A Fly's Taste Experience Is Much Like Ours

In the first detailed genetic study of fly taste receptors, UC Berkeley neuroscientist Kristin Scott and her colleagues showed that fruit flies have receptors devoted to sweet and bitter tastes just like humans. While human taste receptors are limited to the tongue, the receptors in flies are mounted on bristles scattered all over the body, including the legs, the wings, the food-sucking proboscis and the egg-laying ovipositor.

"Taste neurons basically tell the fly whether food is good or bad to eat," said Scott, an assistant professor of molecular and cell biology at UC Berkeley. "It's pretty amazing that after hundreds of millions of years of evolution, flies and humans still use the same logic for taste detection."

Tracing the taste receptor nerve cells into the brain, Scott and her team showed that fly brains contain a map both of the location on the body and the type or quality of the taste.

Though no one has mapped the taste areas inside mammal or human brains, other senses typically are mapped in the brain by location or quality, but not both. Odors, for example, are perceived by the brain according to what, not where, they are. Touch, on the other hand, is mapped to the brain according to its location on the skin.

"We think there are body maps as well as quality maps in the fly brain because flies need to know where the food is located in order to react properly," Scott said. "If a fly tastes sugar with its leg, it automatically extends its proboscis and eats. If it detects sugar with its proboscis, it just eats."

Scott noted that flies, like mammals, probably also have sour and salt taste receptors, but these have yet to be characterized in any animal. Mammals have a fifth taste receptor, umami, which means "savory" in Japanese and corresponds to the glutamate receptor, as in monosodium glutamate, or MSG.

She and postdoctoral fellow Zuoren Wang, graduate student Aakanksha Singhvi and laboratory manager Priscilla Kong - all with UC Berkeley's Helen Wills Neuroscience Institute and the Department of Molecular and Cell Biology - reported their findings in the June 24 issue of the journal Cell.

Scott said that the taste system of flies is much simpler than the smell or olfactory sensory system. The latter uses 50 different odor detectors to discriminate among thousands of smells, while the 68 taste receptors are reduced to only a few different taste categories in the fly brain. Taste is geared mainly to locating food and deciding whether or not to eat it, without any fine taste distinctions, she said.

This also is true of mammals, whose taste receptors send the brain only the basic taste notes of food. Odor receptors provide the fine discrimination of smells that allows us to distinguish foods and enjoy eating.

"The simplicity of the gustatory map of the fruitfly indicates that it will be a model system to examine how the brain translates chemical cues in the periphery into taste perception and behavior," the authors concluded in their Cell paper.

In the past few years, Scott and her colleagues have been working their way through the 68 genes in the fruitfly, Drosophila melanogaster, that code for taste or gustatory receptors. The seven they've studied so far fall into two distinct groups. Five always occur on a taste neuron with a sixth receptor, called Gr66a, while the seventh (Gr5a) occurs by itself, with no overlap between the two groups.

This scenario matches that found in mammals, where there are 35 receptors that respond to bitter substances and three that respond to sweet, with members of the two sets never expressed on the same nerve cell.

To determine whether the two sets of taste receptors correspond to sweet and to bitter foods, Scott and her team killed individual taste neurons by inserting genes that produced diphtheria toxin.

Each taste bristle hosts two to four taste neurons and one neuron that detects movement (a mechanosensory neuron). Typically, one of the taste neurons expresses receptors from the set of six, while another neuron expresses the lone receptor from the second set. The remaining neurons remain a mystery - they may be specific to salt or sour.

Once the researchers had killed a taste neuron, they tested whether the altered flies could taste bitter or sweet. The typical test involved the proboscis extension reflex - if you stick a fly's foot in sugar water, its proboscis will extend. Using trehalose (diglucose), glucose or sucrose as the sugar and caffeine, quinine, berberine (a medicinal alkaloid) or denatonium - a super-bitter compound used to make toxic chemicals unpalatable - as the bitter, the researchers confirmed that the sets of receptors did indeed respond to sweet and bitter just like the taste receptors of mammals. The largest set responded to bitter compounds because there are a greater variety of bitter compounds in nature.

They then put genes for green fluorescent protein into neurons to trace them back to where they first enter the brain. They found that neurons in the mouthparts, that is, inside the proboscis, sent their information to the front part of the brain's subesophageal ganglion, neurons from the proboscis sent their information to the middle of that region, and neurons from the legs went to the back of the ganglion.

Similarly, bitter notes played out in one area of the brain, while sweet notes lit up a separate area.

As Scott continues her genetic studies of the remainder of the 68 gustatory neurons, she and her lab colleagues also are sticking electrodes in the neurons to see how they respond to sugar and bitter tastes, and how these signals integrate in the brain to affect the behavior of the fly.

The research is supported by a grant from the National Institutes of Health.