INTRODUCTION

Retronasal Smell and the New Age of Flavor

The origins of this book are the cooked meal around the family dinner table that my wife, Grethe, and I have shared at the end of each day beginning when we were students together.

Her interests run to food (as a gourmet cook), books (as a reference librarian and an avid reader), flowers and gardens (at our homes in the United States and Denmark), travel, friends, opera, and keeping tabs on our growing family. My life has been in the laboratory, studying the part of the brain responsible for the sense of smell. Through the years—from England to Washington, D.C., Stockholm to New Haven, Philadelphia to Paris, our home in Connecticut to our summer house in Denmark—through student life and family life, that shared meal has been a constant bond. A sip of sherry or wine or fruit juice, with a nibble, to prepare the digestion for a traditional meal, with meat, vegetables and salad, a glass of wine, dessert or fruit, and tea (coffee is for the morning), that varies every day. Always with Grethe’s elegant touches drawn from her native Denmark and the places we’ve lived and visited, and from burgeoning piles of recipes clipped from newspapers and magazines from around the world. We treasure the time to enjoy the flavors of the food while reflecting on the events of the day.

This daily routine would have gone on without reflection except that in 1986, National Geographic prepared its historic article “The Intimate Sense of Smell,” the first comprehensive public overview of this neglected sense. As an olfactory scientist, I was interviewed by the author. You may have seen photographs from this article, the most notorious being of a row of young men stripped to the waist with upraised arms while a row of pleasant middle-aged women in white lab coats have their noses buried in the boys’ armpits, testing the effectiveness of the latest underarm deodorant.

The article started by noting the common idea that smell seemed to have faded in importance for humans when our ancestors started walking upright, relying on the visual sense: “But to Gordon Shepherd, a Yale University neuroscientist, people vastly underrate their sense of smell. ‘We think our lives are dominated by our visual sense,’ he said, ‘but the closer you get to dinner, the more you realize how much your real pleasure in life is tied to smell. It taps into all our emotions. It sets the patterns of behavior, makes life pleasant and disgusting, as well as nutritious.’”

When the author read back to me this quotation that he was planning to use, I protested that I must have phrased it more elegantly, but he insisted that it was what I had said so that is the way it stayed. Anyway, my main point was to oppose the common wisdom that the sense of smell has become weak and insignificant in humans (unless you are a perfumer) by remembering what the aromas and flavors of those daily dinnertimes had meant to me.

Later, it began to dawn on me that I must be pretty dense to be working all my life on the physiology of the sense of smell without trying to figure out how it applied to enjoying my evening meal. It was time for me as a neuroscientist to think about how those smells from the food in my mouth were able to reach the sensory cells deep inside my nose, and how those smells were merged with other sensations to produce flavor.

Searching for those answers sent me on an odyssey that has been fascinating every step of the way. It has introduced me to many investigators working in areas unknown to one another, to the mainstream of neuroscientists, and to the general public. I learned about food scientists, who study how food is chewed in the mouth and how it is swallowed. Physiologists study how the smells are carried to the sensory cells in the nose by our breathing in, as when inhaling the aroma of a cup of coffee, and by breathing out, as when we chew and swallow our food. Psychologists study how smell is combined with taste and the other senses to produce what is called taste but is really flavor, one of the most complex of human sensations. Cognitive neuroscientists use brain imaging to show how flavor arises from activity at the highest cognitive levels of our brains. Neuropharmacologists study how the regions of the brain that are activated by cravings for food involve some of the same regions that are activated by cravings for tobacco, alcohol, and drugs of abuse. Biochemists identify the hormones that circulate in the blood, connecting our bodies with our brains to signal to start eating when we are hungry and stop when we are full. Anthropologists speculate that cooked food was a major driving force in human evolution. Molecular biologists have discovered that the sensory receptors for smell form the largest gene family in the genome, and they are studying how the molecules give rise to our perceptions of different smells. And we are good smellers: behavioral psychologists find that monkeys as well as humans have much more sensitive senses of smell than previously recognized.

All these investigators, most of them without knowing one another’s fields, are building the new science of flavor. In addition, food critics have been pushing and pulling us into a new age of food appreciation. They include Harold McGee, whose book On Food and Cooking: The Science and Lore of the Kitchen has educated thousands and entertained them with the ways in which foods give rise to flavors. An important step on this path was taken by Nicholas Kurti and Hervé This, who became fascinated with the “physical and chemical aspects of cooking” and began to hold workshops on their new passion. They helped a new field to emerge, defined in This’s book Molecular Gastronomy: Exploring the Science of Flavor as the science dealing “with culinary transformations and the sensory phenomena associated with eating.”

Among all this work, several things stood out to me:

1. When we sense the flavor of the food in our mouths, it is not by sniffing in, which we usually associate with smelling something like an aroma, but by breathing out, when we send little puffs of smell from our food and drink out the back of our mouths and backward up through our nasal passages as we chew and swallow. This back door approach is called retronasal smell (retro=backward); we can also call it mouth-smell. It contrasts with orthonasal smell (ortho = forward), which is what we call the common sniffing-smell.

2. As delivered by the retronasal route, smell dominates flavor. We often characterize our food in terms of how it “tastes,” but the sense of taste as properly defined consists of sensitivity only to sweet, salt, sour, bitter, and umami. What we call the taste of our food beyond these simple sensations should be called flavor and is mostly due to retronasal smell. Retronasal smell is the new frontier for studies of smell and flavor and is the dominant factor around which to build a field to study how the brain creates our sense of flavor. Simple tastes are hardwired from birth, whereas retronasal smells are learned and thus open to individual differences. They account, therefore, for the vast variety of cuisines in the world—and for why everyone who walks into a McDonald’s wants a different combination of burger, nuggets, fries, salad, dressing, pastry, and cola. Vive la différence!

3. Our own studies have shown that sniffing in a smell gives rise to a spatial pattern of activity in the brain. These patterns function as images of smell, with different images for different smells, much as different faces form different images in our visual system. Human brains are very good at recognizing faces, which can be thought of as a highly developed form of pattern recognition. From our studies we think that the same ability occurs with the patterns laid down by smells—that is, the ability to recognize many different patterns representing as many different smells.

4. Humans have big brains. Although our sensory apparatus may not possess as many receptor molecules or receptor cells as that of other mammals, this fact should not prevent us from having a strong sense of smell. Humans do not have ears or eyes as sensitive as those of some of our animal brethren, either, but this did not prevent our ancestors from developing advanced abilities such as language, because we had large brains that could carry out complex processing not possible with smaller brains. During my odyssey through the different flavor fields mentioned, I wrote an article in 2004 to put forward the new hypothesis of the high abilities of the human sense of smell, which I called “The Human Sense of Smell: Are We Better Than We Think?” My colleague Avery Gilbert, who himself has written an excellent book on smell, What the Nose Knows: The Science of Scent in Everyday Life, sent me an e-mail with the comment that my title was not quite right. He said it should have been “The Human Sense of Smell: It Is Better Because We Think.” Precisely. The big brain is especially important for flavor. A key premise of this book is that humans have a much more highly developed sense of flavor because of the complex processing that occurs in the large human brain. It is this high level of processing—including systems for memory, emotion, higher cognitive processing, and especially language—that give us what I call our unique human brain flavor system.

In summary, up to now the focus of food science has been on relating the composition of the food to the perceptions of the flavors. Some of the explanations have begun to reach into the mechanisms of the brain. What is now needed is to begin with the brain, and show not only how it receives the sensory stimuli, but how in doing so the brain actively creates the sensation of flavor. It is important to realize that flavor does not reside in a flavorful food any more than color resides in colorful object. Color arises as differences in wavelengths of light given off by an object; our brains transform those wavelengths into color to give it meaning for our behavior. Similarly, the smells that dominate the sense of flavor arise as differences between molecules; our brains represent those differences as patterns and combine them with tastes and other senses to create smells and flavors that have meaning for our perceptions of food.

Understanding how the brain does this constitutes a new science of flavor. In 2006, after the article on how the human sense of smell is better than we think, I reviewed the different fields of study contributing to the new understanding of the brain and flavor for a special issue of the journal Nature called “Nature Insight.” I needed a term to apply to all these fields coming together in the study of flavor, and the word neurogas-tronomy popped out, so that is what I will call it. It builds on the old term gastronomy—first conceived by the ancient Greeks to apply to eating well and living well, and popularized as such in France in the early nineteenth century—and adds neuro to represent the brain. Other fields start with the food, and ask how it stimulates the senses. Neurogastronomy starts with the brain, and asks how it creates the sensations of the food.

This new field is timely. In the past few years, the role of smell in flavor, and the way in which it arises internally from the back of the mouth, have received increasing research interest. However, this role still remains hidden to most people. I am a little shocked when I talk about my newfound passion for retronasal smell and its role in flavor and some of my science colleagues express surprise on hearing that we sense flavor when we breathe out, and that flavor is not all due to taste. How can we hold informed opinions on food and nutrition, gourmet eating, fast food, and obesity if the role of smell is not recognized and understood for its dominant function in the perception of flavor, if flavor itself is not recognized for the dominant role it plays in our daily lives, and if the brain regions involved in cravings for food are not recognized to be the brain regions involved in cravings for drugs of abuse? It is time for a new appreciation of how the brain creates smell and flavor for the twenty-first century.

This book lays out some key elements of the new science.

Chapter 1 gives background on the new ways of thinking about smell as a dominant sense for humans because of its central role in producing flavor. Chapter 2 shows how a dog’s sense of smell is beautifully adapted for tracking while sniffing in, whereas a human’s is equally beautifully adapted for flavor while breathing out. Chapter 3 warns about how the mouth fools the brain into thinking it is producing all the flavor, with experiments you can do to prove it to yourself. Chapter 4 provides an introduction to the molecules in food that give them the flavor that the brain creates.

Chapters 5 through 12 describe the smell pathway in all its glory as the main actor in the flavor system, focusing on the new evidence that the information in the smell molecules is represented in the brain as a smell image, that this occurs through retronasal smell, and that it is subject to a basic neural operation called lateral inhibition to enhance discrimination. We take a detour along the way to show how a smell image draws on our understanding of how complex images in vision work, such as in recognizing faces. Chapters 13 to 16 then show how the other senses—taste, touch, vision, and hearing—play their own important roles in the total sensation of flavor. Chapter 17 brings in all the muscles and movements that bring about the sensing of what is in the mouth and how it leads to retronasal smell.

All this complex machinery is summarized in chapter 18 as the “human brain flavor system,” which is at the heart of neurogastronomy. This system is closely interconnected with regions of the brain that produce emotion by creating “images of desire,” as discussed in chapter 19. Chapter 20, through the iconic tale of Proust and his madeleine cookie, highlights the power of flavor to evoke memories. Chapter 21 shows how fast foods capture the human brain flavor system with excessive activation, and how this leads to poor nutrition and obesity. Why do we choose the foods we do? Chapter 22 introduces the reader to the new field of neuroeconomics. As applied to the brain, it seeks to explore how the flavor system makes decisions that lead us to eat healthy or unhealthy foods. There is increasing evidence that loss of control over those decisions involves the same parts of the brain involved in drug addiction. All of this activity occurs in brain microcircuits that are plastic; that is, our brains are changed by their own activity, as explained in chapter 23. Chapter 24 addresses the fascinating and frustrating link between smell and language, suggesting that smell shares with vision and hearing the challenge of using words to characterize complex images. Chapter 25 explains how perception of smell and flavor gives us new insights into the neural basis of consciousness. The dominant role of retronasal smell in our daily eating behavior implies that it must have played an important role in the evolution of the human brain, a new hypothesis that is discussed in chapter 26.

Why all this matters for public policy is discussed in chapter 27, which addresses key questions of how the brain begins before birth to create flavor preferences that can last a lifetime; how infants and children are especially attracted to both healthy and unhealthy flavors; what the relation is between flavor and nutrition; the critical role that flavor plays in diseases such as obesity and hypertension; and finally, how to use flavor to make better lives for the ill and the elderly.