Multimodal stimulus coding by a gustatory sensory neuron in Drosophila larvae

Giesen, Lena van; Hernandez-Nuñez, Luis; Delasoie-Baranek, Sophie; Colombo, Martino; Renaud, Philippe; Bruggmann, Rémy; Benton, Richard; Samuel, Aravinthan D. T.; Sprecher, Simon G.

doi:10.1038/ncomms10687

Cited by 36 publications

(86 citation statements)

References 47 publications

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“…We recently measured neuronal activity in a single GRN stimulated with multiple tastants from all different taste categories, showing that larvae possess multimodal GRNs 19 , in contrast to previously described unimodal taste neurons in the adult fly or in the mammalian system 20 . However, the described protocol can be used to characterize individual sensory neurons in different types of investigations.…”

Section: Applicationsmentioning

confidence: 76%

“…2c), and a gustatory neuron (C7) from a larva (Fig. 2d) 19 . Multicellular recordings can be obtained; depending on the desired information, they are acquired as stacks (Fig.…”

Section: Anticipated Resultsmentioning

confidence: 99%

“…In our previous publications 19,21 , we used the system to perform recordings from larval taste neurons. Here we show that the chip can also be used to record and measure neuronal activity directly in the cell bodies of GRNs of the adult proboscis or leg (Fig.…”

Section: Applicationsmentioning

confidence: 99%

“…CRITICAL The controller of the micropumps has a USB port and can be directly operated by a computer. In our recent publication 19 , we switched pumps manually, but an automatic control might enhance accuracy of measurements. CRITICAL STEP This first layer of SU8 improves adhesion by reducing internal stress from the second, thicker SU8 layer, which can lead to cracking and detaching of the material from the wafer.…”

Section: Reagentsmentioning

confidence: 99%

“…We used this custom-made microfluidic device to deliver precise and temporally restricted tastant stimulation in the first published physiological characterization of individual larval gustatory receptor neurons (GRNs) expressing the calcium sensor GCaMP5 (ref. 19). …”

Section: Introductionmentioning

confidence: 99%

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A microfluidics-based method for measuring neuronal activity in Drosophila chemosensory neurons

et al. 2016

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Animals possess highly specialized sensory neurons that are capable of perceiving information about a continuously changing environment. Measuring neuronal activity in these cells is an important step toward understanding the basic coding principles, as well as the spatial and temporal dynamics, of sensory systems. The fruit fly Drosophila melanogaster is widely used as a genetic model organism to uncover basic mechanisms of taste coding and odor perception [1][2][3][4][5][6][7] . Recent insights into the molecular and functional mechanisms of sensory perception in Drosophila have been achieved by the use of single-sensillum recordings of adult taste or olfactory sensilla 1,4,[8][9][10][11][12][13] . This method enables sensitive measurements of action potential patterns and shows whether responses are excitatory or inhibitory, but drawing final conclusions about the individual firing neuron is difficult, as each sensillum contains two to four neurons 14 . In the larva, multicellular electrophysiological measurements of the taste system have been performed, but this method is technically challenging and it is not clear how many taste neurons are housed in which sensillum 15 .Microfluidic devices have been used previously to image command interneurons (AVA) and sensory neurons (ASH) in the nematode Caenorhabditis elegans and for studies of axotomy in peripheral sensory neurons of Drosophila larvae [16][17][18] . To implement a similar strategy for Drosophila larval chemosensation, we developed a simple and widely applicable microfluidic chip. We used this custom-made microfluidic device to deliver precise and temporally restricted tastant stimulation in the first published physiological characterization of individual larval gustatory receptor neurons (GRNs) expressing the calcium sensor GCaMP5 (ref. 19). Development of the protocolThe design of the chip is simple. It contains a single channel that is connected to a chamber in which the sample can be mounted to bring it into contact with fluids in the channel. The chamber was originally designed to exactly fit the head of a third-instar Drosophila larva; however, it is also suitable for the proboscis or the leg of an adult fly. The channel for delivering stimulants is relatively broad, designed at a width of 1 mm to reduce flow pressure on the sample. We use a single-channel system in which changes of liquids are performed by the tubing system outside the chip, allowing a relatively slow flow rate inside the chip. Here we provide information required for the design and production of this microfluidic device ( Fig. 1; Supplementary Data), as well as a detailed protocol for live imaging to acquire GCaMP-based calcium imaging (Figs. 2 and 3). By introducing the larval head, or the adult proboscis or leg, into the chamber, neuronal activity can be recorded while chemosensory neurons are in contact with the solution pumped through the channel (Figs. 2 and 3).Overview of the procedure An overview of the workflow involved in implementing the procedure is provided in Figu...

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Section: Applicationsmentioning

confidence: 76%

“…2c), and a gustatory neuron (C7) from a larva (Fig. 2d) 19 . Multicellular recordings can be obtained; depending on the desired information, they are acquired as stacks (Fig.…”

Section: Anticipated Resultsmentioning

confidence: 99%

Section: Applicationsmentioning

confidence: 99%

Section: Reagentsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A microfluidics-based method for measuring neuronal activity in Drosophila chemosensory neurons

et al. 2016

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A map of sensilla and neurons in the taste system of drosophila larvae

Rist

Thum

2017

J of Comparative Neurology

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In Drosophila melanogaster larvae, the prime site of external taste reception is the terminal organ (TO). Though investigation on the TO's implications in taste perception has been expanding rapidly, the sensilla of the TO have been essentially unexplored. In this study, we performed a systematic anatomical and molecular analysis of the TO. We precisely define morphological types of TO sensilla taking advantage of volume electron microscopy and 3D image analysis. We corroborate the presence of five external types of sensilla: papilla, pit, spot, knob, and modified papilla. Detailed 3D analysis of their structural organization allowed a finer discrimination into subtypes. We classify three subtypes of papilla and pit sensilla, respectively, and two subtypes of knob sensilla. Further, we determine the repertoire of receptor genes for each sensillum by analyzing GAL4 driver lines of Ir, Gr, Ppk, and Trp receptor genes. We construct a map of the TO, in which the receptor genes are mapped to neurons of individual sensilla. While modified papillum and spot sensilla are not labeled by any GAL4 driver, neurons of the pit, papilla, and knob type are labeled by partially overlapping but different subsets of GAL4 driver lines of the Ir, Gr, and Ppk gene family. The results suggest that pit, papilla and knob sensilla act in contact chemosensation. However, they likely do these employing different stimulus transduction mechanisms to sense the diverse chemicals of their environment.

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A Family of non-GPCR Chemosensors Defines an Alternative Logic for Mammalian Olfaction

Greer

Bear

Lassance

et al. 2016

Cell

133

134

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Summary Odor perception in mammals is mediated by parallel sensory pathways that convey distinct information about the olfactory world. Multiple olfactory subsystems express characteristic seven-transmembrane G-protein coupled receptors (GPCRs) in a one-receptor-per-neuron pattern that facilitates odor discrimination. Sensory neurons of the “necklace” subsystem are nestled within the recesses of the olfactory epithelium and detect diverse odorants; however, they do not express known GPCR odor receptors. Here we report that members of the four-pass transmembrane MS4A protein family are chemosensors expressed within necklace sensory neurons. These receptors localize to sensory endings and confer responses to ethologically-relevant ligands including pheromones and fatty acids in vitro and in vivo. Individual necklace neurons co-express many MS4A proteins and are activated by multiple MS4A ligands; this pooling of information suggests that the necklace is organized more like subsystems for taste than for smell. The MS4As therefore define a distinct mechanism and functional logic for mammalian olfaction.

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Multimodal stimulus coding by a gustatory sensory neuron in Drosophila larvae

Cited by 36 publications

References 47 publications

A microfluidics-based method for measuring neuronal activity in Drosophila chemosensory neurons

A microfluidics-based method for measuring neuronal activity in Drosophila chemosensory neurons

A map of sensilla and neurons in the taste system of drosophila larvae

A Family of non-GPCR Chemosensors Defines an Alternative Logic for Mammalian Olfaction

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