For a long time, the mechanisms of taste seemed relatively straightforward. For one thing, it's been all about the tongue, that exposed sensory muscle lying limp in our mouth. Ever since Democritus hypothesized in the fourth century B.C. that the sensation of taste was an effect of the shape of food particles, the tongue has been seen as a simple sensory organ. Sweet things, according to Democritus, were “round and large in their atoms,” while “the astringently sour is that which is large in its atoms but rough, angular and not spherical.” Saltiness was caused by isosceles atoms, while bitterness was “spherical, smooth, scalence and small.” Plato believed Democritus, and wrote in Timaeus that differences in taste were caused by atoms on the tongue entering the small veins that traveled to the heart. Aristotle, in turn, believed Plato. In De Anima, the four primary tastes Aristotle described were the already classic sweet, sour, salty, and bitter.

Over the ensuing millennium, this ancient theory remained largely unquestioned. The tongue was seen as a mechanical sensor, in which the qualities of foods were impressed upon its papillaed surface. The discovery of taste buds in the 19th century gave new credence to this theory. Under a microscope, these cells looked like little keyholes into which our chewed food might fit, thus triggering a taste sensation. By the start of the 20th century, scientists were beginning to map the tongue, consigning each of our four flavors to a specific area. The tip of our tongue loved sweet things, while the sides preferred sour. The back of our tongue was sensitive to bitter flavors, and saltiness was sensed everywhere. The sensation of taste was that simple.

If only. We now know that our taste receptors are exquisitely complicated little sensors, and that there are at least five different receptor types scattered all over the mouth, not four. (The fifth receptor is sensitive to the amino acid glutamate, aka umami.) Furthermore, the tongue is only a small part of flavor: As anyone with a stuffy nose knows, the pleasure of food largely depends on its aroma. In fact, neuroscientists estimate that up to 90 percent of what we perceive as taste is actually smell. The scent of something not only prepares us for eating it (our salivary glands become active), but gives the food a complexity that our five different taste sensations can only hint at. If our tongue is the frame for the food - providing us with crucial information about texture, mouthfeel and the rudiments of taste - the sensations of our nose are what make the food worth framing in the first place.

Perhaps the most shocking discovery from this new science of taste, however, is that the act of eating is not the only source of gustatory pleasure. Instead, a big chunk part of our sensory delight – the joy that makes us crave particular foods – comes afterwards, when the food is winding its way through the gut. Look, for instance, at a recent paper in Neuron, led by a team of scientists at Duke. They came up with a clever paradigm for isolating this more indirect pleasure pathway: They studied mice without a functional TRPM5 channel, which is essential for detecting sweetness. As a result, these mutant mice showed no immediate preference for sugar water.

But here comes the cool part of the experiment. The scientists then allowed the mice to spend some time with the sugar water and normal water. After a few hours, it became clear that the mutant mice greatly preferred the sugar water, even though they couldn't taste the sugar. (A control experiment with sucralose, an artificial sweetener, demonstrated that the rats were responding to the caloric intake, not the sweet taste.)

Finally, the scientists measured dopamine levels (via in vivo microdialysis) in the nucleus accumbens (a brain area that processes rewards) in the mutant mice and normal mice.* While normal mice exhibited an increase in dopamine in response to both fake sugar and real sugar — the reward was the sweet taste — the mutant mice only demonstrated a dopaminergic spike when consuming genuine sugar water. What they enjoyed were the calories. As the authors conclude:

We showed that dopamine-ventral striatum reward systems, previously associated with the detection and assignment of reward value to palatable compounds, respond to the caloric value of sucros in the absence of taste receptor signaling. Thus, these brain pathways...also perform previously unidentified functions that include the detection of gastro-intestinal and metabolic signals.

This is fascinating, no? We are so convinced that the tongue is the source of culinary joy – we eat too much ice cream because we want to make our mouth happy – but it's not. Instead, we eat calorically dense foods because we are also trying to pleasure this secondary pathway, which responds not to the nuances of flavor but to the brute intake of energy. (On a more depressing note, this research also explains why the obesity epidemic is so hard to fix. Let's imagine, for instance, that some genius invented a reduced calorie bacon product that tasted exactly like bacon, except it had 50 percent fewer calories. It would obviously be a great day for civilization. But this research suggests that such a pseudo-bacon product, even though it tasted identical to real bacon, would actually give us much less pleasure. Why? Because it made us less fat. Because energy is inherently delicious. Because we are programmed to enjoy calories.)

Of course, it makes evolutionary sense that we'd have an internal mechanism for detecting energy. After all, that's what keeps us alive – the body has a way of learning to love what it needs.

However, a brand new paper, published in The Journal of Neuroscience by scientists at the University of Colorado, extends this line of thinking to that fifth taste sensation, umami. Once again, the researchers began by studying a strain of mutant mice that were utterly unable to enjoy glutamate. This is roughly equivalent to a human who doesn't like the taste of aged cheese, or a well grilled steak, or a ripe tomato. (All of these foods are rich in umami.) While these mice didn't seem to prefer umami at first, they eventually learned to prefer it to a non-umami alternative, suggesting that they had an alternate means of enjoying the tastant. (The scientists used water flavored with MSG, or monosodium glutamate, as the bait. MSG is just umami in concentrated form. This research helps explain why food manufacturers have been seasoning their canned soups and processed products with MSG for decades.) By looking at patterns of activity inside the mouse brain, the scientists were able to see that, although the mutant mice were missing that immediate rush of protein pleasure, they did show similar neural activity (albeit with a slight lag) in other parts of the brain responsible for representing "viscerosensory" cues. In other words, they were enjoying the sensation of protein via their digestive tract, which is why they kept on coming back to the umami water they couldn't even taste.

This, of course, is perfectly logical. We love the flavor of denatured protein, because, being protein and water ourselves, we need it. Our body produces over 40 grams of glutamate a day, so we constantly crave an amino acid refill. In fact, we are trained from birth to savor umami: breast milk has ten times more glutamate than cow milk. Needless to say, this research is bad news for those admirable souls trying to go vegan, since umami remains mostly easily accessible in meats and cheeses. It turns out that, when we give up animal products, we don't just need to trick the tongue into thinking that those tofu hot dogs are full of glutamate. We also need to pull off an even more difficult deception: We have to convince our stomach and intestines that what we're eating is full of meaty amino acids, or at least MSG.

Photo credit: Celestehodges, via Flickr. Marmite, it turns out, is like an umami speedball - it has the highest concentration of glutamate of any manufactured food product. And yet, it still tastes gross. Sometimes, I don't care what my small intestine wants.