Skip to main content
SpringerLink
Log in

Manipulation of Neural Circuits in Drosophila Larvae

  • Chapter
  • First Online:
Decoding Neural Circuit Structure and Function

Abstract

Drosophila has proven to be an extraordinarily prolific model organism to study the integrated function of neural circuits. This success largely stems from the development of powerful genetic tools to monitor and to manipulate the activity of identified neurons in the fly nervous system. However, establishing causal relationships between the activity of a given neuron and the expression of a behavior remains challenging both at a technical and at a conceptual level. First, the characterization of behavioral phenotypes still lacks standardization in the field. Here, we illustrate the importance of quantitative analysis of behaviors as complex as sensory navigation (chemotaxis). Second, experimenters are often confronted with the absence of suitable reagents to exclusively label their neurons of interest. A driver line associated with an interesting loss- or gain-of-function phenotype often covers a heterogeneous group of neurons. In the present chapter, we describe how reagents freely available to the fly community can be combined to nail down the relationships between phenotypic traits and the activity of single neurons.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Asahina K, Watanabe K, Duistermars BJ, Hoopfer E, Gonzalez CR, Eyjolfsdottir EA, Perona P, Anderson DJ (2014) Tachykinin-expressing neurons control male-specific aggressive arousal in Drosophila. Cell 156(1–2):221–235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aso Y, Hattori D, Yu Y, Johnston RM, Iyer NA, Ngo TT, Dionne H, Abbott LF, Axel R, Tanimoto H, Rubin GM (2014) The neuronal architecture of the mushroom body provides a logic for associative learning. eLIFE 3:e04577

    PubMed  PubMed Central  Google Scholar 

  • Baines RA, Uhler JP, Thompson A, Sweeney ST, Bate M (2001) Altered electrical properties in Drosophila neurons developing without synaptic transmission. J Neurosci 21(5):1523–1531

    CAS  PubMed  Google Scholar 

  • Bidaye SS, Machacek C, Wu Y, Dickson BJ (2014) Neuronal control of Drosophila walking direction. Science 344(6179):97–101

    Article  CAS  PubMed  Google Scholar 

  • Clark MQ, McCumsey SJ, Lopez-Darwin S, Heckscher ES, Doe CQ (2016) Functional genetic screen to identify interneurons governing behaviorally distinct aspects of Drosophila larval motor programs. G3 (Bethesda) 6(7):2023–2031

    Google Scholar 

  • Duda RO, Hart PE, Stork DG (2001) Pattern classification. Wiley, New York

    Google Scholar 

  • Ebrahim SA, Dweck HK, Stokl J, Hofferberth JE, Trona F, Weniger K, Rybak J, Seki Y, Stensmyr MC, Sachse S, Hansson BS, Knaden M (2015) Drosophila avoids parasitoids by sensing their semiochemicals via a dedicated olfactory circuit. PLoS Biol 13(12):e1002318

    Article  PubMed  PubMed Central  Google Scholar 

  • Egnor SE, Branson K (2016) Computational analysis of behavior. Annu Rev Neurosci 39:217–236

    Article  CAS  PubMed  Google Scholar 

  • Fenno L, Yizhar O, Deisseroth K (2011) The development and application of optogenetics. Annu Rev Neurosci 34:389–412

    Article  CAS  PubMed  Google Scholar 

  • Gepner RM, Skanata M, Bernat NM, Kaplow M, Gershow M (2015) Computations underlying Drosophila photo-taxis, odor-taxis, and multi-sensory integration. eLIFE 4

    Google Scholar 

  • Gerber B, Stocker RF (2007) The Drosophila larva as a model for studying chemosensation and chemosensory learning: a review. Chem Senses 32(1):65–89

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Marin A, Stephens GJ, Louis M (2011) Active sampling and decision making in Drosophila chemotaxis. Nat Commun 2:441

    Article  PubMed  PubMed Central  Google Scholar 

  • Gonzalez-Bellido PT, Wardill TJ, Kostyleva R, Meinertzhagen IA, Juusola M (2009) Overexpressing temperature-sensitive dynamin decelerates phototransduction and bundles microtubules in Drosophila photoreceptors. J Neurosci 29(45):14199–14210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gordon MD, Scott K (2009) Motor control in a Drosophila taste circuit. Neuron 61(3):373–384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Green CH, Burnet B, Connolly KJ (1983) Organization and patterns of inter- and intraspecific variation in the behaviour of Drosophila larvae. Anim Behav 31(1):282–291

    Article  Google Scholar 

  • Hampel S, Franconville R, Simpson JH, Seeds AM (2015) A neural command circuit for grooming movement control. eLIFE 4:e08758

    Article  PubMed  PubMed Central  Google Scholar 

  • Hartenstein V, Younossi-Hartenstein A, Lovick JK, Kong A, Omoto JJ, Ngo KT, Viktorin G (2015) Lineage-associated tracts defining the anatomy of the Drosophila first instar larval brain. Dev Biol 406(1):14–39

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hernandez-Nunez L, Belina J, Klein M, Si G, Claus L, Carlson JR, Samuel ADT (2015) Reverse-correlation analysis of navigation dynamics in Drosophila larva using optogenetics. eLIFE 4

    Google Scholar 

  • Hwang RY, Zhong L, Xu Y, Johnson T, Zhang F, Deisseroth K, Tracey WD (2007) Nociceptive neurons protect Drosophila larvae from parasitoid wasps. Curr Biol 17(24):2105–2116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inagaki HK, Jung Y, Hoopfer ED, Wong AM, Mishra N, Lin JY, Tsien RY, Anderson DJ (2014) Optogenetic control of Drosophila using a red-shifted Channelrhodopsin reveals experience-dependent influences on courtship. Nat Methods 11(3):325–332

    Google Scholar 

  • Jenett A, Rubin GM, Ngo TT, Shepherd D, Murphy C, Dionne H, Pfeiffer BD, Cavallaro A, Hall D, Jeter J, Iyer N, Fetter D, Hausenfluck JH, Peng H, Trautman ET, Svirskas RR, Myers EW, Iwinski ZR, Aso Y, DePasquale GM, Enos A, Hulamm P, Lam SC, Li HH, Laverty TR, Long F, Qu L, Murphy SD, Rokicki K, Safford T, Shaw K, Simpson JH, Sowell A, Tae S, Yu Y, Zugates CT (2012) A GAL4-driver line resource for Drosophila neurobiology. Cell Rep 2(4):991–1001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kane EA, Gershow M, Afonso B, Larderet I, Klein M, Carter AR, de Bivort BL, Sprecher SG, Samuel AD (2013) Sensorimotor structure of Drosophila larva phototaxis. Proc Natl Acad Sci U S A 110(40):E3868–E3877

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klapoetke NC, Murata Y, Kim SS, Pulver SR, Birdsey-Benson A, Cho YK, Morimoto TK, Chuong AS, Carpenter EJ, Tian Z, Wang J, Xie Y, Yan Z, Zhang Y, Chow BY, Surek B, Melkonian M, Jayaraman V, Constantine-Paton M, Wong GK, Boyden ES (2014) Independent optical excitation of distinct neural populations. Nat Methods 11(3):338–346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li HH, Kroll JR, Lennox SM, Ogundeyi O, Jeter J, Depasquale G, Truman JW (2014) A GAL4 driver resource for developmental and behavioral studies on the larval CNS of Drosophila. Cell Rep 8(3):897–908

    Article  CAS  PubMed  Google Scholar 

  • Luan H, Peabody NC, Vinson CR, White BH (2006) Refined spatial manipulation of neuronal function by combinatorial restriction of transgene expression. Neuron 52(3):425–436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo L, Gershow M, Rosenzweig M, Kang K, Fang-Yen C, Garrity PA, Samuel AD (2010) Navigational decision making in Drosophila thermotaxis. J Neurosci 30(12):4261–4272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marella S, Mann K, Scott K (2012) Dopaminergic modulation of sucrose acceptance behavior in Drosophila. Neuron 73(5):941–950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsunaga T, Fushiki A, Nose A, Kohsaka H (2013) Optogenetic perturbation of neural activity with laser illumination in semi-intact Drosophila larvae in motion. J Vis Exp 77:e50513

    Google Scholar 

  • Nern A, Pfeiffer BD, Rubin GM (2015) Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system. Proc Natl Acad Sci U S A 112(22):E2967–E2976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohyama T, Schneider-Mizell CM, Fetter RD, Aleman JV, Franconville R, Rivera-Alba M, Mensh BD, Branson KM, Simpson JH, Truman JW, Cardona A, Zlatic M (2015) A multilevel multimodal circuit enhances action selection in Drosophila. Nature 520(7549):633–639

    Article  CAS  PubMed  Google Scholar 

  • Olsen SR, Wilson RI (2008) Cracking neural circuits in a tiny brain: new approaches for understanding the neural circuitry of Drosophila. Trends Neurosci 31(10):512–520

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfeiffer BD, Jenett A, Hammonds AS, Ngo TT, Misra S, Murphy C, Scully A, Carlson JW, Wan KH, Laverty TR, Mungall C, Svirskas R, Kadonaga JT, Doe CQ, Eisen MB, Celniker SE, Rubin GM (2008) Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci U S A 105(28):9715–9720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfeiffer BD, Ngo TT, Hibbard KL, Murphy C, Jenett A, Truman JW, Rubin GM (2010) Refinement of tools for targeted gene expression in Drosophila. Genetics 186(2):735–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pulver SR, Pashkovski SL, Hornstein NJ, Garrity PA, Griffith LC (2009) Temporal dynamics of neuronal activation by Channelrhodopsin-2 and TRPA1 determine behavioral output in Drosophila larvae. J Neurophysiol 101(6):3075–3088

    Google Scholar 

  • Rosenzweig M, Kang K, Garrity PA (2008) Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster. Proc Natl Acad Sci U S A 105(38):14668–14673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schleyer M, Reid SF, Pamir E, Saumweber T, Paisios E, Davies A, Gerber B, Louis M (2015) The impact of odor-reward memory on chemotaxis in larval Drosophila. Learn Mem 22(5):267–277

    Article  PubMed  PubMed Central  Google Scholar 

  • Schneider-Mizell CM, Gerhard S, Longair M, Kazimiers T, Li F, Zwart MF, Champion A, Midgley FM, Fetter RD, Saalfeld S, Cardona A (2016) Quantitative neuroanatomy for connectomics in Drosophila. eLIFE 5

    Google Scholar 

  • Schroll C, Riemensperger T, Bucher D, Ehmer J, Voller T, Erbguth K, Gerber B, Hendel T, Nagel G, Buchner E, Fiala A (2006) Light-induced activation of distinct modulatory neurons triggers appetitive or aversive learning in Drosophila larvae. Curr Biol 16(17):1741–1747

    Article  CAS  PubMed  Google Scholar 

  • Schulze A, Gomez-Marin A, Rajendran VG, Lott G, Musy M, Ahammad P, Deogade A, Sharpe J, Riedl J, Jarriault D, Trautman ET, Werner C, Venkadesan M, Druckmann S, Jayaraman V, Louis M (2015). Dynamical feature extraction at the sensory periphery guides chemotaxis. eLIFE 4

    Google Scholar 

  • Simpson JH (2009) Mapping and manipulating neural circuits in the fly brain. Adv Genet 65:79–143

    CAS  PubMed  Google Scholar 

  • Sweeney ST, Broadie K, Keane J, Niemann H, O’Kane CJ (1995) Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14(2):341–351

    Article  CAS  PubMed  Google Scholar 

  • Szigeti B, Deogade A, Webb B (2015) Searching for motifs in the behaviour of larval Drosophila melanogaster and Caenorhabditis elegans reveals continuity between behavioural states. J R Soc Interface 12(113):20150899

    Article  PubMed  PubMed Central  Google Scholar 

  • Tastekin I, Riedl J, Schilling-Kurz V, Gomez-Marin A, Truman JW, Louis M (2015) Role of the subesophageal zone in sensorimotor control of orientation in Drosophila larva. Curr Biol 25(11):1448–1460

    Article  CAS  PubMed  Google Scholar 

  • Thum AS, Knapek S, Rister J, Dierichs-Schmitt E, Heisenberg M, Tanimoto H (2006) Differential potencies of effector genes in adult Drosophila. J Comp Neurol 498(2):194–203

    Article  CAS  PubMed  Google Scholar 

  • Venken KJ, Simpson JH, Bellen HJ (2011) Genetic manipulation of genes and cells in the nervous system of the fruit fly. Neuron 72(2):202–230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vogelstein JT, Park Y, Ohyama T, Kerr RA, Truman JW, Priebe CE, Zlatic M (2014) Discovery of brainwide neural-behavioral maps via multiscale unsupervised structure learning. Science 344(6182):386–392

    Article  CAS  PubMed  Google Scholar 

  • von Philipsborn AC, Liu T, Yu JY, Masser C, Bidaye SS, Dickson BJ (2011) Neuronal control of Drosophila courtship song. Neuron 69(3):509–522

    Article  Google Scholar 

  • Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109(2):229–241

    Article  CAS  PubMed  Google Scholar 

  • Yoshikawa S, Long H, Thomas JB (2016) A subset of interneurons required for Drosophila larval locomotion. Mol Cell Neurosci 70:22–29

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Ge W, Wang Z (2007) A toolbox for light control of Drosophila behaviors through Channelrhodopsin 2-mediated photo activation of targeted neurons. Eur J Neurosci 26(9):2405–2416

    Google Scholar 

  • Zhang W, Yan Z, Jan LY, Jan YN (2013) Sound response mediated by the TRP channels NOMPC, NANCHUNG, and INACTIVE in chordotonal organs of Drosophila larvae. Proc Natl Acad Sci U S A 110(33):13612–13617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmermann G, Wang LP, Vaughan AG, Manoli DS, Zhang F, Deisseroth K, Baker BS, Scott MP (2009) Manipulation of an innate escape response in Drosophila: photoexcitation of acj6 neurons induces the escape response. PLoS One 4(4):e5100

    Article  PubMed  PubMed Central  Google Scholar 

  • Zwart MF, Pulver SR, Truman JW, Fushiki A, Fetter RD, Cardona A, Landgraf M (2016) Selective inhibition mediates the sequential recruitment of motor pools. Neuron 91(3):615–628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Dr. Aiguader 88, 08003, Barcelona, Spain

    Ibrahim Tastekin & Matthieu Louis

  2. Universitat Pompeu Fabra (UPF), 08002, Barcelona, Spain

    Ibrahim Tastekin & Matthieu Louis

  3. Neuroscience Research Institute and Department of Molecular, Cellular and Developmental Biology, University of California Santa Barbara, 93106, Santa Barbara, California, USA

    Matthieu Louis

Authors
  1. Ibrahim Tastekin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthieu Louis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthieu Louis .

Editor information

Editors and Affiliations

  1. Department of Molecular Biology and Genetics, Boğaziçi University, Bebek, Istanbul, Turkey

    Arzu Çelik

  2. Fachbereich Biologie, Chemie, Pharmazie, Institut für Biologie—Neurobiologie, Freie Universität Berlin, Berlin, Germany

    Mathias F. Wernet

Rights and permissions

Reprints and permissions

Copyright information

© 2017 Springer International Publishing AG

About this chapter

Cite this chapter

Tastekin, I., Louis, M. (2017). Manipulation of Neural Circuits in Drosophila Larvae. In: Çelik, A., Wernet, M. (eds) Decoding Neural Circuit Structure and Function. Springer, Cham. https://doi.org/10.1007/978-3-319-57363-2_6

Download citation

Publish with us

Policies and ethics

Search

Navigation