foods while still in their mothers’ wombs. When Mennella began her career, relatively little was known about how and when humans form their preferences for different flavors. Despite a large literature on how maternal diet influences the overall nutrition and health of offspring, few researchers were looking at whether flavor preferences derive from what the mom consumes during pregnancy or soon after birth. Mennella recalls that doctors used to tell women still nursing their child to avoid spicy or pungent foods, based on “folklore” that infants inherently prefer bland foods. Over the past several decades, however, a convergence of findings from psychologists and neuroscientists, including Mennella, has shown that infants’ tastes are malleable. Although our cravings for salt, sugar, and fat do have a genetic basis, new evidence shows that the majority of our food preferences are “not inborn,” Mennella says. Instead, the taste for a variety of flavorful foods, including bitter vegetables, is “part of culture, and something you have to learn.” Through creative experiments with newborns, Mennella and others have shown such learning can begin as early as in the womb.
Downloaded from www.sciencemag.org on August 14, 2014
Babies form flavor preferences as early as in the womb.
The taste of things to come Early postnatal, and even prenatal, experiences shape culinary tastes By Emily Underwood
E
verything about the newborns was normal, except for their pungent aromas of fenugreek, curry, and cumin. At first, the physicians who delivered the four unrelated babies at a Tel Aviv hospital were worried—some strong smells at birth signal disease. But soon they discovered the apparent source of the odors. Hours before labor, the mothers said, they had eaten skhug and amba, spicy traditional Yemeni and Israeli foods. 750
The obscure case study—described in a 1985 issue of the European Journal of Pediatrics—caught Julie Mennella’s attention in the early 1990s. A biopsychologist at the Monell Chemical Senses Center in Philadelphia, Pennsylvania, Mennella studies why we like the foods that we do—what she describes as one of the “biggest mysteries of human behavior.” The Israeli study “was a great ‘aha!’ moment,” Mennella says, because it supported her hunch that infants can perceive—and perhaps even learn to love—the distinct flavors of their culture’s
a figure of speech in Mennella’s lab. An Italian-American for whom food is “very important,” she made pungent garlic the focus of her first attempts to pin down some of the origins of our flavor preferences. Working with Gary Beauchamp, director of the Monell research program, Mennella asked pregnant women to consume either plain-flavored or garlic capsules during the last weeks of their pregnancy. By that point, a fetus clearly has both the ability to taste and to smell—around the 24th week of gestation, for example, mucus plugs blocking the nasal passages dissolve, allowing amniotic fluid to bathe a fetus’s newly formed olfactory receptors (see p. 751). Mennella then asked volunteers, recruited from around the university, to sniff unlabeled bottles of amniotic fluid and breast milk from both groups of mothers. If these amateur sommeliers could smell the garlic in a blind test, it was likely that the fetuses could, too, Mennella reasoned— and the volunteers easily sniffed out which came from the garlic consumers. Mennella next videotaped and documented how babies born to both maternal groups behaved when they were offered garlicky milk. Contrary to the old folk wisdom, the babies whose mothers had eaten garlic sucked their milk down with relish. In contrast, infants with garlic-free mothers grimaced and writhed to avoid it. sciencemag.org SCIENCE
15 AUGUST 2014 • VOL 345 ISSUE 6198
Published by AAAS
PHOTO: WENDELL/DAMBROSIA/WEESTOCK/CORBIS
FOLLOWING YOUR NOSE is more than
PA R E N T I N G
PHOTOS: (BOTTOM LEFT) CATHERINE FORESTELL AND JULIE MENNELLA/MONELL (2); (TOP RIGHT) NESTLE/PETIT FORMAT/SCIENCE SOURCE
Since that series of studies in the 1990s, Mennella and Beauchamp have obtained similar results with other flavors such as vanilla and carrot. Familiarity seems to breed affinity for substances such as alcohol, too, Mennella says. In one study, she and Beauchamp found that 1-year-olds with heavy-drinking or alcoholic parents prefer to mouth toys scented with ethanol over unscented or vanilla-scented toys. Research in mice hints at a potential neurobiological basis for these early associations, says Diego Restrepo, a developmental biologist at the University of Colorado School of Medicine in Aurora. In 2010, he fed cherry- or mint-flavored chow to pregnant mice, then studied which flavor their offspring preferred at 20 days old. Like the human infants, the young mice preferred to eat the chow flavor they’d been exposed to in utero. Neurons that relay information about smell from the nose to the brain respond individually to thousands of odorant molecules, allowing mice and humans to distinguish a vast array of different smells—possibly as many as 1 trillion odors in humans (Science, 21 March, p. 1370). On examining the brains of the two groups of rodents, Restrepo found that in mice exposed to the mint flavor in utero, the junctions between the olfactory sensory neurons that can detect mint and those
Training the fetal palate A fetus learns to recognize the favors of mom’s diet through her amniotic fuid.
Taste By 16 weeks old, the fetus begins to respond to flavors in amniotic fluid, swallowing and smacking its lips if it tastes sweet, and grimacing and swallowing less fluid if it tastes bitter.
Smell At 24 weeks, olfactory receptor cells that respond to different odors begin to function, when plugs obstructing the nasal passages dissolve and allow the fetus to inhale and smell amniotic fluid.
that relay a mint signal to the amygdala, a brain region that processes emotion, were significantly enlarged. In mice exposed to cherry, those junctions between neurons relaying the cherry signal were bigger, suggesting that experience with the smell in utero had strengthened those connections, he says. More evidence that maternal diet can influence the developing brain’s flavor processing came from a study published last year in The FASEB Journal by researchers at the University of Adelaide in Australia. They fed pregnant rats either a monotonous diet or a smorgasbord of tempting treats, including hazelnut spread, peanut butter, chocolate biscuits, sweetened cereal, and a lard and chow mix. Then they observed how the offspring behaved around those foods. Mice whose mothers had a junk food diet developed abnormal neural reward circuitry resembling that seen in addiction. SOME RESEARCHERS DOUBT that pre-
A baby rejects a novel flavor (top), while another exposed to a flavor in utero accepts it (bottom).
SPECIAL SECTION
natal or early postnatal experiences with flavor have much long-lasting effect. Adults are clearly capable of learning to love and hate new flavors, as anyone who’s lost their taste for a favorite food after a bout of nausea can attest. And if you compare foods that college students enjoy with those they ate under their parents’ watchful gazes, the correlation “is not zero, but it’s very low,” says Paul Rozin, a psychologist at the University of Pennsylvania. But Mennella and others believe that there are sensitive periods for flavor learning, just as there are for the development of sight and other senses. At 3.5 months old, many babies will refuse to drink Nutramigen, a sour, bitter-tasting formula often prescribed to underweight infants who can’t digest cow’s milk. She and Beauchamp have shown that if the infants start the formula
SCIENCE sciencemag.org
before that age, most will happily drink the nasty-tasting stuff, and even prefer it. Understanding why infants learn to accept different flavors could help guide treatment for premature babies, who frequently spend their first months of life being tube-fed and often gag when they first taste milk or formula, Mennella says. From an evolutionary point of view, infants need to be receptive to new flavors early in life in order to survive, says Regina Sullivan, a psychiatrist at New York University Langone Medical Center in New York City. Because baby mammals depend so much on their parents, it makes sense that a mechanism exists to ensure that newborns learn to eat what mothers can provide no matter how it tastes, she explains. Mennella hopes that understanding early-life influences on diet in children will help parents buffer children from an environment increasingly filled with sugar- and salt-laden foods. That is challenging because, as she and Beauchamp have found, infants are more sensitive than adults to both sweet flavors and bitter ones, making it harder for them to resist sugary foods and to eat vegetables. A handful of correlational studies suggest that children eat more fruits and vegetables later in life if their mothers did the same while pregnant or breast-feeding. Rozin notes, however, that it is difficult to determine how much those early experiences affect long-term outcomes because the foods we’re exposed to at a very young age often continue to surround us up until we leave the nest. The most potent aspect of early flavor experiences may be their emotional power, Mennella says. Our first flavors are among “the oldest, most enduring memories that take us to our past,” she says. “Food is much more than a source of calories—it provides us with an identity.” ■ 15 AUGUST 2014 • VOL 345 ISSUE 6198
Published by AAAS
751
Downloaded from www.sciencemag.org on August 14, 2014
Babies form flavor preferences as early as in the womb.
The taste of things to come Early postnatal, and even prenatal, experiences shape culinary tastes By Emily Underwood
E
verything about the newborns was normal, except for their pungent aromas of fenugreek, curry, and cumin. At first, the physicians who delivered the four unrelated babies at a Tel Aviv hospital were worried—some strong smells at birth signal disease. But soon they discovered the apparent source of the odors. Hours before labor, the mothers said, they had eaten skhug and amba, spicy traditional Yemeni and Israeli foods. 750
The obscure case study—described in a 1985 issue of the European Journal of Pediatrics—caught Julie Mennella’s attention in the early 1990s. A biopsychologist at the Monell Chemical Senses Center in Philadelphia, Pennsylvania, Mennella studies why we like the foods that we do—what she describes as one of the “biggest mysteries of human behavior.” The Israeli study “was a great ‘aha!’ moment,” Mennella says, because it supported her hunch that infants can perceive—and perhaps even learn to love—the distinct flavors of their culture’s
a figure of speech in Mennella’s lab. An Italian-American for whom food is “very important,” she made pungent garlic the focus of her first attempts to pin down some of the origins of our flavor preferences. Working with Gary Beauchamp, director of the Monell research program, Mennella asked pregnant women to consume either plain-flavored or garlic capsules during the last weeks of their pregnancy. By that point, a fetus clearly has both the ability to taste and to smell—around the 24th week of gestation, for example, mucus plugs blocking the nasal passages dissolve, allowing amniotic fluid to bathe a fetus’s newly formed olfactory receptors (see p. 751). Mennella then asked volunteers, recruited from around the university, to sniff unlabeled bottles of amniotic fluid and breast milk from both groups of mothers. If these amateur sommeliers could smell the garlic in a blind test, it was likely that the fetuses could, too, Mennella reasoned— and the volunteers easily sniffed out which came from the garlic consumers. Mennella next videotaped and documented how babies born to both maternal groups behaved when they were offered garlicky milk. Contrary to the old folk wisdom, the babies whose mothers had eaten garlic sucked their milk down with relish. In contrast, infants with garlic-free mothers grimaced and writhed to avoid it. sciencemag.org SCIENCE
15 AUGUST 2014 • VOL 345 ISSUE 6198
Published by AAAS
PHOTO: WENDELL/DAMBROSIA/WEESTOCK/CORBIS
FOLLOWING YOUR NOSE is more than
PA R E N T I N G
PHOTOS: (BOTTOM LEFT) CATHERINE FORESTELL AND JULIE MENNELLA/MONELL (2); (TOP RIGHT) NESTLE/PETIT FORMAT/SCIENCE SOURCE
Since that series of studies in the 1990s, Mennella and Beauchamp have obtained similar results with other flavors such as vanilla and carrot. Familiarity seems to breed affinity for substances such as alcohol, too, Mennella says. In one study, she and Beauchamp found that 1-year-olds with heavy-drinking or alcoholic parents prefer to mouth toys scented with ethanol over unscented or vanilla-scented toys. Research in mice hints at a potential neurobiological basis for these early associations, says Diego Restrepo, a developmental biologist at the University of Colorado School of Medicine in Aurora. In 2010, he fed cherry- or mint-flavored chow to pregnant mice, then studied which flavor their offspring preferred at 20 days old. Like the human infants, the young mice preferred to eat the chow flavor they’d been exposed to in utero. Neurons that relay information about smell from the nose to the brain respond individually to thousands of odorant molecules, allowing mice and humans to distinguish a vast array of different smells—possibly as many as 1 trillion odors in humans (Science, 21 March, p. 1370). On examining the brains of the two groups of rodents, Restrepo found that in mice exposed to the mint flavor in utero, the junctions between the olfactory sensory neurons that can detect mint and those
Training the fetal palate A fetus learns to recognize the favors of mom’s diet through her amniotic fuid.
Taste By 16 weeks old, the fetus begins to respond to flavors in amniotic fluid, swallowing and smacking its lips if it tastes sweet, and grimacing and swallowing less fluid if it tastes bitter.
Smell At 24 weeks, olfactory receptor cells that respond to different odors begin to function, when plugs obstructing the nasal passages dissolve and allow the fetus to inhale and smell amniotic fluid.
that relay a mint signal to the amygdala, a brain region that processes emotion, were significantly enlarged. In mice exposed to cherry, those junctions between neurons relaying the cherry signal were bigger, suggesting that experience with the smell in utero had strengthened those connections, he says. More evidence that maternal diet can influence the developing brain’s flavor processing came from a study published last year in The FASEB Journal by researchers at the University of Adelaide in Australia. They fed pregnant rats either a monotonous diet or a smorgasbord of tempting treats, including hazelnut spread, peanut butter, chocolate biscuits, sweetened cereal, and a lard and chow mix. Then they observed how the offspring behaved around those foods. Mice whose mothers had a junk food diet developed abnormal neural reward circuitry resembling that seen in addiction. SOME RESEARCHERS DOUBT that pre-
A baby rejects a novel flavor (top), while another exposed to a flavor in utero accepts it (bottom).
SPECIAL SECTION
natal or early postnatal experiences with flavor have much long-lasting effect. Adults are clearly capable of learning to love and hate new flavors, as anyone who’s lost their taste for a favorite food after a bout of nausea can attest. And if you compare foods that college students enjoy with those they ate under their parents’ watchful gazes, the correlation “is not zero, but it’s very low,” says Paul Rozin, a psychologist at the University of Pennsylvania. But Mennella and others believe that there are sensitive periods for flavor learning, just as there are for the development of sight and other senses. At 3.5 months old, many babies will refuse to drink Nutramigen, a sour, bitter-tasting formula often prescribed to underweight infants who can’t digest cow’s milk. She and Beauchamp have shown that if the infants start the formula
SCIENCE sciencemag.org
before that age, most will happily drink the nasty-tasting stuff, and even prefer it. Understanding why infants learn to accept different flavors could help guide treatment for premature babies, who frequently spend their first months of life being tube-fed and often gag when they first taste milk or formula, Mennella says. From an evolutionary point of view, infants need to be receptive to new flavors early in life in order to survive, says Regina Sullivan, a psychiatrist at New York University Langone Medical Center in New York City. Because baby mammals depend so much on their parents, it makes sense that a mechanism exists to ensure that newborns learn to eat what mothers can provide no matter how it tastes, she explains. Mennella hopes that understanding early-life influences on diet in children will help parents buffer children from an environment increasingly filled with sugar- and salt-laden foods. That is challenging because, as she and Beauchamp have found, infants are more sensitive than adults to both sweet flavors and bitter ones, making it harder for them to resist sugary foods and to eat vegetables. A handful of correlational studies suggest that children eat more fruits and vegetables later in life if their mothers did the same while pregnant or breast-feeding. Rozin notes, however, that it is difficult to determine how much those early experiences affect long-term outcomes because the foods we’re exposed to at a very young age often continue to surround us up until we leave the nest. The most potent aspect of early flavor experiences may be their emotional power, Mennella says. Our first flavors are among “the oldest, most enduring memories that take us to our past,” she says. “Food is much more than a source of calories—it provides us with an identity.” ■ 15 AUGUST 2014 • VOL 345 ISSUE 6198
Published by AAAS
751
