preference for salt taste. By 18 months of age, children begin rejecting salted water and become more adult-like in their preferences; they begin exhibiting robust preferences for salt in soup and other foods such as carrots or pretzels.39 In other words, the same level of saltiness may elicit either a positive or negative response depending on the medium in which salt is presented to the child. These studies underline the importance of sensory context in perceived pleasantness and preference. Early Experience and Preference for Salt Taste Although there is no evidence that high salt intake in infancy influences later preferences, there are data suggesting that the opposite is true. Several human studies have been conducted and were stimulated by a series of animal model studies that demonstrated that early alterations in sodium balance alter long-term salt preference behavior.38'o Rat pups whose mothers were severely saltrestricted during an early period of gestation have altered sensitivity, both behaviorally and electrophysiologically, when tested at various times after birth.40
In the human studies, the adult offspring (college students) of mothers who experienced considerable morning sickness during their pregnancies had greater salt preferences compared with students whose mothers suffered little or no morning sickness.41 The authors suggest that morning sickness leads to transient fluid and sodium depletion in a manner analogous to sodium depletion reported in the animal model studies. Consistent with these findings, 12- to 14-year-old children who had been erroneously fed a chloride-deficient formula during infancy had heightened preference for salty (but not sweet) food relative to their unexposed siblings.42 Because chloride deficiencies mimic sodium deficiencies in some ways (e.g., altered hormonal profile), this finding is consistent with the hypothesis that early sodium depletion leads to heightened preferences many years later. Studies on Smell
During the past decade, research at Monell has focused on the early olfactory experiences of the human infant, using mother's milk as the medium for these experiences. Our research revealed that human milk, like the milk of other animals, is indeed rich in flavors43 which directly reflect the foods and spices (e.g., garlic, mint, vanilla, carrot) eaten by the mother. The breast-feeding infant's ability to detect the sensory changes in the mother's milk is suggested by the infant's altered suckling behavior when the milk is flavored, that is, the infant feeds longer and sucks more overall when the milk is flavored with either garlic or vanilla.44"45 The mouth movements made during suckling may facilitate the retronasal perception of the volatiles in the milk, enhancing the infant's ability to "taste" the change. Moreover, experience with a flavor in mother's milk modifies how that infant responds to that flavor during subsequent feedings. Interestingly, formulafed infants responded in a similar manner when we added the flavor of vanilla to their formula; they sucked more during their initial exposure to the flavor, but this response diminished after repeated exposures.45
The flavor world of breast-fed infants is potentially much richer than previously thought. Because the chemical senses are not only functioning during infancy, but change during development, breast-fed infants may be afforded an opportunity to learn about the flavor of the foods of their people long before solids are introduced. Alcohol and Breast Feeding
The flavor of human milk is also altered when nursing women drink alcohol, a beverage that has been recommended for centuries to nursing mothers as an aid to lactation. Folklore relates that drinking small quantities of alcohol shortly before nursing increases milk yield, facilitates milk let-down, and relaxes both the mother and her baby. Contrary to this lore, research has demonstrated that breast-fed infants consume significantly less milk during the 3 to 4 hours after their mothers drink an alcoholic beverage.4647 This rejection was not due to infants responding to the altered flavored of the milk, however.48 Whether the alcohol was having a pharmacological effect on the nursing mother, the infant, or both is the subject of present investigations. Whatever the case, it would seem that the recommendation for a nursing mother to drink a glass of beer or wine before nursing may actually be counterproductive. While the mother may be more relaxed after a drink, her baby will ingest less milk. Moreover, infants appear to be learning about the flavor of alcohol as evidenced by changes in their suckling behavior.49 Conclusions
As a relatively new and exciting area of study, many questions remain unanswered about the infant's sense of taste and smell. The long-term goals of research at Monell are to uncover whether early exposure to flavors, most often experienced in amniotic fluid, mother's milk, or formula, affects later preferences, the development of food habits, and the willingness to accept new foods at weaning or thereafter. Although much research is still needed to fully understand the impact of early flavor experiences of the human infant, it is clear that they are not passive receptacles for flavored foods. Rather, they will avidly accept some flavors, while decidedly rejecting others.
We are particularly intrigued with the notion that there may be sensitive periods during early development when experiences with flavors produce particularly enduring preferences. The concept of sensitive periods, first introduced into the field of behavior from embryological studies by the ethologist Konrad Lorenz,5o implies that there is a period during early development when the organism is primed to receive and perhaps permanently encode important environmental information. An early knowledge of what is safe, appropriate, and nutritious foods would intuitively be important information for the fetus, infant, and young child. This is not to say that later learning is not important, but it highlights the possible significance of these very early experiences. Studies on breast-fed infants and infants fed casein hydrolysate formulas provide possible model systems to further study this issue. Because every baby is an individual, with distinct likes and dislikes, parents should expect that their child will need time to learn to like some foods while never liking others. Parents who offer their babies and growing children a variety of foods will provide both a nutritious, wellbalanced diet as well as an opportunity for their child's own personal preferences to develop.
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Dr. Beauchamp is Member and Director, and Dr. Mennella is Associate Member, Monell Chemical Senses Center, Philadelphia, PA 19104-3308, USA. This article is reprinted with permission of Pediatric Basics, Vol. 82. 1998 Gerber Products Company.
Copyright International Life Sciences Institute and Nutrition Foundation Jul 1998
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