Abstract
Monoaminergic modulation of insect flight is well documented. Recently, we demonstrated that synaptic activity is required in serotonergic neurons for Drosophila flight. This requirement is during early pupal development, when the flight circuit is formed, as well as in adults. Using a Ca2+-activity-based GFP reporter, here we show that serotonergic neurons in both prothoracic and mesothoracic segments are activated upon air-puff-stimulated flight. Moreover ectopic activation of the entire serotonergic system by TrpA1, a heat activated cation channel, induces flight, even in the absence of an air-puff stimulus.
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References
Banerjee S, Lee J, Venkatesh K, Wu CF and Hasan G 2004 Loss of flight and associated neuronal rhythmicity in inositol 1,4,5-trisphosphate receptor mutants of Drosophila. J. Neurosci. 24 7869–7878
Barreteau H, Perriere C, Brousse-Gaury P, Gayral P, Jacquot C and Goudey-Perriere F 1991 Indolamines in the cockroach Blaberus craniifer Burm. nervous system--I. Fed and crowded young females. Comp. Biochem. Physiol. C. 99 567–571
Berkowitz A and Laurent G 1996 Local control of leg movements and motor patterns during grooming in locusts. J. Neurosci. 16 8067–8078
Bidaye SS, Machacek C, Wu Y and Dickson BJ 2014 Neuronal control of Drosophila walking direction. Sci. 344 97–101
Brembs B, Christiansen F, Pfluger HJ and Duch C 2007 Flight initiation and maintenance deficits in flies with genetically altered biogenic amine levels. J. Neurosci. 27 11122–11131
Buhl E, Schildberger K and Stevenson PA 2008 A muscarinic cholinergic mechanism underlies activation of the central pattern generator for locust flight. J. Exp. Biol. 211 2346–2357
Claassen DE and Kammer AE 1986 Effects of octopamine, dopamine, and serotonin on production of flight motor output by thoracic ganglia of Manduca sexta. J. Neurobiol. 17 1–14
Consoulas C, Levine RB and Restifo LL 2005 The steroid hormone-regulated gene Broad Complex is required for dendritic growth of motoneurons during metamorphosis of Drosophila. J. Comp. Neurol. 485 321–337
Dickinson MH and Tu MS 1997 The function of dipteran flight muscle. Comp. Biochem. Physiol. Part A: Physiol. 116 223–238
Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, Jegla TJ and Garrity PA 2008 An internal thermal sensor controlling temperature preference in Drosophila. Nature 454 217–220
Hammond S and O'Shea M 2007 Escape flight initiation in the fly. J. Comp. Physiol. A Neuroethol. Sens. Neural. Behav. Physiol. 193 471–476
Hasan G 2012 The early years of Drosophila chemosensory genetics in Mumbai's Tata Institute of Fundamental Research. J. Neurogenet. 26 264–266
Kamyshev NG, Smirnova GP, Savvateeva EV, Medvedeva AV and Ponomarenko VV 1983 The influence of serotonin and p-chlorophenylalanine on locomotor activity of Drosophila melanogaster. Pharmacol. Biochem. Behav. 18 677–681
Lai SL and Lee T 2006 Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 9 703–709
Li H, Chaney S, Roberts IJ, Forte M and Hirsh J 2000 Ectopic G-protein expression in dopamine and serotonin neurons blocks cocaine sensitization in Drosophila melanogaster. Curr. Biol. 10 211–214
Lorez M 1995 Neural control of hindleg steering in flight in the locust. J. Exp. Biol. 198 869–875
Masuyama K, Zhang Y, Rao Y and Wang JW 2012 Mapping neural circuits with activity-dependent nuclear import of a transcription factor. J. Neurogenet. 26 89–102
Neckameyer WS, Coleman CM, Eadie S and Goodwin SF 2007 Compartmentalization of neuronal and peripheral serotonin synthesis in Drosophila melanogaster. Genes Brain Behav. 6 756–769
Novak MG and Rowley WA 1994 Serotonin depletion affects blood-feeding but not host-seeking ability in Aedes triseriatus (Diptera: Culicidae). J. Med. Entomol. 31 600–606
Parker D 1995 Serotonergic modulation of locust motor neurons. J. Neurophysiol. 73 923–932
Rillich J, Stevenson PA and Pflueger HJ 2013 Flight and walking in locusts-cholinergic co-activation, temporal coupling and its modulation by biogenic amines. PLoS One 8 e62899
Ritzmann R and Zill SN 2013 Neuroethology of insect walking. Scholarpedia 8 30879
Sadaf S, Birman S and Hasan G 2012 Synaptic Activity in serotonergic neurons is required for air-puff stimulated flight in Drosophila melanogaster. PLoS One 7 e46405
Sadaf S, Reddy OV, Sane SP and Hasan G Context-dependent neural control of wing coordination in flies. Under Review
Sane SP, Dieudonne A, Willis MA and Daniel TL 2007 Antennal mechanosensors mediate flight control in moths. Science 315 863–866
Sitaraman D, LaFerriere H, Birman S and Zars T 2012 Serotonin is critical for rewarded olfactory short-term memory in Drosophila. J. Neurogenet. 26 238–244
Sombati S and Hoyle G 1984 Generation of specific behaviors in a locust by local release into neuropil of the natural neuromodulator octopamine. J. Neurobiol. 15 481–506
Stevenson P and Meuser S 1997 Octopaminergic innervation and modulation of a locust flight steering muscle. J. Exp. Biol. 200 633–642
Strauss R 2002 The central complex and the genetic dissection of locomotor behaviour. Curr. Opin. Neurobiol. 12 633–638
Vandervorst P and Ghysen A 1980 Genetic control of sensory connections in Drosophila. Nature 286 65–67
Acknowledgements
This work was supported by a research fellowship from the Council of Scientific and Industrial research ( http://rdpp.csir.res.in/csir_acsir/Home.aspx ) to SS. The project was supported financially by core funding from the National Centre for Biological Sciences, Tata Institute of Fundamental Research ( http://www.ncbs.res.in ), to GH. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. We thank Dr Serge Birman (ESPCI, France) for providing reagents and Dr H Krishnamurthy and the NCBS Central Image-Flow Facility for help with confocal imaging.
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[Sadaf S and Hasan G 2014 Serotonergic neurons of the Drosophila air-puff-stimulated flight circuit. J. Biosci. 39 1–9] DOI 10.1007/s12038-014-9449-5
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Sadaf, S., Hasan, G. Serotonergic neurons of the Drosophila air-puff-stimulated flight circuit. J Biosci 39, 575–583 (2014). https://doi.org/10.1007/s12038-014-9449-5
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DOI: https://doi.org/10.1007/s12038-014-9449-5