The Pleasure Instinct: Why We Crave Adventure, Chocolate, Pheromones, and Music (10 page)

 

 

The history of olfaction is inextricably linked with the natural history of humans and the emergence of the first mammals. One theory suggests that during the Devonian period (about four hundred million years ago) life on Earth was dominated by aquatic species that used chemical senses to navigate their environment, find food, and attract mates. This may have taken the form of taste sensation or something similar, such as having appendages lined with receptor cells sensitive to the presence of amino acids. Nutritious food would have to be found by literally swimming through it. Many crustaceans still employ this form of chemical sampling.

A big improvement came with the appearance of the first nose, which was little more than a pair of epithelia pits or indentations on the early ancestors of the modern hagfish. These species had a significant advantage over competitors in that their primitive version of smell allowed them to detect food, mates, predators, and other elements important for their survival across extended distances. They no longer had to come into direct contact with an object to sense its presence; they only needed a sample of it in the form of volatile molecules unstable enough to diffuse through water or air.

The brain circuitry that processes olfactory information is essentially the same across all modern mammals. The differences are largely in terms of where the information is sent after reaching the primary olfactory cortex, and the sizes of the olfactory brain regions relative to other structures. For instance, rodents depend critically on a keen sense of smell, and their olfactory bulbs are enormous relative to other brain structures when compared to humans. This clearly has an impact on the ability of rodents to distinguish one smell from another, which is a key element of their survival. The basic mechanisms of olfactory sensation are the same as in humans, but not so heavily emphasized due to our equal reliance on the other senses.

Imagine you are walking before dinner one summer evening—on past the flowering dogwoods and myrtles that have exploded with color in the past few weeks, toward that unmistakable signature smell of the holiday weekend.You wonder if those are ribs or burgers, but after consulting your stomach decide that either would do. The chain of events that occurs between encountering the odor molecules and perceiving barbecued meat involves multiple stages of processing that provide a road map for understanding the evolution of smell in our species and the development of this sense in each individual.

The smell of barbecue is a complex mixture of scents. There is the smell that emanates from the charcoal, as well as from the cooking meat and flavorings. Each of these molecule types has different shapes and will activate different epithelia cells. The charcoal odorants will activate one set of epithelia cells, the cooking meat another set, and the smell of flavorings still other sets.Together, the group of activated cells forms an ensemble code that represents the complex barbecued meat smell that we actually perceive.

This signal is sent from the olfactory epithelia to the olfactory bulbs (one on each side of the brain), where it undergoes further processing and is then sent to several higher-level destinations. One copy is sent to the primary olfactory cortex, which is responsible for the conscious perception of the smell. A second copy is sent to the amygdala and adjacent structures that are responsible for translating motivational states such as hunger into appropriate responses such as feeding behaviors. Other copies are sent to limbic areas, including the hippocampus and the entorhinal cortex, which are critical for memory storage, as well as to the orbitofrontal cortex, which integrates the olfactory signals with those from other senses such as taste and assigns a reward value to the percept, in this case a hamburger. Hence, olfactory perception is situated in the primary olfactory cortex, and multisensory integration (for example, associating the smell of barbecue with taste information, which gives us the perception of flavor) with the reward value of a stimulus occurs in frontal locations that emerged later in our evolutionary lineage. Brain damage confined to the primary olfactory cortex—through stroke or physical trauma—leads to classic anosmia (an inability to smell and distinguish odors), while damage to the orbitofrontal cortex results in a complex syndrome of deficits in smell recognition and associated abilities that depend on multisensory integration.

 

 

When Melissa and I had our first glimpse of Kai at the sixth-week ultrasound, he was little more than a blastocyst, but even at this early stage in gestation he had the beginnings of an epithelia pit. From this point on in development, however, he shared fewer and fewer features in common with a hagfish embryo. At about eleven weeks into gestation, his olfactory epithelia cells began to extend toward cells that were beginning to grow in his olfactory bulb, and the bulb cells were, in turn, beginning to extend toward cortical sites. None of these developmental changes depends on smell experience, since until about the twenty-eighth week, Kai’s nasal cavity will be filled with a soft tissue plug that prevents chemicals from stimulating these cells. Interestingly, olfactory epithelial and olfactory bulb cells do not reach biochemical maturity until about the twenty-sixth week into gestation, and this is precisely when they will begin to need stimulation to continue developing normally.

You may be inclined to think that fetuses probably can’t smell very much, but research shows that their olfactory world is as rich as their mother’s. By the twenty-eighth week, Kai’s placenta has thinned to the point that virtually anything his mom smells is passed to him through the amniotic fluid. In fact, scientists have speculated that odor molecules may diffuse even faster in amniotic fluid than they do in air, since they ultimately must enter a liquid phase when binding to epithelia cells in the nasal mucus. So by the third trimester everything that Melissa eats and smells is experienced by Kai, and this has a huge impact on the continuing development of his nervous system and on olfactory preferences that will appear after his birth.

Once the nasal plugs are out and Kai begins to have his first encounters with smells, these experiences will kick the development of his olfactory system into overdrive, and the connections from the olfactory bulb to limbic and cortical brain regions will become more and more refined. First the connections between the olfactory bulb and limbic structures come online and allow Kai to perceive and distinguish among simple smells. These new connections allow Kai to perceive smells for the first time; however, the continued development of his olfactory system—most notably the important connections between the olfactory bulbs and higher cortical sites, such as the orbitofrontal cortex—depends critically on Kai receiving a wide variety of olfactory stimulation at this time, the more varied the better.

In animal models, if one of the two nasal passages remains sealed during this critical period so that no olfactory stimulation takes place, the corresponding epithelial cells, the olfactory bulb, and even cortical areas that normally would receive information from this side of the nose shrink up to 40 percent and lose cells rapidly. As expected, this results in a significant loss of smell perception and recognition after birth. Contrasting this, when premature animals born at thirty weeks are stimulated with an increased variety of smells (such as mint, cinnamon, banana, pine, or vanilla) through only one nasal passage, the olfactory brain regions that receive input from that side become larger and develop about 30 percent more cells than the control side that is stimulated with only ambient laboratory smells. Clearly, olfactory experience begins in the womb.

Animal experiments have also demonstrated that exposure to certain odors in utero has a dramatic influence on both pre- and postnatal behaviors. Rat fetuses display a sudden increase in excitable activity after pleasurable scents such as mint or lemon are injected into the amniotic fluid. Injections of simple saline solution or comparably bland scents have no apparent effects. After birth, the rats that were exposed to a mint or lemon scent while still in the womb prefer to nurse on nipples where these scents are present, rather than on those with neutral scents, a behavioral preference that keeps the pups near odors associated with the maternal environment.

Rats can also be classically conditioned to odors while in the womb. If their amniotic fluid is scented with an odor (even a pleasurable odor such as apple) and the fetus is then injected with a substance that makes it nauseous, it will avoid places and objects that bear that scent after birth. Such conditioned taste aversion was once thought to occur only in more mature animals, but it is now clear that prenatal animals are capable of many forms of learning.

These data tell us three very important things about olfaction. First, fetuses have a significant capacity for olfactory learning, since they remember a scent associated with the womb and seek it out after birth. Second, certain odors are innately excitable or pleasurable to animals in that they can function as primary reinforcers of behavior and have an impact on behavior and physiological responses the very first time they are experienced. Finally, the capacity for olfactory learning and memory can offset innate odor preferences, making a scent that is normally attractive something to avoid after birth.

 

 

Humans show remarkably similar forms of olfactory learning, and prenatal exposure to odors seems to play an important role in parental bonding and kin recognition. Newborns have an innate fondness for the smell of amniotic fluid, particularly their own. Experiments performed in culturally diverse populations have shown that babies as young as one day old prefer the smell of their own amniotic fluid to that of age-matched controls. The most commonly used test of preference in newborns is, of course, sucking behavior. When given the choice between nursing on their mother’s breast scented with their amniotic fluid or that of an age-matched control, they almost always choose the former. Newborns also cry less and show a diminished stress response when they smell their own amniotic fluid. Since the many odors that emanate from a mother—such as the smell of milk, colostrum, saliva, and perspiration—stem from the same genetic and dietary sources as the amniotic fluid, they will all have some shared chemical groups. Hence, a preference for the smell of maternal amniotic fluid may evolve functionally into a preference for the smells of Mom in general; an adaptation such as this would have obvious utility in keeping the newborn close to its primary caregiver. These behaviors are evidence that olfactory labeling occurs in humans as it does in other animals.

Olfactory labeling while still in the womb has a profound influence on our postnatal ability to identify a person as kith and kin. Within hours after birth, a breast-fed infant can readily identify and will orient toward a breast pad worn by their lactating mother over a breast pad worn by an unrelated lactating woman. Newborns show abrupt changes in behavior—such as decreasing arm and leg movements, initiation of the sucking reflex, and are generally calmer—when exposed to odors that originate from their mother’s body, including those that emanate from her breast, underarms, and neck.Almost any natural smell that can be used as a reliable indicator of Mom’s presence has these effects on behavior.

Olfactory labeling also has an impact on the development of odor preferences and aversions after birth. In the Alsatian region of France, there is widespread use of anise flavoring in the local cuisine.Taking advantage of this custom, a group of scientists compared the olfactory responsiveness of neonates who were born to mothers who had or had not consumed anise flavor during pregnancy. Infants born to anise-consuming mothers showed a stable preference for the smell of anise when tested immediately after birth and four days later. Contrasting this pattern, infants born to mothers who did not consume anise tended to display either an aversion or no response at all to the odor. This study indicates that olfactory labeling also occurs in response to dietary influences that may alter the in utero chemical environment. One can imagine the profound implications of this process for the newborn in that it most likely influences a host of functions that range from the emergence of odor and food preferences to the development of early mother-infant attachment.

 

 

Although not all scientists agree, it appears that newborns may also have innate preferences for certain odors, such as floral and fruity smells. These odorants are not necessarily present in the amnion of most mothers, yet the preference for these smells emerges in most newborns across different cultures and persists into childhood. Researchers have found that newborns can discriminate among a number of qualitatively different odorants, evidenced by changes in body movements, facial responses, and heart and respiratory rates. It is much easier, however, to test verbal children who can simply tell you whether they find a smell pleasing.The few published studies that have focused on the olfactory preferences of verbal children have not always found consistent effects, and one reason may be that differences in experimental design influence the results. For instance, it is well known that young children tend to answer a positively phrased question in the affirmative. When these and similar methodological issues are controlled for, however, some universal tendencies do indeed emerge.

It is generally accepted that children as young as three years old exhibit stable hedonic preferences for specific odors independent of the culture in which they were raised. Some of the most popular smells include strawberry, floral, spearmint, and wintergreen, while odors such as butyric acid (strong cheese/vomit) and pyridine (spoiled milk) are universally disliked. That most children find fruit and floral odors pleasing should come as no surprise, since they often signal the presence of a nearby nutritionally rich food source—an important adaptation, to be sure, within an evolutionary context.