Peripheral coding of bitter taste in <i>Drosophila</i>

Meunier, Nicolas; Marion‐Poll, Frédéric; Rospars, Jean-Pierre; Tanimura, Teiichi

doi:10.1002/neu.10235

Cited by 197 publications

(248 citation statements)

References 39 publications

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“…Two-way choice assays were performed essentially as described (50). Briefly, 3-to 6-day-old flies (50 ± 10 flies per experiment) were starved on 1% agarose for ∼18 h and placed into 72-well microtiter dishes with 1% agarose.…”

Section: Methodsmentioning

confidence: 99%

Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons

Kim

Lee

Akitake

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

159

154

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Mammalian sweet, bitter, and umami taste is mediated by a single transduction pathway that includes a phospholipase C (PLC)β and one cation channel, TRPM5. However, in insects such as the fruit fly, Drosophila melanogaster, it is unclear whether different tastants, such as bitter compounds, are sensed in gustatory receptor neurons (GRNs) through one or multiple ion channels, as the cation channels required in insect GRNs are unknown. Here, we set out to explore additional sensory roles for the Drosophila TRPA1 channel, which was known to function in thermosensation. We found that TRPA1 was expressed in GRNs that respond to aversive compounds. Elimination of TRPA1 had no impact on the responses to nearly all bitter compounds tested, including caffeine, quinine, and strychnine. Rather, we found that TRPA1 was required in a subset of avoidance GRNs for the behavioral and electrophysiological responses to aristolochic acid. TRPA1 did not appear to be activated or inhibited directly by aristolochic acid. We found that elimination of the same PLC that leads to activation of TRPA1 in thermosensory neurons was also required in the TRPA1-expressing GRNs for avoiding aristolochic acid. Given that mammalian TRPA1 is required for responding to noxious chemicals, many of which cause pain and injury, our analysis underscores the evolutionarily conserved role for TRPA1 channels in chemical avoidance.

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Section: Methodsmentioning

confidence: 99%

Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons

Kim

Lee

Akitake

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

159

154

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“…L-and S-type sensillum contain four GRNs, and the I type contains two GRNs. Based on electrophysiological investigations, each GRN is thought to respond exclusively to either sugar, water, low salt concentration, or high salt concentration and bitter compounds [16][17][18][19][20]. Taste bristle have a terminal pore at the tip, allowing taste stimuli access to the dendrite of the GRN, which extends into the bristle shaft [21].…”

Section: The Drosophila Taste Systemmentioning

confidence: 99%

Taste and pheromone perception in the fruit fly Drosophila melanogaster

Ebbs

Amrein

2007

Pflugers Arch - Eur J Physiol

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Taste is an essential sense for detection of nutrient-rich food and avoidance of toxic substances. The Drosophila melanogaster gustatory system provides an excellent model to study taste perception and taste-elicited behaviors. "The fly" is unique in the animal kingdom with regard to available experimental tools, which include a wide repertoire of molecular-genetic analyses (i.e., efficient production of transgenics and gene knockouts), elegant behavioral assays, and the possibility to conduct electrophysiological investigations. In addition, fruit flies, like humans, recognize sugars as a food source, but avoid bitter tasting substances that are often toxic to insects and mammals alike. This paper will present recent research progress in the field of taste and contact pheromone perception in the fruit fly. First, we shall describe the anatomical properties of the Drosophila gustatory system and survey the family of taste receptors to provide an appropriate background. We shall then review taste and pheromone perception mainly from a molecular genetic perspective that includes behavioral, electrophysiological and imaging analyses of wild type flies and flies with genetically manipulated taste cells. Finally, we shall provide an outlook of taste research in this elegant model system for the next few years.Keywords Drosophila . Gustatory receptor neurons . GTP-binding protein-coupled receptors Like most animals, Drosophila monitor their chemical world with two distinct senses: the olfactory system, which is used for the detection of volatile chemicals, and the gustatory (taste) system, which enables the fly to detect soluble compounds. The olfactory sensory system (or the fly nose) is comprised of two pairwise head appendages, the third segments of the antennae, and the maxillary palps (Fig. 1). These appendages are covered with hundreds of sensory hairs, each of which contains two to four olfactory sensory neurons (OSNs) [1]. In contrast, the gustatory system is widely distributed over the animal's body. The main taste organ, the proboscis or labial palps (i.e., the fly tongue), is located on the distal end of the labellum (also a head appendage), but flies, like many other insects, have taste sensilla on legs and wings and, in females, on the genitalia [1,2].The roles of the olfactory and taste systems are clearly separated with regard to the physical state of chemicals they detect (volatile vs solubilized). However, the two systems often cooperate to fulfill specific functions in related processes and behaviors, the most obvious of them being the location and identification of food. For example, chemical cues such as the specific odor of a flower and the sugar compounds present in its nectar are by nature associated with one another. Thus, the odor cue provides a primary sensory input for an insect such as a honeybee to locate a food source (nectar), whose particular chemical composition is subsequently verified by the taste system. Similarly, the typical odor of yeast, which produces high amounts of t...

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“…First, compared with many insects [e.g., Orthopterans and Dipterans (Chapman et al, 1991;Meunier et al, 2003)], caterpillars have a paucity of bittersensitive taste cells, ϳ16 in total (Fig. 1).…”

Section: Functional Implicationsmentioning

confidence: 99%

Temporal Coding Mediates Discrimination of “Bitter” Taste Stimuli by an Insect

Glendinning

Davis²,

Rai³

2006

J. Neurosci.

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The mechanisms that mediate discriminative taste processing in insects are poorly understood. We asked whether temporal patterns of discharge from the peripheral taste system of an insect (Manduca sexta caterpillars; Sphingidae) contribute to the discrimination of three "bitter" taste stimuli: salicin, caffeine, and aristolochic acid. The gustatory response to these stimuli is mediated exclusively by three pairs of bitter-sensitive taste cell, which are located in the medial, lateral, and epipharyngeal sensilla. We tested for discrimination by habituating the caterpillars to salicin and then determining whether the habituation generalized to caffeine or aristolochic acid. We ran habituation-generalization tests in caterpillars with their full complement of taste sensilla (i.e., intact) and in caterpillars with ablated lateral sensilla (i.e., lat-ablated). The latter perturbation enabled us to examine discrimination in caterpillars with a modified peripheral taste profile. We found that the intact and lat-ablated caterpillars both generalized the salicin-habituation to caffeine but not aristolochic acid. Next, we determined whether this pattern of stimulus-generalization could be explained by salicin and aristolochic acid generating distinct ensemble, rate, temporal, or spatiotemporal codes. To this end, we recorded excitatory responses from the bitter-sensitive taste cells and then used these responses to formulate predictions about whether the salicin-habituation should generalize to caffeine or aristolochic acid, separately for each coding framework. We found that the pattern of stimulus generalization in both intact and latablated caterpillars could only be predicted by temporal coding. We conclude that temporal codes from the periphery can mediate discriminative taste processing.

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Peripheral coding of bitter taste in Drosophila

Cited by 197 publications

References 39 publications

Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons

Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons

Taste and pheromone perception in the fruit fly Drosophila melanogaster

Temporal Coding Mediates Discrimination of “Bitter” Taste Stimuli by an Insect

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