Functional dissociation in sweet taste receptor neurons between and within taste organs of Drosophila

Thoma, Vladimiros; Knapek, Stephan; Arai, Shigeo; Hartl, Marion; Kohsaka, Hiroshi; Sirigrivatanawong, Pudith; Abe, Ayako; Hashimoto, Koichi; Tanimoto, Hiromu

doi:10.1038/ncomms10678

Cited by 60 publications

(87 citation statements)

References 48 publications

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“…In previous studies, Tsh-Gal80 and Otd-nls:FLP were successfully used to specifically suppress Gr gene expression in either the labellum or legs, respectively [37, 38]. However, both Tsh-Gal80 and Otd-nls:FLP appear to be expressed in bitter and sweet GRNs, respectively, leaving expression unaffected in a subset of IR76b-GAL4 expressing GRNs (Figure S5).…”

Section: Resultsmentioning

confidence: 95%

Ionotropic Receptors Mediate Drosophila Oviposition Preference through Sour Gustatory Receptor Neurons

2017

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Summary Carboxylic acids are present in many foods, being especially abundant in fruits. Yet, relatively little is known about how acids are detected by the gustatory systems, whether they have a potential role in nutrition or provide other health benefits. Here, we identify sour gustatory receptor neurons (GRNs) in tarsal taste sensilla of Drosophila melanogaster. We find that most tarsal sensilla harbor a sour GRN that is specifically activated by carboxylic and mineral acids, but does not respond to sweet and bitter-tasting chemicals or salt. One pair of taste sensilla features two GRNs that respond only to a subset of carboxylic acids and high concentrations of salt. All sour GRNs prominently express two Ionotropic Receptor (IR) genes, IR76b and IR25a, and we show that both these genes are necessary for the detection of acids. Furthermore, we establish that IR25a and IR76b are essential in sour GRNs of females for oviposition preference on acid containing food. Our investigations reveal that acids activate a unique set of taste cells largely dedicated to sour taste, and they indicate that both pH/proton concentration and the structure of carboxylic acids contribute to sour GRN activation. Together, our studies provide new insights into the cellular and molecular basis of sour taste.

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Section: Resultsmentioning

confidence: 95%

Ionotropic Receptors Mediate Drosophila Oviposition Preference through Sour Gustatory Receptor Neurons

2017

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“…Expression of the trans -Tango ligand in Gr64f+ GRNs revealed extensive postsynaptic signal in the CNS (Figure 5A and 5B, Movie S2). Gr64f+ GRNs are present in each leg and either terminate in the thoracic ganglia or project directly to the posterior SEZ with collaterals in the thoracic ganglia (Figure 5A) (Kwon et al ., 2014; Thoma et al ., 2016). Gr64f+ GRNs also innervate the abdominal ganglion (Movie S2).…”

Section: Resultsmentioning

confidence: 99%

Transsynaptic Mapping of Second-Order Taste Neurons in Flies by trans-Tango

Talay

Richman

Snell

et al. 2017

Neuron

278

360

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SUMMARY Mapping neural circuits across defined synapses is essential for understanding brain function. Here we describe trans-Tango, a technique for anterograde transsynaptic circuit tracing and manipulation. At the core of trans-Tango is a synthetic signaling pathway that is introduced into all neurons in the animal. This pathway converts receptor activation at the cell-surface into reporter expression through site-specific proteolysis. Specific labeling is achieved by presenting a tethered ligand at the synapses of genetically defined neurons, thereby activating the pathway in their postsynaptic partners and providing genetic access to these neurons. We first validated trans-Tango in the Drosophila olfactory system and then implemented it in the gustatory system, where projections beyond the first-order receptor neurons are not fully characterized. We identified putative second-order neurons within the sweet circuit that include projection neurons targeting known neuromodulation centers in the brain. These experiments establish trans-Tango as a flexible platform for transsynaptic circuit analysis.

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“…The wide expression pattern, presence of multiple receptors in the same neurons, and different combinations of receptors in different neurons indicate that gustatory-receptor-expressing neurons in various locations may respond quite differently to different sugars (Thoma et al, 2016; Miyamoto and Amrein, 2014). We focused particularly on Gr43a-expressing neurons for their specific involvement in L-arabinose memory, and previous studies suggested they act as nutrient sensors (Miyamoto et al, 2012).…”

Section: Resultsmentioning

confidence: 99%

Immediate perception of a reward is distinct from the reward’s long-term salience

McGinnis

Jiang

Agha

et al. 2016

eLife

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Reward perception guides all aspects of animal behavior. However, the relationship between the perceived value of a reward, the latent value of a reward, and the behavioral response remains unclear. Here we report that, given a choice between two sweet and chemically similar sugars—L- and D-arabinose—Drosophila melanogaster prefers D- over L- arabinose, but forms long-term memories of L-arabinose more reliably. Behavioral assays indicate that L-arabinose-generated memories require sugar receptor Gr43a, and calcium imaging and electrophysiological recordings indicate that L- and D-arabinose differentially activate Gr43a-expressing neurons. We posit that the immediate valence of a reward is not always predictive of the long-term reinforcement value of that reward, and that a subset of sugar-sensing neurons may generate distinct representations of similar sugars, allowing for rapid assessment of the salient features of various sugar rewards and generation of reward-specific behaviors. However, how sensory neurons communicate information about L-arabinose quality and concentration—features relevant for long-term memory—remains unknown.DOI: http://dx.doi.org/10.7554/eLife.22283.001

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Functional dissociation in sweet taste receptor neurons between and within taste organs of Drosophila

Cited by 60 publications

References 48 publications

Ionotropic Receptors Mediate Drosophila Oviposition Preference through Sour Gustatory Receptor Neurons

Ionotropic Receptors Mediate Drosophila Oviposition Preference through Sour Gustatory Receptor Neurons

Transsynaptic Mapping of Second-Order Taste Neurons in Flies by trans-Tango

Immediate perception of a reward is distinct from the reward’s long-term salience

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