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. 2006 Jan 24;103(4):1094-9.
doi: 10.1073/pnas.0502376103. Epub 2006 Jan 13.

Cellular identification of water gustatory receptor neurons and their central projection pattern in Drosophila

Tsuyoshi Inoshita  1 , Teiichi Tanimura
Affiliations

Cellular identification of water gustatory receptor neurons and their central projection pattern in Drosophila

Tsuyoshi Inoshita et al. Proc Natl Acad Sci U S A. .

Abstract

Water perception is important for insects, because they are particularly vulnerable to water loss because their body size is small. In Drosophila, gustatory receptor neurons are located at the base of the taste sensilla on the labellum, tarsi, and wing margins. One of the gustatory receptor neurons in typical sensilla is known to respond to water. To reveal the neural mechanisms of water perception in Drosophila, it is necessary to identify water receptor neurons and their projection patterns. We used a Gal4 enhancer trap strain in which GAL4 is expressed in a single gustatory receptor neuron in each sensillum on the labellum. We investigated the function of these neurons by expressing the upstream activating sequence transgenes, shibire(ts1), tetanus toxin light chain, or diphtheria toxin A chain. Results from the proboscis extension reflex test and electrophysiological recordings indicated that the GAL4-expressing neurons respond to water. We show here that the water receptor neurons project to a specific region in the subesophageal ganglion, thus revealing the water taste sensory map in Drosophila.

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Figures

Fig. 1.
Fig. 1.
GAL4 is expressed in a single gustatory receptor neuron. (A) A fluorescent image of NP1017 carrying the UAS-GFP transgene. The GFP expression pattern on the labellum is shown. (B) Diagram showing distribution of taste sensilla on labellum. Location of l- and s-type sensilla associated with GFP-expressing neurons on the labellum is shown. No GFP-expressing neurons were seen in the i-type sensilla. (C) Immunostaining of GFP-expressing cells on the labellum. Only one neuron was stained with antibody against GFP in each sensillum. (D–F) There are GFP-expressing neurons at the base of l-type (D) and s-type (E) sensilla, but no GFP-expressing neuron was observed in i-type (F) sensilla. (Scale bars: 50 μm in A and 10 μm in C–F.)
Fig. 2.
Fig. 2.
Functional identification of the GAL4-expressing neuron. (A) Sugar responses (on the left) and salt aversion (on the right) in NP1017 carrying UAS-shibirets1 flies. Open bars represent the percentage of responding flies at a permissive temperature (22°C), and solid bars represent the result at a restrictive temperature (30°C). (B) The percentage of water-responding flies was decreased in NP1017 carrying UAS-shibirets1 flies. Water responses of parental control strains were not affected. (C) Water and sugar responses of taste sensilla on the labellum in NP1017 carrying UAS-TNT flies. Data are based on two to six experiments using 10–16 flies in one series of tests. Error bars indicate SE. *, P < 0.01.
Fig. 3.
Fig. 3.
Electrical and cytological identification of a water receptor neuron by ablation with UAS-DTI. (A) No spikes to water were recorded. (B) In a sensillum of other flies, spikes were recorded only at the initial phase after stimulation. (C) Normal water responses were recorded from most of taste sensilla. Arrowheads show the start of stimulation in A–C. (D and E) There are five neurons (arrows in E) in a taste sensillum, and there are four neurons (arrowheads in D) in an l4 sensillum from which no water responses were recorded, as shown in A. (Scale bar: 10 μm.)
Fig. 4.
Fig. 4.
Central projection of the water receptor neurons. (A and E) Diagrams of the frontal (A) and sagittal (E) views of the head and brain. Axons of gustatory receptor neurons in taste sensilla on the labellum project to the SOG. (B) A frontal view of the SOG of an adult brain in NP1017 carrying UAS-GFP flies. Two projection patterns were observed in the SOG (arrows and arrowheads). (C and D) One group of axons is winding and has less arborization (arrowheads in B and D), and another had narrow arborizations in the synaptic region (arrows in B and C). (F) A sagittal view of the projection pattern of water receptor neurons in the SOG. Less-arborized fibers (arrowhead) projected to the anterior region of the SOG, and narrow arborized axons (arrow) projected to the central region of the SOG. Left is anterior. (Scale bars: 50 μm.)
Fig. 5.
Fig. 5.
Projection pattern of a single GAL4-expressing neuron. Images of projection pattern (shown in C–F) were taken from one side of SOG (a box of broken lines in A). (B and C) There is one GFP-expressing neuron in one side of the labellum. This GFP-expressing neuron is connected with an s-type sensillum (arrow in B), and the axon of this neuron projects to the central region and has arborizations in the synaptic region (C). (D) A GFP-expressing neuron connecting with interpseudotracheal papillae projects to the lateral–anterior region in the SOG. (E) Axons of two GAL4-expressing neurons, one connected with a taste sensillum and the other connected with interpseudotracheal papillae, project to different regions in the SOG. (F) Axons of GAL4-expressing neurons in one s-type sensillum and two l-type sensilla project to same region in the SOG. (Scale bars: 50 μm in B and 20 μm in C–F.)
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