You may like black coffee and gin & tonic now but, rest assured,they're both acquired tastes. Bitter substances are usually repellent and many animals avoid bitter-tasting compounds; flies are no exception! Nicolas Meunier and colleagues show in their recent Journal of Neurobiologypaper that some taste sensilla on the legs of Drosophila respond to bitter compounds and must possess specific receptor molecules to do so.
Receptors for bitter molecules have only recently been discovered in mammals. In Drosophila, a family of putative taste receptor genes has been identified, some of which may encode for receptors tuned to bitter substances. Behavioral studies had shown that quinine (the bitter substance in tonic water) has a repulsive effect on flies. However, it was not known whether flies have taste neurons that specifically respond to such substances.
Taste sensilla on the forelegs of flies usually house four taste neurons that have been classified according to the substances they generally respond best to. There is one for water, one for sugar and two for salts. The sensilla play a role in determining feeding choice. Meunier and colleagues first identified a number of bitter compounds that were effective in influencing feeding behavior. They gave the flies the choice between a blue sugar solution and a red sugar solution mixed with a bitter substance, using the food colorings to check the preferred choice. Fortunately, Drosophila is small enough and has a relatively transparent abdomen, so they could tell from the color that a number of substances that taste bitter to us had been avoided.
But how are bitter substances detected? They could either inhibit the normal taste neuron response to sugar or they could excite specific neurons that signal the presence of a bitter compound, or they could do both.
First, Meunier ruled out the possibility that bitter substances exclusively inhibit the sugar response of taste neurons. A fly usually sticks out its proboscis when a drop of sugar solution is applied to its foreleg. Meunier could decrease the probability of this reflex response when he gave a bitter substance to the other leg before he applied the sugar. This other leg hadn't seen any sugar solution, so the bitter substance could not have just inhibited the taste neurons in this leg that respond to sugar.
Meunier and colleagues went on to test whether they could identify neurons that are responsive to bitter substances by looking directly at neuronal responses. They used small glass capillaries filled with an electrolyte and various combinations of sugar and bitter compounds. These capillaries were placed briefly over the tip of sensillum and served both as a recording electrode and to deliver the stimulus. The action potentials of the four different neurons in a sensillum could be filtered and sorted according to the cell type. It turned out that in some sensilla bitter substances activate the taste neuron called L2, which has been classified as responding best to higher salt concentrations. L2 cells in other sensilla responded best to a different selection of bitter substances, so a range of receptor molecules with different specificities must exist. In addition, bitter substances inhibited the taste neuron that responds best to sugar and the neuron that responds to water. Interestingly, this inhibitory effect was also present in sensilla that showed no response of the L2 cell.
These findings should provide a solid physiological basis for understanding detection and discrimination of bitter compounds in Drosophila. Given the powerful genetic tools available in Drosophila, there is reason to expect that general principles about the molecular mechanisms of chemoreception will eventually emerge.