Drosophila Bitter Taste(s)

Abstract

Most animals possess taste receptors neurons detecting potentially noxious compounds. In humans, the ligands which activate these neurons define a sensory space called "bitter". By extension, this term has been used in animals and insects to define molecules which induce aversive responses. In this review, based on our observations carried out in Drosophila, we examine how bitter compounds are detected and if bitter-sensitive neurons respond only to molecules bitter to humans. Like most animals, flies detect bitter chemicals through a specific population of taste neurons, distinct from those responding to sugars or to other modalities. Activating bitter-sensitive taste neurons induces aversive reactions and inhibits feeding. Bitter molecules also contribute to the suppression of sugar-neuron responses and can lead to a complete inhibition of the responses to sugar at the periphery. Since some bitter molecules activate bitter-sensitive neurons and some inhibit sugar detection, bitter molecules are represented by two sensory spaces which are only partially congruent. In addition to molecules which impact feeding, we recently discovered that the activation of bitter-sensitive neurons also induces grooming. Bitter-sensitive neurons of the wings and of the legs can sense chemicals from the gram negative bacteria, Escherichia coli, thus adding another biological function to these receptors. Bitter-sensitive neurons of the proboscis also respond to the inhibitory pheromone, 7-tricosene. Activating these neurons by bitter molecules in the context of sexual encounter inhibits courting and sexual reproduction, while activating these neurons with 7-tricosene in a feeding context will inhibit feeding. The picture that emerges from these observations is that the taste system is composed of detectors which monitor different "categories" of ligands, which facilitate or inhibit behaviors depending on the context (feeding, sexual reproduction, hygienic behavior), thus considerably extending the initial definition of "bitter" tasting.

Keywords: aversive; behavior; electrophysiology; insects; pheromones; taste.

Figure 1

Gr genes expressed in proboscis taste sensilla (after Weiss et al., 2011). (A) Cellular composition of the different type of sensilla located on the external side of the proboscis. L-type sensilla house four neurons, one of which is sensitive to sugars (S). S-type sensilla house four neurons, including one sugar-sensitive neuron (S) and one sensitive to bitter (B); I-type sensilla house only two taste neurons (B and S). Each of these sensilla also include one mechanoreceptor neuron not represented here. (B) Table showing a map of the expression of the gustatory genes within the different types of sensilla and bitter-sensitive (bitter row) and sugar-sensitive (sweet row) neurons. This map was obtained by establishing GAL4 lines with the promoter of each of these gustatory genes to map the neurons which express these gustatory genes.

Figure 2

Bitter-sensitive neurons are activated by bitter substances (from Hiroi et al., 2004). (A) Sample recordings from I-type sensilla stimulated with strychnine at increasing concentrations (0.1 mM, 1 mM, 10 mM), showing that one cell is activated by strychnine. (B) Dose response curves showing the response of this cell to increasing concentrations of strychnine (empty circle), berberine (empty diamond), quinine (black square) and caffeine (empty circle and dotted line).

Figure 3

Bitter-sensitive cells respond also to inhibitory sexual pheromones. (A) Diagram showing the two electrodes configuration used to record extracellular activities from taste sensilla of Drosophila. In all cases, a glass capillary containing the stimulus is used to cap the tip of a gustatory sensillum. If the stimulus is water-soluble, the stimulus electrode can contain an electrolyte and can be used to record electrical signals from the neurons within the sensilla. If the stimulus is lipophilic, the stimulus electrode which contains paraffin oil with the ligand, is no longer conductive and we use another electrode, for example a fine tapered tungsten rod, inserted at the base of a sensillum. (B) Sample recordings obtained from an I-type sensillum on the proboscis of Drosophila using a tungsten recording electrode, and stimulating either with sucrose (suc), caffeine (caff), 7-tricosene (7-T) or a mixture of 7-tricosene and caffeine (reproduced from Lacaille et al., 2007).

Figure 4

Inhibition of the response to sugars by bitter chemicals (Sellier, 2010). (A) Adding increasing concentrations of quinine to 35 mM fructose inhibits the firing activity recorded from L-type sensilla of the proboscis of Drosophila. (B) At the same molar concentration (1 mM), bitter chemicals differ in their power to inhibit the response to 0.1 M sucrose. Each point represents the average of 5–10 responses. Bars display SEM.

Figure 5

Fundamental differences between olfaction and contact chemoreception in insects. Although taste and olfactory sensilla have similar cellular compositions, the wiring of the neurons to the central nervous system and the number of different receptors expressed in each neuron is very different. These differences certainly impact the discriminative power and the speed at which information is processed.