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The Sweet Taste of Expectation
Alfredo Fontanini, M.D., Ph.D.
Photo courtesy of Dr. Fontanini
You were late getting to the awards luncheon. When you arrived, the kitchen staff had already removed the entrees and so all you could toss onto your plate was some hastily assembled salad—but at least there were a few of those small grape tomatoes that you love. Grabbing one of the last seats at a table, the lights went down and you speared a tasty oval with your fork, popped it in your mouth and looked forward to the juicy burst of tomato goodness. Except that’s not what you got. What you got instead was something dense and rubbery and with a flavor that you couldn’t figure out at first until you realized that you were chewing on an olive.
What happens during that moment when expectation and sensation meet in the mouth is what fascinates Alfredo Fontanini, M.D., Ph.D., an NIDCD grantee and 2010 winner of the Presidential Early Career Award for Scientists and Engineers (PECASE), the highest honor given by the United States government to science and engineering professionals in the early stages of their independent research careers. He and his laboratory team at Stony Brook University in New York study the gustatory cortex, the area of the brain that processes and interprets taste. In his way of looking at things, taste isn’t just a straight-up report from the taste buds on our tongue. His studies suggest taste is created in the brain and that psychological states—anticipation, expectation, and attention—have such a profound influence on the process that no two bites, or sips, taste exactly the same.
Recently, Dr. Fontanini and his team have been studying the impact of expectation on taste processing by measuring the responses of neurons in the gustatory cortex of rodents to specific cues and taste stimuli. “We train our rodents on a go/no-go task that uses two auditory tones—one signals the availability of a pulse of sugar water and the other the availability of a pulse of bitter water—and there’s a lever that the rat can push to get a taste,” he says. Over time, the animals learn to press the lever following the "sweet" tone and not to press when they hear the "bitter" tone, and their behavior tells the researchers that they have learned to expect specific tastes on the basis of the auditory cues.
Looking at how the neurons respond in the gustatory cortex, Dr. Fontanini and his teammates observed that their response becomes cue specific. Distinct subsets of neurons display patterns of unique activity that are specific to either the anticipation of something sweet or something bitter.
To further test the role of expectation, they fooled their subjects. “We play the sweet tone,” says Dr. Fontanini, “but sneak in a taste of bitter to see how neurons respond to misleadingly cued tastes. What we see is something that looks more like the response to sweet, particularly at the beginning—as if just the expectation itself biases the response—and then it eventually converges into a response that looks like bitter.” The neurons also took a longer amount of time to eventually exhibit bitter-specific activity.
These findings suggest that what goes on in the gustatory cortex isn’t just neurons encoding what they receive from taste receptors on the tongue. Apparently, just the expectation of what you’re about to taste is enough to create taste-specific activity in the gustatory cortex that, along with sensory information from the tongue, ultimately shapes the neural coding for taste.
According to Dr. Fontanini, this approach to taste integrates the study of two systems—the sensory system and the reward system—that have traditionally been studied separately. The common wisdom has been that sensory systems receive information from the outer world and expectation is processed in another area (or areas) of the brain. But what Dr. Fontanini’s research appears to be telling us is that reward areas are communicating directly with sensory areas to determine expectations and emotions.
If so, then the study of taste offers an excellent model to understand how any kind of sensory stimuli is shaped by psychological state. “In taste, the hedonic value—whether it tastes good or it tastes bad—is so central to perception,” says Fontanini, “that it offers the unique possibility to study how sensory and emotional processes are intermingled.”
The implications of these studies could go beyond a better understanding of taste coding in the brain and also lay the groundwork for other researchers to begin to explore potential neural networks involved in eating disorders, addictions, and depression—all of which are characterized by alterations in reward systems.