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Real-Time Measurement of Stimulated Dopamine Release in Compartments of the Adult Drosophila melanogaster Mushroom Body

Cite this: Anal. Chem. 2020, 92, 21, 14398–14407
Publication Date (Web):October 13, 2020
https://doi.org/10.1021/acs.analchem.0c02305
Copyright © 2020 American Chemical Society

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    Abstract

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    Drosophila melanogaster, a fruit fly, is an exquisite model organism to understand neurotransmission. Dopaminergic signaling in the Drosophila mushroom body (MB) is involved in olfactory learning and memory, with different compartments controlling aversive learning (heel) vs. appetitive learning (medial tip). Here, the goal was to develop techniques to measure endogenous dopamine in compartments of the MB for the first time. We compared three stimulation methods: acetylcholine (natural stimulus), P2X2 (chemogenetics), and CsChrimson (optogenetics). Evoked dopamine release was measured with fast-scan cyclic voltammetry in isolated adult Drosophila brains. Acetylcholine stimulated the largest dopamine release (0.40 μM) followed by P2X2 (0.14 μM) and CsChrimson (0.07 μM). With the larger acetylcholine and P2X2 stimulations, there were no regional or sex differences in dopamine release. However, with CsChrimson, dopamine release was significantly higher in the heel than the medial tip, and females had more dopamine than males. Michaelis–Menten modeling of the single-light pulse revealed no significant regional differences in Km, but the heel had a significantly lower Vmax (0.12 μM/s vs. 0.19 μM/s) and higher dopamine release (0.05 μM vs. 0.03 μM). Optogenetic experiments are challenging because CsChrimson is also sensitive to blue light used to activate green fluorescent protein, and thus, light exposure during brain dissection must be minimized. These experiments expand the toolkit for measuring endogenous dopamine release in Drosophila, introducing chemogenetic and optogenetic experiments for the first time. With a variety of stimulations, different experiments will help improve our understanding of neurochemical signaling in Drosophila.

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.analchem.0c02305.

    • Supplemental methods on chemical information and methods for Drosophila line preparations, electrochemical measurements, and confocal imaging and supplemental figures on control experiment puffing ATP without P2X2 expressed or shining light without CsChrimson, characterization of dopamine clearance in P2X2 and control flies, current traces of CsChrimson-evoked dopamine release at various CsChrimson stimulation parameters, raw trace of Michaelis–Menten modeling of evoked dopamine release, cyclic voltammograms of acetylcholine-stimulated dopamine release at dopamine, octopamine, and serotonin waveforms (PDF)

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    Cited By

    This article is cited by 10 publications.

    1. Eduard Dumitrescu, Jeffrey M. Copeland, B. Jill Venton. Parkin Knockdown Modulates Dopamine Release in the Central Complex, but Not the Mushroom Body Heel, of Aging Drosophila. ACS Chemical Neuroscience 2023, 14 (2) , 198-208. https://doi.org/10.1021/acschemneuro.2c00277
    2. Mahdieh Darroudi, Kevin A. White, Matthew A. Crocker, Brian N. Kim. Dopamine Measurement Using Engineered CNT–CQD–Polymer Coatings on Pt Microelectrodes. Sensors 2024, 24 (6) , 1893. https://doi.org/10.3390/s24061893
    3. Jiatao Chen, Xiuting Ding, Dongdong Zhang. Challenges and strategies faced in the electrochemical biosensing analysis of neurochemicals in vivo: A review. Talanta 2024, 266 , 124933. https://doi.org/10.1016/j.talanta.2023.124933
    4. Aleksandra Plačkić, Tilmann J. Neubert, Kishan Patel, Michel Kuhl, Kenji Watanabe, Takashi Taniguchi, Amaia Zurutuza, Roman Sordan, Kannan Balasubramanian. Electrochemistry at the Edge of a van der Waals Heterostructure. Small 2023, 499 https://doi.org/10.1002/smll.202306361
    5. Celeste R. Rousseau, Hope Kumakli, Ryan J. White. Perspective—Assessing Electrochemical, Aptamer-Based Sensors for Dynamic Monitoring of Cellular Signaling. ECS Sensors Plus 2023, 2 (4) , 042401. https://doi.org/10.1149/2754-2726/ad15a1
    6. Cinzia Volonté, Francesca Alberti, Giuseppe Vitale, Francesco Liguori. Delineating Purinergic Signaling in Drosophila. International Journal of Molecular Sciences 2022, 23 (23) , 15196. https://doi.org/10.3390/ijms232315196
    7. Mimi Shin, B. Jill Venton. Fast‐Scan Cyclic Voltammetry (FSCV) Reveals Behaviorally Evoked Dopamine Release by Sugar Feeding in the Adult Drosophila Mushroom Body. Angewandte Chemie 2022, 134 (44) https://doi.org/10.1002/ange.202207399
    8. Mimi Shin, B. Jill Venton. Fast‐Scan Cyclic Voltammetry (FSCV) Reveals Behaviorally Evoked Dopamine Release by Sugar Feeding in the Adult Drosophila Mushroom Body. Angewandte Chemie International Edition 2022, 61 (44) https://doi.org/10.1002/anie.202207399
    9. Kelly E. Dunham, B. Jill Venton. SSRI antidepressants differentially modulate serotonin reuptake and release in Drosophila. Journal of Neurochemistry 2022, 162 (5) , 404-416. https://doi.org/10.1111/jnc.15658
    10. Chuanrui Chen, Xuemei Sun, Huisheng Peng. The Rise of Soft Neural Electronics. Giant 2021, 8 , 100075. https://doi.org/10.1016/j.giant.2021.100075

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