By Daniel Dunaief

Pull into the parking lot of your favorite restaurant and you can almost taste the onion rings, the fresh baked bread or the steamed clams. The combination of the sign, the smell of the food piped out of the familiar building, and even the familiar voice of the restaurant owner welcoming you back is a hint of the experience of eating. Indeed, when these anticipatory stimuli are a part of the dining experience, they contribute to forming flavor.

Alfredo Fontanini, an associate professor in the Department of Neurobiology & Behavior at Stony Brook University, recently conducted research on rodents in which he explored how other senses — touch, taste, smell and sight — contributed to the part of the brain responsible for taste, the gustatory cortex.

In work published recently in the journal eLife, Fontanini demonstrated that rats who heard particular sounds, smelled odors, felt a puff of air against their whiskers, or saw the flash of an LED light before they ate showed increased activity in the gustatory cortex even before they started eating. If this experiment sounds familiar, it’s because Russian scientist Ivan Pavlov demonstrated the anticipation of food in conditioning experiments with dogs, showing that their digestive systems became active when they heard a tone before they ate, associating the sound with the presentation of food.

Fontanini took this research further, however, showing that the brain regions responsible for taste can, and did, show activity prior to eating. “As we paired the stimuli in a Pavlovian task, the animal would produce mouth movements and licks in response,” Fontanini said. These movements were not there right away, but developed after three to seven days of training, suggesting that the animal could infer taste. He recorded the responses of single neurons in the gustatory cortex. Before conditioning, the neuronal response in the gustatory cortex varied according to the sense stimulated. Prior to training, neurons in the gustatory cortex showed a 16 percent response, while that went up to 33 percent after learning. “This suggested that the stimulation was predictive of taste,” Fontanini said. “More neurons were integrating between all the stimuli.”

Donald Katz, a professor of psychology at Brandeis University who oversaw Fontanini’s graduate research for five years, suggested that his former student was one of a few neuroscientists studying how anticipation of an experience, knowing what’s coming, impacts how the brain handles that experience. This study, he explained in an email, “makes perfect sense — while few researchers study how different sensory systems work together, it is well-known that taste is linked to all of the other senses. It is of great evolutionary import that this be so,” because the animal that can recognize something good to eat at the greatest distance will be the one that eats.

Katz described Fontanini’s recent work as a “wonderful finding in that it provides a substantial, natural extension” to work completed in his lab, Katz’s lab and those of other scientists. In exploring which specific senses are most important to the gustatory reflex, Fontanini said olfaction and touch are considered more relevant for food-related decisions. “These are animals that use these senses to navigate their world and explore food,” he said.

In the bigger picture, Fontanini would like to understand how the brain integrates and fuses sensory perceptions with emotions. He explained that one of the tests in animal models of depression is to look at how much a test subject still likes something sweet. “Studying taste allows us to understand how the brain creates pleasure or creates aversion that negates emotions,” he said.

Fontanini plans to extend this study to additional research. He would like to know the neurological pathways that link the visual, auditory, somatosensory and olfaction senses that contribute to forming an expectation about taste. He is also eager to understand how the anticipatory activation influences the way taste is perceived. This, he explained, would be a way to explore how expectations shape perception.

Fontanini, who grew up in the town of Brescia, Italy, which is near Milan, arrived at this particular field of research because of his interest in understanding perception and emotion. He would like to explore how the brain creates emotions. Recognizing the multisensory element to taste and eating, Fontanini suggests that understanding how olfaction and taste can interact may lead to eating sweets where the smell enhances the flavor and taste, even of a lower-calorie dessert, like a piece of chocolate cake. “If you can leverage more of the odor and less” of the taste, “you can find a way of having that richness without the need for overwhelming sweetness.”

A resident of Setauket, Fontanini lives with his wife Arianna Maffei, who is an associate professor in the Department of Neurobiology & Behavior at Stony Brook and their 11-year-old son Carlo. Relying on vocabulary of the gustatory cortex, Fontanini suggested Long Island has a “soothing sweetness” that springs from the quaint and beautiful setting his family enjoys.

As for his work, Fontanini said studying taste in the brain is challenging. “What happens when you taste chocolate: are you activating chocolate neurons or are you activating a complex pattern of activity?” The answer, he said, describing taste while borrowing from another sense, is much more like a musical ensemble during a symphonic experience than like a solo. “Understanding how taste is represented in the cortex is incredibly complex,” he said.