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Authors: Hervé This

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Tests of species sensitivity to sweetening agents have brought out surpris-

ing differences. For our species, monellin (a protein present in the red berries

of the African shrub
Dioscoreophyllum cumminsii
) is 100,000 times sweeter

than sucrose. Nonetheless, although the taste of this protein is identified by

African nonhuman primates, it is not perceived by American primates. The

same difference is observed in the case of thaumatin, a protein sweetener ex-

tracted from the fruit of another African plant,
Thaumatoccus danielli
. It may

also be encountered in the case of brazzein, identified in 1994 in the creeper

Pentadiplandra brazzeana
.

Differentiation of receptor proteins in the papillary cells of the tongue

probably occurred 30 million years ago, after the separation of the New World

Platyrrhina and the Old World Catarrhina. In their respective environments

these animals found various plants with which they evolved in tandem, eating

the fruits of these plants while dispersing their seeds. In the Americas, where

no protein sweetener has yet been found, coevolution should have caused

new molecules to appear that would not have seemed sweet to Old World

monkeys.

It has been known for several decades that vertebrates are able to detect so-

dium chloride and actively seek it in case of insufficiency. For example, horses

lick salt deposits only if they have to, an observation confirmed by the study of

salt-deprived rats. In natural environments (particularly forests) salt deficiency

is rare, but in 1978 the American biologist John Oates observed that
Colobus

guereza,
a shy monkey that seldom ventures out of its normal tree habitat, comes

down to the ground to eat the leaves of the plant
Hydrocotyle ranunculoides,

which grows in ponds and contains more salt than other available sources.

Natural Medicine

Other primates eat earthy matter even though they do not suffer from salt

deficiency. The soil eaten by
Colobus satanas
(another colobus monkey that

lives in the forests of Gabon) contains less salt than the fruits that make up

an important part of its normal diet, but this behavior occurs during the two

84 | t he physiology of f l a vor

periods of the year when the animal must supplement its diet with mature

leaves (feeding the rest of the year on young shoots and leaves in addition to

flowers, fruits, and grains). These older leaves contain not only molecules of

the polyphenol family (hydroxyl [–oh] groups that attach to benzene rings hav-

ing six carbon atoms) but also tannins, which inhibit the digestion of proteins

by forming complexes with them. Because clay and other soil compounds read-

ily absorb tannins, the geophagy of these monkeys can be explained as a way of

compensating for the ingestion of unwanted plant products. “From your food

you shall make your medicine,” Hippocrates is credited with saying. Could it

be that our primate ancestors whispered this phrase in his ear?

Often an aversion to bitter tastes favors the avoidance not only of dangerous

alkaloids but also of astringent compounds such as tannins, terpenes, sapo-

nins, and strong acids. Nonetheless, not all toxic compounds are bitter: Di-

oscin, a lethal alkaloid found in the yam
Dioscorea dumetorum,
is almost taste-

less. The animal kingdom is protected by the phenomenon of neophobia—the

fear of eating what is new—and by conditioning from postingestive symptoms

that trigger the appearance of an aversion (observed in rats and primates alike).

Even so, chimpanzees are known to heal themselves by eating the bitter plant

Vernonia amygdalina,
generally avoided by healthy animals. This plant con-

tains several steroidal glycosides that are effective in treating gastrointestinal

troubles. What shall we call this type of behavior? Natural medicine?

Food as Medicine
| 85

21

Taste and Digestion

The absorption of monosodium glutamate triggers mechanisms for assimi-

lating proteins.

w h y d o w e s t o p e a t i n g even though only a small quantity of metabolites

has entered the bloodstream? The sensation of a full stomach does not signal

satiety: A rat whose belly has been pumped full of air does not cease to eat.

Through a series of reflexes, however, the organism is able to anticipate the

metabolism of foods. For example, a bit of sugar placed on the tongue triggers

the almost immediate release of glucose by the liver.

Around 1960, Stylianos Nicolaïdis and his colleagues at the Collège de

France observed that the stimulation of the taste receptors by saccharine caused

two hormones to be released by the pancreas: glucagon, which is responsible

for the release of glucose, and insulin, which is responsible for the metabolism

of glucose. Moreover, stimulation of receptors for the sweet taste produces an

anticipated reaction that enables the body to metabolize glucides.

More recently, Nicolaïdis and a team of researchers including Claire Viar-

ouge, Patrick Even, and Roland Caulliez examined reflexes that are triggered

by detection of the taste of proteins and prepare the organism to metabolize

them. One aspect of their investigation involved the ingestion of monosodium

glutamate, which earlier studies had suggested is perceived by the organism

as a signal to begin absorbing proteins. Previously limited to the seasoning

of oriental soups, monosodium glutamate is now very commonly used in the

food industry as a flavor enhancer. In addition to a salty taste, for some peo-

ple it possesses a particular taste called umami that is distinct from the four

86 |

classically recognized tastes (salt, sweet, sour, and bitter); mind you, the classic

theory is wrong, as all good neurophysiologists know. Two questions presented

themselves. First, does monosodium glutamate increase metabolic intensity in

the same way that the absorption of proteins does? Second, does it trigger the

same reflexive release of hormones (glucagon and insulin) as the one normally

induced by the appearance of amino acids in the bloodstream?

To study these questions the team at the Collège de France constructed

a device capable of isolating the various components of the metabolism and

separately recording the metabolic demands associated with locomotion and

thermogenesis, or heat production, in relation to food intake. Thermogenesis

measures metabolic intensity without regard for an animal’s locomotive be-

havior. Experiments performed in 1991 to determine levels of thermogenesis

during periods of activity and in the resting animal showed that stimulation

of rats by intravenous administration of monosodium glutamate in the mouth

and stomach produced only a weak hormonal reaction. Although it induced

an anticipatory reflex, the monosodium glutamate seemed to be effective only

when it was associated with other signals characteristic of food intake.

To test this hypothesis, the physiologists placed cannulas in the mouths of

rats in order to be able to directly inject solutions of monosodium glutamate or

distilled water using a catheter connected to the top of their cage. The rats were

free to move around, and their metabolism was continuously monitored.

Immediately after implantation of the cannulas, the rats were trained to

receive water or monosodium glutamate solutions through these tubes. One

group of rats was injected with various concentrations of monosodium gluta-

mate while they were eating. The other group, used as a control, received only

distilled water during this time.

The physiologists were able to verify that the taste of sodium, when it ac-

companies a complete meal, causes notable metabolic changes. The thermo-

genesis induced by food intake increased much more, and much more rapidly,

in the rats injected with monosodium glutamate than in the control group,

suggesting that monosodium glutamate acts as a sort of protein “saccharine”

capable of misleading the organism by its taste. Although it consisted mostly

of carbohydrates, the meal was perceived as primarily protein.

How long the organism allows itself to be fooled when this gustatory informa-

tion is not confirmed during the course of metabolism and whether the anticipa-

tory reflexes contribute to satiation are questions that remain to be answered.

Taste and Digestion
| 87

22

Taste in the Brain

The cerebral areas activated during the perception of tastes have been

identied by means of nuclear magnetic resonance imaging.

j e a n - a n t h e l m e b r i l l a t - s a v a r i n o b s e r v e d in Meditation 2 of
The

Physiology of Taste,
“Up to the present time there is not a single circumstance

in which a given taste has been analyzed with stern exactitude, so that we have

been forced to depend on a small number of generalizations, such as
sweet,

sugary, sour, bitter,
and other like ones which express, in the end, no more than

the words
agreeable
or
disagreeable,
and are enough to make themselves under-

stood and to indicate, more or less, the taste properties of the sapid body which

they describe. Men who will come after us will know much more than we of

this subject; and it cannot be disputed that it is chemistry which will reveal the

causes or the basic elements of taste.”

Brillat-Savarin was prescient. Today biochemists and neurobiologists know

a good deal about the function of receptor molecules for tastes, which are lo-

cated on the surface of papillary cells on the tongue. Even so, nuclear magnetic

resonance imaging (mri) techniques are helping them better understand how

information perceived by the taste receptors travels up into the brain for pro-

cessing.

With the development of these techniques, which record cerebral activity by

detecting changes in blood flow in the brain, neurobiologists have paid special

attention to cognitive activities such as language, calculation, and memoriza-

tion. Olfaction has been less studied and the perception of tastes completely

88 |

neglected. Barbara Cerf and Annick Faurion of the Laboratoire de Neurobiolo-

gie Sensorielle in Massy and Denis Le Bihan of the Centre Hospitalier d’Orsay

in Paris have identified the cerebral areas activated by taste molecules.

Basic knowledge was rudimentary. The only thing that was known, from

observation of people whose brains had been partly destroyed by wartime inju-

ries, was that the parietal operculum, located near the central sulcus (Rolando’s

fissure), undoubtedly played a role in the perception of tastes. Nonetheless,

electrophysiological studies yielded contradictory results, which pointed in-

stead to another area located in the insula.

Because an mri requires subjects to lie down inside a tunnel-like machine,

they were fed with solutions transmitted through flexible tubes. These con-

straints determined the sapid substances that were tested: The subjects re-

ceived solutions of aspartame (a sweetener), sodium chloride, quinine (bitter

taste), glycyrrhizic acid (licorice taste), guanosine monophosphate (the umami

taste, similar to that of monosodium glutamate, used in Asian cooking), and d-

threonine (indescribable—you have to taste it for yourself). The experimenters

first gave the subjects water, then sapid solutions, then water again, and so on,

in order to forestall habituation while sustaining stimulation for several dozen

seconds, the time needed for the mri device to record a signal.

Lateralization of Taste

The subjects who received these solutions were instructed to concentrate

on their taste in order to minimize interfering activations of other parts of

the brain. The subjects described the intensity of their sensations by moving

a cursor along a graduated scale. By calculating correlations between the vari-

ous perceptual profiles and activations of the different areas of the brain, the

neurobiologists were able to determine which activations were linked to the

perception of tastes. Individual differences were pronounced and the images

noisy, so that many experiments had to be analyzed in order to pinpoint the

areas that were specifically associated with the perception of taste.

The first studies showed that four cerebral areas are activated by sapid

solutions: the insula and the frontal, parietal, and temporal opercula. There

is no single taste center in the brain nor any cerebral areas that are specifi-

cally linked to particular tastes. On the other hand, certain areas that were not

Taste in the Brain
| 89

systematically activated are known to play a role in language comprehension,

hence the hypothesis that the detection of taste may be associated with the act

of naming it.

A second study comparing five left-handed and five right-handed people

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