Their findings, they said, favor a model for taste encoding in the brain that holds that specific cells are dedicated to detecting specific tastes. Competing models hold that multiple neurons combine information to encode taste, or that the timing of patterns of taste information encodes taste.
In their studies, the researchers explored the behavioral effects of activating fly taste neurons that had either of two chemical taste receptors on their surface. In earlier studies, the researchers had shown that the Gr5a receptor on taste neurons was essential for response to sugar and that the Gr66a receptor was essential for response to bitter tastes. However, those studies left open the question of whether those different neurons selectively detected the different tastes and whether they generated taste behaviors.
To directly monitor taste responses of the flies, the researchers generated flies with fluorescent labels on their neurons that would signal activation of one or the other type. They used microscopic imaging through tiny windows in the fly brains to watch neuronal response when they exposed the flies to sweet or bitter chemicals
They found that a whole range of sweet substances selectively switched-on the Gr5a neurons, while a range of bitter substances switched-on the Gr66a neurons. However, the "sweet neurons" did not respond to bitter substances, and vice versa.
In behavioral studies, they found that flies preferred to spend time tasting substances that activated the Gr5a neurons and avoided substances that activated Gr66a neurons.
In the most telling experiments, the researchers engineered flies so that the hot pepper compound capsaicin would selectively switch-on either the sweet-detecting Gr5a neurons or the bitter-detecting Gr66a neurons. Normal flies do not respond to the hot pepper taste.
The researchers found that flies engineered to recognize capsaicin on the sweet-tasting neurons were attracted to the chemical, while those that recognized it as a bitter taste avoided it.
"In this paper, we demonstrate that these taste cells selectively recognize different taste modalities, such that there is functional segregation of taste qualities in the periphery and at the first relay in the brain," concluded the researchers. "Moreover, we show that activation of these different taste neurons is sufficient to elicit different taste behaviors. Thus, activity of the sensory neuron, rather than the receptor, is the arbiter of taste behavior.
Our studies argue that animals distinguish different tastes by activation of dedicated neural circuits that dictate behavioral outputs," they wrote.
The researchers include Sunanda Marella, Walter Fischler, Priscilla Kong, Sam Asgarian, and Kristin Scott of the University of California, Berkeley in Berkeley, CA; Erroll Rueckert of the Howard Hughes Medical Institute and Columbia University in New York, NY. This work was supported by a grant from the NIDCD 1R01DC006252-01, a Burroughs Wellcome Fund Career Award in the Biomedical Sciences, a McKnight Scholar Award, and a Sloan Research Fellowship (to K.S.).
Marella et al.: "Imaging taste responses in the fly brain reveals a functional map of taste category and behavior." Publishing in Neuron Vol. 49, pages 285–295, January 19, 2006, DOI 10.1016/j.neuron.2005.11.037 www.neuron.org
Journal
Neuron