Caffeine Taste Signaling in Drosophila Larvae

Apostolopoulou, Anthi A.; Köhn, Saskia; Stehle, Bernhard; Lutz, Michael W.; Wüst, Alexander; Mazija, Lorena; Rist, Anna; Galizia, C. Giovanni; Lüdke, Alja; Thum, Andreas S.

doi:10.3389/fncel.2016.00193

Cited by 37 publications

(38 citation statements)

References 92 publications

(180 reference statements)

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“…In a previous study, we found that a specific pair of neurons in the dorsal pharyngeal sensilla called DP1 is necessary and sufficient for caffeine-mediated decrease in ingestion (Choi et al, 2016). An independent study found that the same neurons mediate caffeine avoidance (Apostolopoulou et al, 2016). The DP1 neuron expresses the Gr33a-, Gr39b-, and Gr22d-GAL4 drivers (Choi et al, 2016).…”

Section: Dp1 Neurons Are Necessary and Sufficient For Caffeine-inducementioning

confidence: 97%

Cellular Basis of Bitter-Driven Aversive Behaviors inDrosophilaLarva

Choi

et al. 2020

eNeuro

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Feeding, a critical behavior for survival, consists of a complex series of behavioral steps. In Drosophila larvae, the initial steps of feeding are food choice, during which the quality of a potential food source is judged, and ingestion, during which the selected food source is ingested into the digestive tract. It remains unclear whether these steps employ different mechanisms of neural perception. Here, we provide insight into the two initial steps of feeding in Drosophila larva. We find that substrate choice and ingestion are determined by independent circuits at the cellular level. First, we took 22 candidate bitter compounds and examined their influence on choice preference and ingestion behavior. Interestingly, certain bitter tastants caused different responses in choice and ingestion, suggesting distinct mechanisms of perception. We further provide evidence that certain gustatory receptor neurons (GRNs) in the external terminal organ are involved in determining choice preference, and a pair of larval pharyngeal GRNs is involved in mediating both avoidance and suppression of ingestion. Our results show that feeding behavior is coordinated by a multistep regulatory process employing relatively independent neural elements. These findings are consistent with a model in which distinct sensory pathways act as modulatory circuits controlling distinct subprograms during feeding. Significance Statement Here we provide molecular and cellular evidence that feeding can indeed be dissected into two distinct steps, namely the determination of preference and initiation of ingestion. We find that bitter tastants have individual characteristics when negatively affecting feeding, with most chemicals negatively affecting both preference and ingestion, and certain chemicals negatively affecting only preference. These characteristics are due to different sensory neurons being responsible for detecting different bitter compounds. The different sensory neurons appear to act in relatively independent neural circuits to differentially affect the multiple steps that comprise feeding.

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Section: Dp1 Neurons Are Necessary and Sufficient For Caffeine-inducementioning

confidence: 97%

Cellular Basis of Bitter-Driven Aversive Behaviors inDrosophilaLarva

Choi

et al. 2020

eNeuro

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“…Defined ORN activation (standardized CS) can then be paired with activation of individual sensory neurons expressing gustatory receptors, ionotropic receptors, transient receptor potential cation channels, and/or pickpocket ion channel genes ( Clyne, 2000 ; Dunipace et al, 2001 ; Scott et al, 2001 ; Liu et al, 2003 ; Montell, 2005 ; Benton et al, 2009 ). In this manner, one could comprehensively identify the sensory neurons that encode for appetitive and aversive reinforcement in Drosophila larvae (e.g., Gr93a for aversive reinforcement and IR60c potentially for appetitive reinforcement) ( Apostolopoulou et al, 2016 ; Croset et al, 2016 ).…”

Section: Discussionmentioning

confidence: 99%

Maggot Instructor: Semi-Automated Analysis of Learning and Memory in Drosophila Larvae

2018

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For several decades, Drosophila has been widely used as a suitable model organism to study the fundamental processes of associative olfactory learning and memory. More recently, this condition also became true for the Drosophila larva, which has become a focus for learning and memory studies based on a number of technical advances in the field of anatomical, molecular, and neuronal analyses. The ongoing efforts should be mentioned to reconstruct the complete connectome of the larval brain featuring a total of about 10,000 neurons and the development of neurogenic tools that allow individual manipulation of each neuron. By contrast, standardized behavioral assays that are commonly used to analyze learning and memory in Drosophila larvae exhibit no such technical development. Most commonly, a simple assay with Petri dishes and odor containers is used; in this method, the animals must be manually transferred in several steps. The behavioral approach is therefore labor-intensive and limits the capacity to conduct large-scale genetic screenings in small laboratories. To circumvent these limitations, we introduce a training device called the Maggot Instructor. This device allows automatic training up to 10 groups of larvae in parallel. To achieve such goal, we used fully automated, computer-controlled optogenetic activation of single olfactory neurons in combination with the application of electric shocks. We showed that Drosophila larvae trained with the Maggot Instructor establish an odor-specific memory, which is independent of handling and non-associative effects. The Maggot Instructor will allow to investigate the large collections of genetically modified larvae in a short period and with minimal human resources. Therefore, the Maggot Instructor should be able to help extensive behavioral experiments in Drosophila larvae to keep up with the current technical advancements. In the longer term, this condition will lead to a better understanding of how learning and memory are organized at the cellular, synaptic, and molecular levels in Drosophila larvae.

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“…Therefore, the actual stimuli can only be confirmed by physiological and behavioral tests. Indeed, few studies have defined a link between gustatory stimuli and particular neurons of the TO (Apostolopoulou et al, ; Apostolopoulou et al, ; Apostolopoulou et al, ; van Giesen et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…The terminal organ (TO) lies close and ventrally to the dorsal organ (DO). Below, the mouth hooks are visible above the mouth opening (modified from Apostolopoulou et al, ). Cuticle cirri (cirri) cover the frontal part of the cephalic lobes.…”

Section: Introductionmentioning

confidence: 99%

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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Caffeine Taste Signaling in Drosophila Larvae

Cited by 37 publications

References 92 publications

Cellular Basis of Bitter-Driven Aversive Behaviors inDrosophilaLarva

Cellular Basis of Bitter-Driven Aversive Behaviors inDrosophilaLarva

Maggot Instructor: Semi-Automated Analysis of Learning and Memory in Drosophila Larvae

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

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