Modulation of Flight and Feeding Behaviours Requires Presynaptic IPRs in Dopaminergic Neurons

Overview

Journal Elife

Specialty Biology

Date 2020 Nov 6

PMID 33155978

Citations 10

Authors

Anamika Sharma

Gaiti Hasan

Affiliations

Soon will be listed here.

Abstract

Innate behaviours, although robust and hard wired, rely on modulation of neuronal circuits, for eliciting an appropriate response according to internal states and external cues. flight is one such innate behaviour that is modulated by intracellular calcium release through inositol 1,4,5-trisphosphate receptors (IPRs). Cellular mechanism(s) by which IPRs modulate neuronal function for specific behaviours remain speculative, in vertebrates and invertebrates. To address this, we generated an inducible dominant negative form of the IPR (IPR). Flies with neuronal expression of IPR exhibit flight deficits. Expression of IPR helped identify key flight-modulating dopaminergic neurons with axonal projections in the mushroom body. Flies with attenuated IPRs in these presynaptic dopaminergic neurons exhibit shortened flight bouts and a disinterest in seeking food, accompanied by reduced excitability and dopamine release upon cholinergic stimulation. Our findings suggest that the same neural circuit modulates the drive for food search and for undertaking longer flight bouts.

Citing Articles

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References

Chakraborty S, Hasan G . Functional complementation of Drosophila itpr mutants by rat Itpr1. J Neurogenet. 2012; 26(3-4):328-37. DOI: 10.3109/01677063.2012.697501. View

Aso Y, Hattori D, Yu Y, Johnston R, Iyer N, Ngo T . The neuronal architecture of the mushroom body provides a logic for associative learning. Elife. 2014; 3:e04577. PMC: 4273437. DOI: 10.7554/eLife.04577. View

Lutas A, Wahlmark C, Acharjee S, Kawasaki F . Genetic analysis in Drosophila reveals a role for the mitochondrial protein p32 in synaptic transmission. G3 (Bethesda). 2012; 2(1):59-69. PMC: 3276185. DOI: 10.1534/g3.111.001586. View

Manjila S, Hasan G . Flight and Climbing Assay for Assessing Motor Functions in . Bio Protoc. 2021; 8(5):e2742. PMC: 8203865. DOI: 10.21769/BioProtoc.2742. View

Agrawal T, Sadaf S, Hasan G . A genetic RNAi screen for IP₃/Ca²⁺ coupled GPCRs in Drosophila identifies the PdfR as a regulator of insect flight. PLoS Genet. 2013; 9(10):e1003849. PMC: 3789835. DOI: 10.1371/journal.pgen.1003849. View

Tsao C, Chen C, Lin C, Yang H, Lin S . mushroom bodies integrate hunger and satiety signals to control innate food-seeking behavior. Elife. 2018; 7. PMC: 5910021. DOI: 10.7554/eLife.35264. View

Agrawal N, Padmanabhan N, Hasan G . Inositol 1,4,5- trisphosphate receptor function in Drosophila insulin producing cells. PLoS One. 2009; 4(8):e6652. PMC: 2721413. DOI: 10.1371/journal.pone.0006652. View

Aso Y, Rubin G . Dopaminergic neurons write and update memories with cell-type-specific rules. Elife. 2016; 5. PMC: 4987137. DOI: 10.7554/eLife.16135. View

Cervantes-Sandoval I, Phan A, Chakraborty M, Davis R . Reciprocal synapses between mushroom body and dopamine neurons form a positive feedback loop required for learning. Elife. 2017; 6. PMC: 5425253. DOI: 10.7554/eLife.23789. View

10.

Baines R, Uhler J, Thompson A, Sweeney S, Bate M . Altered electrical properties in Drosophila neurons developing without synaptic transmission. J Neurosci. 2001; 21(5):1523-31. PMC: 6762927. View

11.

Baines R . Postsynaptic protein kinase A reduces neuronal excitability in response to increased synaptic excitation in the Drosophila CNS. J Neurosci. 2003; 23(25):8664-72. PMC: 6740429. View

12.

Scaplen K, Talay M, Fisher J, Cohn R, Sorkac A, Aso Y . Transsynaptic mapping of mushroom body output neurons. Elife. 2021; 10. PMC: 7877909. DOI: 10.7554/eLife.63379. View

13.

Kitamoto T . Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J Neurobiol. 2001; 47(2):81-92. DOI: 10.1002/neu.1018. View

14.

Terry L, Alzayady K, Furati E, Yule D . Inositol 1,4,5-trisphosphate Receptor Mutations associated with Human Disease. Messenger (Los Angel). 2018; 6(1-2):29-44. PMC: 6128530. View

15.

Handler A, Graham T, Cohn R, Morantte I, Siliciano A, Zeng J . Distinct Dopamine Receptor Pathways Underlie the Temporal Sensitivity of Associative Learning. Cell. 2019; 178(1):60-75.e19. PMC: 9012144. DOI: 10.1016/j.cell.2019.05.040. View

16.

Agrawal N, Venkiteswaran G, Sadaf S, Padmanabhan N, Banerjee S, Hasan G . Inositol 1,4,5-trisphosphate receptor and dSTIM function in Drosophila insulin-producing neurons regulates systemic intracellular calcium homeostasis and flight. J Neurosci. 2010; 30(4):1301-13. PMC: 6633787. DOI: 10.1523/JNEUROSCI.3668-09.2010. View

17.

Venkatesh K, Siddhartha G, Joshi R, Patel S, Hasan G . Interactions between the inositol 1,4,5-trisphosphate and cyclic AMP signaling pathways regulate larval molting in Drosophila. Genetics. 2001; 158(1):309-18. PMC: 1461650. DOI: 10.1093/genetics/158.1.309. View

18.

Pathak T, Agrawal T, Richhariya S, Sadaf S, Hasan G . Store-Operated Calcium Entry through Orai Is Required for Transcriptional Maturation of the Flight Circuit in Drosophila. J Neurosci. 2015; 35(40):13784-99. PMC: 6605383. DOI: 10.1523/JNEUROSCI.1680-15.2015. View

19.

Root C, Ko K, Jafari A, Wang J . Presynaptic facilitation by neuropeptide signaling mediates odor-driven food search. Cell. 2011; 145(1):133-44. PMC: 3073827. DOI: 10.1016/j.cell.2011.02.008. View

20.

Bartok A, Weaver D, Golenar T, Nichtova Z, Katona M, Bansaghi S . IP receptor isoforms differently regulate ER-mitochondrial contacts and local calcium transfer. Nat Commun. 2019; 10(1):3726. PMC: 6700175. DOI: 10.1038/s41467-019-11646-3. View