The Pleasure Instinct Part 2

We're often told that newborns and infants are soothed by rocking because this motion emulates what they experienced in the womb, and that they must take comfort in this familiar feeling. This may be true; however, to date there are no compelling data that demonstrate a significant relationship between the amount of time a mother moves during gestation and her newborn's response to rocking. Just as plausible is the idea that newborns come to a.s.sociate gentle rocking with being fed. Parents understand that rocking quiets a newborn, and they very often provide gentle, repet.i.tive movement during feeding. Since the appearance of food is a primary reinforcer, newborns may acquire a fondness for motion because they have been conditioned through a process of a.s.sociative learning (see chapter 3).

Another possibility is that the sensation of motion is actually a primary reinforcer itself and is inherently pleasurable independent of any a.s.sociations it may have with other forms of stimulation. In this scenario, the sensation of motion is desirable and soothing because it is critical for primates to experience these types of stimulation for normal development. The fact that both motion and touch sensation are the earliest sensory capacities to emerge and are keenly dependent on stimulation during development suggest that newborns, toddlers, and children may seek out experiences of motion as a primary reinforcer that promotes the continued growth and maturation of these systems. Children, of course, are unaware of this relationship-they needn't be consciously aware of why they enjoy certain forms of movement for this growth and maturation to take place. They only need to crave the experience enough so that they seek it out. This process is reminiscent of the relationship between our fondness for sweets and their ability to produce energy. Evolutionary mechanisms do not require that primates understand the biochemical reactions involved in converting sugars to ATP for them to benefit from the relationship. They only have to seek out sugar (for whatever reason) to give those individuals in a population who crave these high-energy food sources a selective advantage over their competing hominids.The end result is a contemporary population of sweet-toothed primates with an extraordinary means for fulfilling their biologically driven desires.

How Movement and Touch Promote Brain Development The early emergence of touch and motion sensation is critical to the normal development of other parts of the nervous system. Because these sensory capacities have such an early onset, they organize other sensory and motor systems. Biologists have been moved by these findings to begin thinking of development as a c.u.mulative process rather than a simple schedule of programmed events. For instance, children who have delayed vestibular system maturation tend to reach motor milestones such as crawling, sitting up, and walking more slowly than normal children, sometimes taking twice as long to pa.s.s these hurdles. Each of these behaviors depends on a sense of balance, and hence vestibular function becomes a critical force in organizing motor behavior.

Children born with deficits in touch and vestibular function also frequently have emotional and cognitive disturbances that often involve learning and memory, attention, visual-motor integration, language, and autism, to name just a partial list. Neuroscientists sensitive to this new view of development are now beginning to understand how early touch and vestibular experiences organize and jump-start the growth of so many other processes.

Although there is enormous variability in the way newborns respond to being touched, there is remarkable consistency from baby to baby in terms of their bodies'physiological response. Gentle touching or vestibular stimulation such as rocking initially produces a state of biological arousal that resembles the cla.s.sic stress response. Increased brain-stem activation triggers a series of chemical cascades involving all the usual suspects-increases in cortisol, ACTH, and other stress hormones. These effects reverse, however, with continued stimulation. During prolonged touch or slow, repet.i.tive movements, the brainstem systems that were once activated become inhibited, and slowly this process down-regulates the body's stress system. The stress hormones that were at first elevated begin to fall with continued stimulation and actually decrease below normal baseline levels (measured while the baby is at rest and not being touched or moved).

Studies now show that down-regulation of the stress system continues long after the touching or rocking stops. The effects of touch and motion are enduring, measurable hours after stimulation has ceased, and it is this property that seems to have such a significant impact on the development of other systems. Stress hormones such as cortisol have been found to have deleterious effects on synaptogenesis and synaptic pruning in laboratory animals, and brain limbic regions seem particularly susceptible. Rodents and primates that have been subjected to elevated cortisol levels show significantly reduced brain volume in several limbic regions including the hippocampus when compared to those that are not stressed. Moreover, animals that are given these experimental manipulations repeatedly for periods as short as two weeks exhibit a range of behavioral problems as juveniles that often persist into adulthood, including deficits in learning ability, memory, attention, sensory-motor integration, solving tasks that require flexibility and adaptability, and regulating their emotions. This suggests that the pleasure of touch and motion contributes to normal brain growth by regulating stress hormone levels during development.

These findings have led some researchers to ask if there are protective benefits for developing animals (including humans) exposed to stimulation and experiences that lower stress hormone levels. The answer, of course, is yes. For instance, gentle daily ma.s.sage of laboratory mice for a period as short as two weeks during their first three months of life results in faster maturation of several cortical brain regions (hippocampus, somatosensory cortex, cerebellum) when compared to controls not given the stimulation.These mice are also less fearful and prefer novelty more than controls that are not given the extra stimulation.

The implications of studies like this have not been lost on neonatal care units. Preterm babies are now routinely swaddled in an effort to improve their rate of maturation and ensure that the prerequisite tactile sensations needed for proper brain development are experienced as much as possible. Some hospitals have even gone a step farther and offer swaddling in conjunction with programmed movement stimulation that occurs on specially constructed infant waterbeds. Although there have not been many controlled evaluations of these treatments, those that have been conducted have found that swaddling and movement therapy significantly increase the rate at which preterm babies reach critical developmental milestones when compared to preemies given the usual care. These benefits include reported increases in a number of behavioral measures such as learning to crawl and walk earlier, increases in formula intake and weight gain, improved responsiveness to touch, better muscle tone, increased visual acuity, recognition memory, and attention, among many others.

Older babies also benefit from touch and motion stimulation. In one experiment babies aged three to sixteen months were given scheduled vestibular stimulation by being placed on their parents' laps and rotated in a swivel chair for ten minutes each day over a period of two weeks. The babies, of course, loved the experiment-giggling and jumping during the rotation. Interestingly, the babies who were spun reached key developmental landmarks such as crawling and walking more quickly than their nonspun counterparts. This effect was even demonstrated in identical twins. The twin who received the motion stimulation began walking four months earlier than his brother.

Humans are programmed from birth to experience certain forms of touch and motion as intrinsically pleasurable. The roots of these hedonic preferences can be found in babies who are pacified by cradling and rocking; toddlers and children who self-stimulate their touch and vestibular systems using age-specific behaviors such as bouncing, rocking, and self-hugging; on through adolescents and young adults who have a need for speed. Like other hedonic preferences such as our desire for sweets, the pleasure we find in touch and motion satisfies critical developmental requirements for normal brain and behavioral maturation.The problem, however, is that technology has radically outpaced evolutionary pressures in the past two hundred years, leading to new and potentially harmful methods of satisfying this biological imperative. In chapter 11 we will consider how our need for touch and motion often couples with other hedonic preferences that together foster maladaptive behaviors such as addiction and thrill-seeking.

Chapter 5.

In Praise of Odors I will be arriving in Paris tomorrow evening. Don't wash.

-Napoleon to Josephine

All good k.u.mrads you can tell by their altruistic smell.

-E. E. c.u.mmings

No other sense is so intimately bound to memory and emotion as smell. To this day, the mere hint of something sulfuric takes me back to a steamy August birthday and the gift of a Junior Scientist Chemistry Set from my mother. The blurb on the back of the box was encouraging: "Perform over 1,500 experiments and procedures in the gaseous phases of matter, chemical models, solutions, acids, bases, electrochemistry, organic chemistry and more." For the next few weeks I couldn't stop playing with this thing. Mom was thrilled and, I'm sure, convinced that one day I would be the next Louis Pasteur. But parents often forget that eight-year-old boys are not terribly interested in a.n.a.lyzing the covalent bond properties of solvents or learning how to neutralize an acid; they tend to like things that make loud noises, blow up, or best of all, some combination of the two.

Scouring the list of experiments one evening, I found a promising entry called "Outrageous Ooze," which guaranteed an "explosive miniature volcanic reaction with real lava flow." Mom was busy cooking and cleaning in preparation for a dinner party at our house that night, and Dad was out driving across the state and back to pick up some fancy German chocolate ice cream for dessert. I was given advance warning to be on my best behavior, and yes, my friend Hector could come over as long as we played in the back room.

Hector was the best lab a.s.sistant I ever had; he was always eager to see what happened if we mixed this and that, and had a natural talent for combining compounds that we were warned against mixing. A rule for toy manufacturers: The phrase "Warning-never combine Chemical A and Chemical B" is usually translated by eight-year-olds into "Attention-please do this immediately." Just before the first guests began arriving I ran in the kitchen and asked my mother for some vinegar, baking soda, and dishwashing detergent. She hesitated for a moment, but then the doorbell rang and she didn't have time to protest.

Back in the lab, Hector and I mixed the ingredients carefully. We stood back and waited for the Vesuvial display, only to be disappointed by the slow trickle that emanated pathetically from the jar, so we consulted the next paragraph, which instructed us to "incorporate the following mixture to produce hydrogen sulfide gas for extra realism." I began heating the sulfuric mix before Hector finished reading the sentence, and suddenly we were treated to a thick display of smoke, and a horrible stench of rotten eggs began to fill the room. Even after removing the mixture from the heat, the pungent smell and smoke worsened and eventually, to my parents' horror, spread throughout the entire house.The memory I usually a.s.sociate with this smell today consists of my parents and the complete dinner party standing out in the street watching fetid-smelling smoke billow from the front and side windows of our small house.

The chemical senses of smell and taste are as phylogentically ancient as touch, and their age is given away by basic anatomy. Whereas the perceptual seat of sight and sound resides in the neocortex-a recent addition in mammals-the representations of the chemical senses are stowed away in the rather archaic limbic and paralimbic regions. This is true for humans, primates, and virtually all mammals large and small.

The cortical representations of smell and taste are located in regions of the brain long believed to be important for processing the motivational state of an animal as well as the emotional significance of external stimuli. Experiments have shown that when humans are stimulated through taste or smell, large portions of the brain that are critical for processing emotional information and memory become activated, including the amygdala, insula, cingulate cortex, and orbitofrontal cortex.

Let's consider smell-it is the one sense that simply can't be turned off without immediate consequences. We can close our eyes, cover our ears, shut our mouths, and refrain from touching things, but stop breathing for a moment and you quickly realize that we are all slaves to olfaction. Humans take more than 23,000 breaths each day, pa.s.sing close to 450 cubic feet of air through their nose. Our nasal pa.s.sages act as miniature wind tunnels powered by a respiratory vacuum that induces air molecules to enter with astonishing force. Odor molecules have a b.u.mpy ride as they enter the nose-first heated by the frictional forces as they pa.s.s on either side of the septum and then thrust up through three complicated horizontal chambers shaped by vascular tissue. The turbulent journey ends at the roof of these interior pa.s.sages as the molecules collide with a small patch of yellowish tissue on either side of the septum known as the olfactory epithelia olfactory epithelia. At this point, the air molecules have reached the brain.

Each cell in the olfactory epithelia-and there are hundreds of thousands of them-has receptors that are tuned to a particular odor. The shape of the odor molecule is what matters most. If an odor molecule has a shape, or a very close match, that allows it to bind to one of the many olfactory epithelia cells, it can cause that cell to send a signal in the form of an action potential on to the next stage of neural processing. The sole job of the olfactory epithelia cells is to convert chemical signals that find their way up our noses into electrical signals that the brain will understand. Although we generally think of our sense of smell as being rather limited compared to other mammals-dogs, for example-humans can perceive and distinguish differences among thousands of odors.

In her book A Natural History of the Senses A Natural History of the Senses, Diane Ackerman refers to smell as "the mute sense." While we can detect and even perceive thousands of smells, we are woefully inept at describing them without reference to other things or, even more often, how they make us feel.This verbal shortfall may arise in part because the brain regions that register smells are only weakly and indirectly connected to those areas that support language processing. A more direct set of connections exists between areas that deal with emotions and language, and so the lexicon of smells is riddled with descriptions of how a smell makes us feel. Try to describe the smell of camphor without reference to a pine tree; or imagine explaining the smell of the ocean in the morning to someone who has never had the experience.

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 compet.i.tors 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 a.s.signs 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, a.s.sociating 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 cla.s.sic 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 a.s.sociated 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 pa.s.sed 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 pa.s.sages 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 pa.s.sage, 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 a.s.sociated with the maternal environment.

Rats can also be cla.s.sically 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 a.s.sociated 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.

The emergence of this evolutionary adaptation in our species is echoed in the development of each individual with the growth and maturity of brain pathways that connect olfactory cortical areas with midbrain and orbitofrontal regions that mediate natural reward. While the midbrain reward centers develop at a fairly early embryonic stage in humans, the pathways that connect these regions to the areas responsible for perceiving odors do not mature until rather late in gestation and are known to depend on experience. Because this is the case, many scientists believe that although these olfactory preferences are very similar across cultures, their development probably results from learning to a.s.sociate these smells (in the womb) with flavorful food and the onset of an intrinsically rewarding behavior-eating.

Consummatory behaviors such as eating and s.e.xual activity are known to increase levels of circulating neuropeptides called endorphins, those lovely chemicals that provide a feeling of relaxation and calm and that are chemically similar to morphine.The development of these pathways-which depend on exposure to odors that signal the presence of potential sources of nutrition-may occur during the last trimester, while the fetus is exposed to the coappearance of certain smells and tastes with an increase in amniotic endorphin levels that have a calming effect on mother and fetus alike. Hence, the emergence of "universal" olfactory preferences is likely to result from the same learning mechanisms that mediate olfactory labeling in all mammals.

The Smell of Attraction Like it or not, we smell, and the subtle odorous messages we send and receive-often unknowingly-have a profound influence on our social ident.i.ties and a wide range of behaviors, including mate selection, courtship, and the timing of ovulation.The word pheromone pheromone calls up a variety of images to mind: mammals communicating using a hidden language of scents; trendy socialites paying $300 per ounce for a vial of boar effluvia that promises to allure the opposite s.e.x; and sorority sisters who menstruate in synchrony month after month. calls up a variety of images to mind: mammals communicating using a hidden language of scents; trendy socialites paying $300 per ounce for a vial of boar effluvia that promises to allure the opposite s.e.x; and sorority sisters who menstruate in synchrony month after month.

Although it has proven rather difficult to isolate and identify a human pheromone, there is a growing body of evidence that we use them to communicate chemically much like other mammals.The first convincing evidence came from an unexpected place-an undergraduate dormitory room at Wellesley College. In 1967, an undergraduate student named Martha McClintock noticed that many of the girls in her dorm menstruated on the same days and wondered if such coordination might have survival value. She asked two simple questions in her research project: "When did you last menstruate?" and "Who are your two best friends?" The results surprised everyone.Women who spent the most time together tended to menstruate at the same time.

It wasn't until ten years later that the mechanism that causes this synchrony (now known as the McClintock Effect) was discovered. In a simple experiment, psychologist Michael Russell and his colleagues at Sonoma State Hospital in California rubbed an extract from the underarm of a woman with a very regular twenty-eight-day cycle under the noses of sixteen other women three times a week. Within four months, all of the women were menstruating within three days of one another.The odors of a single person, it turns out, can influence the menstrual cycles of many others. It was still unclear, however, how such an effect might have survival or adaptive value.

The answer came the following year, when it was discovered that men have cycles as well, and that their regular rise and fall in core body temperature and the production of essential steroids such as testosterone can be modulated by the presence of other males. The final link came when additional experiments showed that the production of testosterone and other androgens in men often becomes synchronized to the menstrual cycles of their wives and lovers.Taken together, an impressive display of synchrony emerges between men and women in close contact with each other on a regular basis, and this patterning might facilitate the timing needed for effective s.e.xual reproduction.

In addition to regulating menstrual and physiological cycles, pheromones have a say in other very personal affairs, such as distinguishing those we find s.e.xually attractive from those who remind us of a sibling. But what is the physical basis for this hidden conversation of scents? Humans don't seem very interested in smelling the urine or underarm odor of potential mates, so where do human pheromones come from and what do they smell like?

The Desana Indians of the Amazon rain forest have a cosmological worldview built around olfaction. For them, the essence of a person is revealed by their smell, which emanates directly from their bones. Mores that guide courtship and social relationships are intertwined with the relationships among different smells. The Desana believe that people of the same tribe share a common smell, and strict rules exist forbidding marriage between those who have similar scents-an olfactory-inspired incest taboo. Certain smells should never be mixed, yet some naturally go together. An answer to the puzzle of how human pheromones influence behaviors such as mate selection came out of left field and was inspired by studies of the Desana.

It has been known for ages that foreign tissue implanted into a host is often rejected by the host's immune system. Each of our own cells bears proteins that our immune system recognizes as "self." When a foreign cell enters the body, the immune system attempts to cla.s.sify the nonself intruder by attaching a labeling protein to it and generating antibodies designed to destroy it. The immune system has a memory for intruder cells, and the next time the same foreigner is encountered, the antibodies can be launched even faster, since they do not need to be generated from scratch.

A segment of our DNA called the major histocompatability complex (MHC) codes for the immune cells that identify intruding disease organisms, essentially functioning as our immune system's first line of defense. Unlike many genes that have only a few alternative versions (called alleles), MHC genes have upward of a hundred or so, with each providing immunity against different sets of potential disease strains.

When we think of heredity, we typically have in mind the cla.s.sical pattern of single allele combinations-the dominant-recessive pairings that play a winner-take-all game with traits such as eye and hair color. If one parent has blue eyes and the other brown, one gene will dominate, meaning the gene from the other parent that controls this trait is not expressed.

MHC genes work differently in that they are codominant. Say you inherit one version of an MHC gene from your father that improves resistance to disease A and another version of the gene from your mother that happens to help fight disease B. Since MHC genes are codominant, you will be able to resist both diseases. Thus, parental combinations that have the greatest degree of MHC genetic heterozygosity 3 3 will produce offspring with the most robust immune functioning.These offspring would have a distinct survival advantage over offspring from parents who have considerable overlap in their MHC genes, providing resistance to a smaller spectrum of disease strains. Variation in this dimension, then, can serve as an important selection factor in the evolution of our species. The question is, what serves to attract us toward mates who have MHC genes different from our own? will produce offspring with the most robust immune functioning.These offspring would have a distinct survival advantage over offspring from parents who have considerable overlap in their MHC genes, providing resistance to a smaller spectrum of disease strains. Variation in this dimension, then, can serve as an important selection factor in the evolution of our species. The question is, what serves to attract us toward mates who have MHC genes different from our own?

The initial clues emerged from animal experiments. If a female mouse is offered two suitors, she inevitably chooses the mate whose MHC genes have the least overlap with her own, and it is now known that they do this through smell. Scientists have found that each version of the MHC gene codes protein by-products that are excreted from the body, and they have a unique odor. Mice that have damage to their olfactory nerve or olfactory epithelia cells perform this test at chance levels-deciding on the heterozygous mate only about half of the time.

So if you're a smart rodent, a big part of your mate selection process is in deciding if a suitor has the right smell. Mice that are most attracted to the smells of potential mates with dissimilar versions of MHC genes will be less likely to inbreed and will maximize the genetic fitness of their offspring. Can such a process be important for human mate selection? The fact that perfume and cologne sales account for approximately 12 to 15 percent of annual consumer luxury item spending suggests that we believe smell is a key factor in shaping our own attractiveness.

Intrigued by the idea that humans may use a very similar process to select mates, evolutionary psychologist Chris Wedekind and his colleagues conducted an experiment in which they asked more than one hundred men and women to score the odor of T-shirts worn for two consecutive days by male and female subjects. Each person tested was brought into a room with six odorous T-shirts stored in separate plastic containers and asked to rank them in terms of their "s.e.xiness" and "pleasantness." The results were surprising.

Scores of the pleasantness and s.e.xiness were indeed found to relate to the degree of MHC similarity between the smeller and the T-shirt wearer. For most subjects, the most pleasant and s.e.xy smells were a.s.sociated with members of the opposite s.e.x whose MHC genes had the least overlap with their own. When asked why they liked a specific smell, many subjects offered that it reminded them of their present lover or an ex-mate. Interestingly, lower-ranking odors were said to remind the smeller of a sibling or other relative. This is one case where opposites definitely attract, and for a good reason-the observed mating preferences stemming from these choices would naturally increase immune system heterozygosity of the offspring.

In this mechanism we find that there is no single attractive smell that works for everyone-one person's sentir bon sentir bon may repulse another. To take advantage of this adaptation, lonely singles in search of a mate would have to get a genetic fingerprint of his or her intended before a scent could be custom-designed. But all hope is not lost. In 2001, Wedekind's group showed that we unwittingly use our own MHC geneotype information in choosing perfume and cologne for personal use. In this study 137 male and female students who had been typed for MHC were asked to rate 36 different scents for personal use-"Would you like to smell like that yourself ?" The researchers found a significant correlation between MHC genotype and scent rankings, indicating that people with similar MHC alleles preferred to wear similar-smelling perfumes. These results suggest "that perfumes are selected 'for self ' to amplify in some way body odors that reveal a person's immunogenetics." While it is commonly a.s.sumed that perfumes are worn primarily to mask a person's natural odors, Wedekind has argued that we actually prefer to wear scents that accentuate these olfactory cues, announcing our MHC genotype through a form of olfactory advertising. may repulse another. To take advantage of this adaptation, lonely singles in search of a mate would have to get a genetic fingerprint of his or her intended before a scent could be custom-designed. But all hope is not lost. In 2001, Wedekind's group showed that we unwittingly use our own MHC geneotype information in choosing perfume and cologne for personal use. In this study 137 male and female students who had been typed for MHC were asked to rate 36 different scents for personal use-"Would you like to smell like that yourself ?" The researchers found a significant correlation between MHC genotype and scent rankings, indicating that people with similar MHC alleles preferred to wear similar-smelling perfumes. These results suggest "that perfumes are selected 'for self ' to amplify in some way body odors that reveal a person's immunogenetics." While it is commonly a.s.sumed that perfumes are worn primarily to mask a person's natural odors, Wedekind has argued that we actually prefer to wear scents that accentuate these olfactory cues, announcing our MHC genotype through a form of olfactory advertising.

In this chapter we've seen that there are a few treasured scents that are universally appealing. Floral and fruity smells top the list in most countries, probably because they signify the presence of nutritious food sources. Newborns and children alike are attracted to these scents, independent of the culture in which they were raised.

Newborns and infants are also universally attracted to the smell of their own amniotic fluid and those that are breast-fed come to a.s.sociate maternal odors with the arrival of food. Attraction to maternal odors has obvious survival benefits by keeping the offspring in close proximity to its mother.

We have been wired by natural selection factors to find pleasure in these and similar smells because they have survival value. Pheromones, on the other hand, have a different kind of universal appeal. While no single odor is pleasurable to everyone, the rule is very simple (and universal): s.e.xy/pleasurable smells signify the presence of potential mates that can lead to viable offspring.The pleasure we find in these "hidden" scents is driven not by natural selection factors, but rather through s.e.xual selection because these adaptations have clear reproductive value.

In the next chapter we turn our search for pleasure toward the epicurean in us all. We will discover that our l.u.s.t for certain tastes fosters normal immune system and brain development, but at a growing cost to public health in Western societies.

Chapter 6.

For the Love of Chocolate As life's pleasures go, food is second only to s.e.x.

Except for salami and eggs. Now that's better than s.e.x, but only if the salami is thickly sliced.

-Comedian Alan King

Music with dinner is an insult both to the cook and the violinist.

-G. K. Chesterton

If you ever make it to the Amazon, ask your guide to show you what is likely the most revered tree throughout all of South and Central America. The theobromo cacao theobromo cacao, or "food of the G.o.ds," was named by Linnaeus, the great eighteenth-century cataloger of nature. The designation makes clear his admiration for the almost indescribably savory taste of its fruit and seeds as well as the role of the tree in world history. Before taking a bite, few people stop to think-and who can blame them?-about the influence of chocolate on the social, political, and economic evolution of those cultures that came in contact with cacao beans as they spread from equatorial America to Europe, and then Asia.

After a short trek into the jungle, your guide will stop in front of an odd-looking tree, probably no taller than ten meters or so. If it is a mature tree-older than three years-it will have large patches of pink or blue cauliflorous growth on its bark, but your eyes will skip right past this feature and focus on the strange football-size pods that dangle expectantly from its trunk. The outer covering of the tree's fruit is a tough hide of corrugated green and yellow, which when broken reveals a soft, whitish pulp. The taste of the pulp will catch you off guard. Most people antic.i.p.ate the tangy sweet flavor of fruit with their first bite, only to be surprised by the subtle, bittersweet taste of chocolate. Enveloped inside the pulp are dark, purple-colored seeds-about thirty to forty per pod-that after being dried and processed can be recognized by epicureans around the world as "chocolate beans."