Turning taste on and off in the brain

A new study proves that sense of taste is hardwired in the brain, independent of learning or experience.

Most people probably think that we perceive the five basic tastes — sweet, sour, salty, bitter and umami (savory) — with our tongue, which sends signals to our brain "telling" us what we've tasted. However, scientists have turned this idea on its head, demonstrating in mice that they can change the way something tastes by manipulating groups of cells in the brain.

The findings were published in the online edition of Nature.

"Taste, the way you and I think of it, is ultimately in the brain. Dedicated taste receptors in the tongue detect sweet or bitter and so on, but it's the brain that affords meaning to these chemicals."

Charles S. Zuker PhD, professor of biochemistry and molecular biophysics and of neuroscience, a member of the Kavli Institute for Brain Science and the Mortimer B. Zuckerman Mind Brain Behavior Institute, and a Howard Hughes Medical Institute Investigator at Columbia University Medical Center (CUMC), and project leader.

The primary aim of Dr. Zuker's lab is to understand how the brain transforms chemical stimuli into perception. Over the past decade, Dr. Zuker and colleagues have proved there are dedicated receptors for each taste on the tongue, and that each class of receptor sends a specific signal to the brain. More recently, they demonstrated each taste is sensed by unique sets of brain cells, in separate locations in the brain's cortex — generating a map of taste perception in the brain.

The scientists used optogenetics, allowing them to directly activate specific neurons with laser light. Yueqing Peng, a postdoctoral associate in Dr. Zuker's lab, examined whether manipulating neurons in these regions could evoke perception of sweet or bitter, without the mouse actually tasting either. Sweet and bitter were chosen because they are the most critical tastes for animals, including ourselves. Sweet taste identifies energy-rich nutrients, while bitter warns against potentially noxious chemicals.

Zucker: "In this study, we wanted to know if specific regions in the brain really represent sweet and bitter. If they do, silencing these regions would prevent the animal from tasting either, no matter how much we gave them. And if we activate these fields, they should taste bitter or sweet, even though they're only getting plain water."

Which is exactly what they observed. When scientists injected a substance into the mice to silence sweet neurons, the animals could not reliably identify sweet. They could, however, still detect bitter. The animals regained their ability to taste sweet when the drug was flushed from their brain. Conversely, silencing the bitter neurons prevented the mice from recognizing bitter, but they could still taste sweet.

Remarkably, researchers were also able to convince animals they were tasting bitter or sweet, even when drinking only water. During drinking, when researchers activated the sweet neurons they observed behaviors such as greatly increased licking. In contrast, stimulating bitter neurons dramatically suppressed licking, and elicited taste-rejection responses, including gagging.

The researchers also performed optogenetic tests on animals that had never tasted sweet or bitter chemicals, and showed activation of corresponding neurons triggered the appropriate behavioral response.

"These experiments formally prove that the sense of taste is completely hardwired, independent of learning or experience, which is different from the olfactory system.

"Odors don't carry innate meaning until you associate them with experiences. One smell could be great for you and horrible to me."

Charles S. Zuker PhD

In a final set of experiments, animals were trained to report the identity of an oral sweet or bitter taste by performing a task. In the experiments, mice tasted bitter, sweet and salty chemicals sometimes, but at other times researchers activated laser lights to stimulate an animals' sweet or bitter cortical brain field.

The behavior of the mice did not differ between the real tastes and stimulated brain tastes, demonstrating that the light mimicked the perception of bitter and sweet.

"In other words, taste is all in the brain," said Zuker.

Abstract
Taste is responsible for evaluating the nutritious content of food, guiding essential appetitive behaviours, preventing the ingestion of toxic substances, and helping to ensure the maintenance of a healthy diet. Sweet and bitter are two of the most salient sensory percepts for humans and other animals; sweet taste allows the identification of energy-rich nutrients whereas bitter warns against the intake of potentially noxious chemicals1. In mammals, information from taste receptor cells in the tongue is transmitted through multiple neural stations to the primary gustatory cortex in the brain2. Recent imaging studies have shown that sweet and bitter are represented in the primary gustatory cortex by neurons organized in a spatial map3, 4, with each taste quality encoded by distinct cortical fields4. Here we demonstrate that by manipulating the brain fields representing sweet and bitter taste we directly control an animal’s internal representation, sensory perception, and behavioural actions. These results substantiate the segregation of taste qualities in the cortex, expose the innate nature of appetitive and aversive taste responses, and illustrate the ability of gustatory cortex to recapitulate complex behaviours in the absence of sensory input.

The paper is titled, "Sweet and bitter taste in the brain of awake behaving animals." The other contributors are Yueqing Peng (CUMC), Sarah Gillis-Smith (CUMC), Hao Jin (CUMC), Dimitri Tränkner (CUMC and Howard Hughes Medical Institute, Asburn, Va.), and Nicholas J. P. Ryba (National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, Md.).

The study was supported by grants from the National Institute of Drug Abuse (DA035025) and the Intramural Research Program of the National Institutes of Health and the National Institute of Dental and Craniofacial Research.

The researchers declare no financial or other conflicts of interest.

Columbia University Medical Center provides international leadership in basic, preclinical, and clinical research; medical and health sciences education; and patient care. The medical center trains future leaders and includes the dedicated work of many physicians, scientists, public health professionals, dentists, and nurses at the College of Physicians and Surgeons, the Mailman School of Public Health, the College of Dental Medicine, the School of Nursing, the biomedical departments of the Graduate School of Arts and Sciences, and allied research centers and institutions. Columbia University Medical Center is home to the largest medical research enterprise in New York City and State and one of the largest faculty medical practices in the Northeast. For more information, visit cumc.columbia.edu or columbiadoctors.org.

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New study proves that a sense of taste is hardwired in the brain,
independent of learning  or experience.
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