Bitter-sweet processing in larval Drosophila.
"Sweet-" and "bitter-" tasting substances distinctively support attractive and aversive choice behavior, respectively, and therefore are thought to be processed by distinct pathways. Interestingly, electrophysiological recordings in adult Drosophila suggest that bitter and salty tastants, in addition to activating bitter, salt, or bitter/salt sensory neurons, can also inhibit sweet-sensory neurons. However, the behavioral significance of such a potential for combinatorial coding is little understood. Using larval Drosophila as a study case, we find that the preference towards fructose is inhibited when assayed in the background of the bitter tastant quinine. When testing the influence of quinine on the preference to other, equally preferred sweet tastants, we find that these sweet tastants differ in their susceptibility to be inhibited by quinine. Such stimulus specificity argues that the inhibitory effect of quinine is not due to general effects on locomotion or nausea. In turn, not all bitter tastants have the same potency to inhibit sweet preference; notably, their inhibitory potency is not determined by the strength of the avoidance of them. Likewise, equally avoided concentrations of sodium chloride differ in their potency to inhibit sugar preference. Furthermore, Gr33a-Gal4-positive neurons, while being necessary for bitter avoidance, are dispensable for inhibition of the sweet pathway. Thus, interactions across taste modalities are behaviorally significant and, as we discuss, arguably diverse in mechanism. These results suggest that the coding of tastants and the organization of gustatory behavior may be more combinatorial than is generally acknowledged.
Department of Genetics, Institute of Biology, University of Leipzig, Talstr. 33, 04103 Leipzig, Germany, Research Group Molecular Systems Biology of Learning, Leibniz Institute for Neurobiology, Brenneckestr. 6, 39118 Magdeburg, Germany.
Christian
C
König
Department of Genetics, Institute of Biology, University of Leipzig, Talstr. 33, 04103 Leipzig, Germany, Department of Genetics of Learning and Memory, Leibniz Institute for Neurobiology, Brenneckestr. 6, 39118 Magdeburg, Germany.
Michael
M
Schleyer
Department of Genetics, Institute of Biology, University of Leipzig, Talstr. 33, 04103 Leipzig, Germany, Department of Genetics of Learning and Memory, Leibniz Institute for Neurobiology, Brenneckestr. 6, 39118 Magdeburg, Germany.
Judith
J
Leibiger
Department of Genetics, Faculty of Agriculture, Tanta University, Tanta-Kafr El-Sheikh Road, Seberbay Campus, 31527 Tanta, Egypt.
Amira
A
El-Keredy
Department of Genetics of Learning and Memory, Leibniz Institute for Neurobiology, Brenneckestr. 6, 39118 Magdeburg, Germany, Institute of Biology, Otto von Guericke University of Magdeburg, Universitätsplatz 2, 39106 Magdeburg, Germany and Center for Behavioral Brain Sciences, Universitätsplatz 2, 39106 Magdeburg, Germany bertram.gerber@lin-magdeburg.de.
Bertram
B
Gerber
D000818:Animals; D004330:Drosophila / Q000254:growth & development / Q000502:physiology*; D005518:Food Preferences; D007814:Larva / Q000502:physiology; D008297:Male; D009474:Neurons / Q000378:metabolism; D011803:Quinine / Q000378:metabolism; D012965:Sodium Chloride / Q000378:metabolism; D013395:Sucrose / Q000378:metabolism; D013649:Taste
D012965:Sodium Chloride; D013395:Sucrose; D011803:Quinine
Drosophila; bitter; combinatorial coding; inhibition; sweet; taste