Peripheral coding of bitter taste in Drosophila

Nicolas Meunier 1 2 *, Frédéric Marion-Poll 1, Jean-Pierre Rospars 1, Teiichi Tanimura 2

1INRA Station de Phytopharmacie et Médiateurs Chimiques, 78026 Versailles Cedex, France
2Department of Biology, Graduate School of Sciences, Kyushu University, Ropponmatsu, Fukuoka, 810-8560 Japan

*Correspondence to Nicolas Meunier, INRA Station de Phytopharmacie et Médiateurs Chimiques, 78026 Versailles Cedex, France

Funded by:
* French Ministry of Education and Research
* French Ministry of Foreign Affairs through a Lavoisier program grant delivered by EGIDE
* Ministry of Education, Culture, Sports, Science and Technology of Japan

 
Keywords
taste neurons • bitter compounds • Drosophila • electrophysiology • spikes sorting

 
Abstract
Taste receptors play a crucial role in detecting the presence of bitter compounds such as alkaloids, and help to prevent the ingestion of toxic food. In Drosophila, we show for the first time that several taste sensilla on the prothoracic legs detect bitter compounds both through the activation of specific taste neurons but also through inhibition of taste neurons activated by sugars and water. Each sensillum usually houses a cluster of four taste neurons classified according to their best stimulus (S for sugar, W for Water, L1 and L2 for salts). Using a new statistical approach based on the analysis of interspike intervals, we show that bitter compounds activate the L2 cell. Bitter-activated L2 cells were excited with a latency of at least 50 ms. Their sensitivity to bitter compounds was different between sensilla, suggesting that specific receptors to bitter compounds are differentially expressed among L2 cells. When presented in mixtures, bitter compounds inhibited the responses of S and W, but not the L1 cell. The inhibition was effective even in sensilla where bitter compounds did not activate the L2 cell, indicating that bitter compounds directly interact with the S and W cells. Interestingly, this inhibition occurred with latencies similar to the excitation of bitter-activated L2 cells. It suggests that the inhibition in the W and S cells shares similar transduction pathways with the excitation in the L2 cells. Combined with molecular approaches, the results presented here should provide a physiological basis to understand how bitter compounds are detected and discriminated. © 2003 Wiley Periodicals, Inc. J Neurobiol 56: 139-152, 2003


Received: 12 October 2002; Accepted: 11 February 2003