Genetic Manipulation of Genes and Cells in the Nervous System of the Fruit Fly

Research in the fruit fly Drosophila melanogaster has led to insights in neural development, axon guidance, ion channel function, synaptic transmission, learning and memory, diurnal rhythmicity, and neural disease that have had broad implications for neuroscience. Drosophila is currently the eukaryotic model organism that permits the most sophisticated in vivo manipulations to address the function of neurons and neuronally expressed genes. Here, we summarize many of the techniques that help assess the role of specific neurons by labeling, removing, or altering their activity. We also survey genetic manipulations to identify and characterize neural genes by mutation, overexpression, and protein labeling. Here, we attempt to acquaint the reader with available options and contexts to apply these methods.

[1]  Scott Barolo,et al.  New Drosophila transgenic reporters: insulated P-element vectors expressing fast-maturing RFP. , 2004, BioTechniques.

[2]  Jay Hirsh,et al.  A Pair of Dopamine Neurons Target the D1-Like Dopamine Receptor DopR in the Central Complex to Promote Ethanol-Stimulated Locomotion in Drosophila , 2010, PloS one.

[3]  C. Sabatti,et al.  Robust discrimination between self and non-self neurites requires thousands of Dscam1 isoforms , 2009, Nature.

[4]  Y. Rong,et al.  A targeted gene knockout in Drosophila. , 2001, Genetics.

[5]  C. Doe Neural stem cells: balancing self-renewal with differentiation , 2008, Development.

[6]  W. Gelbart,et al.  Using the P[wHy] hybrid transposable element to disrupt genes in region 54D-55B in Drosophila melanogaster. , 2002, Genetics.

[7]  B. Dickson,et al.  Distinct Protein Domains and Expression Patterns Confer Divergent Axon Guidance Functions for Drosophila Robo Receptors , 2010, Cell.

[8]  Richard Y. Hwang,et al.  Pickpocket Is a DEG/ENaC Protein Required for Mechanical Nociception in Drosophila Larvae , 2010, Current Biology.

[9]  K. J. Sepp,et al.  Conversion of lacZ enhancer trap lines to GAL4 lines using targeted transposition in Drosophila melanogaster. , 1999, Genetics.

[10]  Karl Mechtler,et al.  BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals , 2008, Nature Methods.

[11]  Jeff J. Sekelsky,et al.  From sequence to phenotype: reverse genetics in drosophila melanogaster , 2002, Nature Reviews Genetics.

[12]  M. Noll,et al.  Sensory Integration Regulating Male Courtship Behavior in Drosophila , 2009, PloS one.

[13]  A. Borst,et al.  Fly motion vision. , 2010, Annual review of neuroscience.

[14]  W. Gelbart,et al.  A deletion-generator compound element allows deletion saturation analysis for genomewide phenotypic annotation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Liqun Luo,et al.  Wiring Stability of the Adult Drosophila Olfactory Circuit after Lesion , 2006, The Journal of Neuroscience.

[16]  P. Hiesinger,et al.  Mapping Drosophila mutations with molecularly defined P element insertions , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Sunil Q. Mehta,et al.  Synaptojanin Is Recruited by Endophilin to Promote Synaptic Vesicle Uncoating , 2003, Neuron.

[18]  S. Lindquist,et al.  The FLP recombinase of yeast catalyzes site-specific recombination in the drosophila genome , 1989, Cell.

[19]  Gero Miesenböck,et al.  Transmission of Olfactory Information between Three Populations of Neurons in the Antennal Lobe of the Fly , 2002, Neuron.

[20]  James J. L. Hodge,et al.  Ion Channels to Inactivate Neurons in Drosophila , 2009, Front. Mol. Neurosci..

[21]  Andreas Prokop,et al.  Are dendrites in Drosophila homologous to vertebrate dendrites? , 2005, Developmental biology.

[22]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[23]  H. Vogel,et al.  Drosophila models of neurodegenerative diseases. , 2009, Annual review of pathology.

[24]  D. LaJeunesse,et al.  Three new Drosophila markers of intracellular membranes. , 2004, BioTechniques.

[25]  Doris Chen,et al.  Genome-wide analysis of Notch signalling in Drosophila by transgenic RNAi , 2009, Nature.

[26]  C. O’Kane Drosophila as a model organism for the study of neuropsychiatric disorders. , 2011, Current topics in behavioral neurosciences.

[27]  Kiyoko F. Aoki-Kinoshita,et al.  Identification of Genes Required for Neural-Specific Glycosylation Using Functional Genomics , 2010, PLoS genetics.

[28]  Jeffrey C. Hall,et al.  Neurogenetics of courtship and mating in Drosophila. , 2008, Advances in genetics.

[29]  T. Holmes,et al.  2 Circuit-breaking and Behavioral Analysis by Molecular Genetic Manipulation of Neural Activity in Drosophila , 2007 .

[30]  B. Barrell,et al.  Mapping and identification of essential gene functions on the X chromosome of Drosophila , 2002, EMBO reports.

[31]  Andreas S. Thum,et al.  Differential potencies of effector genes in adult Drosophila , 2006, The Journal of comparative neurology.

[32]  M. Low,et al.  Disruption of neurotransmission in Drosophila mushroom body blocks retrieval but not acquisition of memory , 2022 .

[33]  P. Taghert,et al.  Widespread Receptivity to Neuropeptide PDF throughout the Neuronal Circadian Clock Network of Drosophila Revealed by Real-Time Cyclic AMP Imaging , 2008, Neuron.

[34]  H. Bellen,et al.  Transgenesis upgrades for Drosophila melanogaster , 2007, Development.

[35]  I. Meinertzhagen,et al.  Synaptic organization in the fly's optic lamina: few cells, many synapses and divergent microcircuits. , 2001, Progress in brain research.

[36]  E. Kravitz,et al.  Aggression in invertebrates , 2003, Current Opinion in Neurobiology.

[37]  R. W. Draft,et al.  Transgenic strategies for combinatorial expression of fluorescent proteins in the nervous system , 2007, Nature.

[38]  Gilles Laurent,et al.  Evaluating a Genetically Encoded Optical Sensor of Neural Activity Using Electrophysiology in Intact Adult Fruit Flies , 2007, Frontiers in neural circuits.

[39]  T. Mackay,et al.  Mutations in many genes affect aggressive behavior in Drosophila melanogaster , 2009, BMC Biology.

[40]  S. Kunes,et al.  Synaptic Protein Synthesis Associated with Memory Is Regulated by the RISC Pathway in Drosophila , 2006, Cell.

[41]  Bassem A. Hassan,et al.  Conditional Mutagenesis in Drosophila , 2009, Science.

[42]  D. Suzuki,et al.  Temperature-sensitive mutations in Drosophila melanogaster. VII. A mutation (para-ts) causing reversible adult paralysis. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[43]  L. Buck,et al.  A genetic approach to trace neural circuits. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[44]  N. Bonini,et al.  Maintaining the brain: insight into human neurodegeneration from Drosophila melanogaster mutants , 2009, Nature Reviews Genetics.

[45]  Shamik Dasgupta,et al.  A Neural Circuit Mechanism Integrating Motivational State with Memory Expression in Drosophila , 2009, Cell.

[46]  M. Koganezawa,et al.  Fruitless and Doublesex Coordinate to Generate Male-Specific Neurons that Can Initiate Courtship , 2008, Neuron.

[47]  T. Mackay,et al.  The DSC1 channel, encoded by the smi60E locus, contributes to odor-guided behavior in Drosophila melanogaster. , 2002, Genetics.

[48]  Leonard K. Kaczmarek,et al.  Targeted Attenuation of Electrical Activity in Drosophila Using a Genetically Modified K+ Channel , 2001, Neuron.

[49]  S. Cohen,et al.  Recombinase-Mediated Cassette Exchange Provides a Versatile Platform for Gene Targeting: Knockout of miR-31b , 2009, Genetics.

[50]  D. Guarnieri,et al.  Genetic Dissociation of Ethanol Sensitivity and Memory Formation in Drosophila melanogaster , 2008, Genetics.

[51]  P. Brûlet,et al.  In vivo Bioluminescence Imaging of Ca2+ Signalling in the Brain of Drosophila , 2007, PloS one.

[52]  G. Jefferis,et al.  Double Brainbow , 2011, Nature Methods.

[53]  L. Zhou,et al.  Distinct cell killing properties of the Drosophila reaper, head involution defective, and grim genes , 1999, Cell Death and Differentiation.

[54]  W. Pak,et al.  Mutants of the Visual Pathway of Drosophila melanogaster , 1970, Nature.

[55]  R. Hoskins,et al.  Exploring Strategies for Protein Trapping in Drosophila , 2007, Genetics.

[56]  L. Luo,et al.  Mosaic Analysis with Double Markers in Mice , 2005, Cell.

[57]  C. Thummel,et al.  Inducible expression of double-stranded RNA directs specific genetic interference in Drosophila , 2000, Current Biology.

[58]  H. Ishimoto,et al.  Neuronal Mechanisms of Learning and Memory Revealed by Spatial and Temporal Suppression of Neurotransmission Using Shibirets1, a Temperature-Sensitive Dynamin Mutant Gene in Drosophila Melanogaster , 2009, Front. Mol. Neurosci..

[59]  T. Kitamoto Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. , 2001, Journal of neurobiology.

[60]  R J Konopka,et al.  Clock mutants of Drosophila melanogaster. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[61]  Richard Axel,et al.  Spatial Representation of the Glomerular Map in the Drosophila Protocerebrum , 2002, Cell.

[62]  Ronald L. Davis,et al.  Detection of Calcium Transients in DrosophilaMushroom Body Neurons with Camgaroo Reporters , 2003, The Journal of Neuroscience.

[63]  H. Bellen,et al.  Rumi Is a CAP10 Domain Glycosyltransferase that Modifies Notch and Is Required for Notch Signaling , 2008, Cell.

[64]  L. Luo,et al.  Comprehensive Maps of Drosophila Higher Olfactory Centers: Spatially Segregated Fruit and Pheromone Representation , 2007, Cell.

[65]  Aljoscha Nern,et al.  Multiple new site-specific recombinases for use in manipulating animal genomes , 2011, Proceedings of the National Academy of Sciences.

[66]  JF Ferveur,et al.  Genetic feminization of brain structures and changed sexual orientation in male Drosophila , 1995, Science.

[67]  Michael B. Reiser,et al.  Walking Modulates Speed Sensitivity in Drosophila Motion Vision , 2010, Current Biology.

[68]  Liqun Luo,et al.  Glia Engulf Degenerating Axons during Developmental Axon Pruning , 2004, Current Biology.

[69]  K. Golic,et al.  Ends-out, or replacement, gene targeting in Drosophila , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[70]  Soh Kohatsu,et al.  Female Contact Activates Male-Specific Interneurons that Trigger Stereotypic Courtship Behavior in Drosophila , 2011, Neuron.

[71]  E. Popodi,et al.  A Molecularly Defined Duplication Set for the X Chromosome of Drosophila melanogaster , 2010, Genetics.

[72]  L. Luo,et al.  Representation of the Glomerular Olfactory Map in the Drosophila Brain , 2002, Cell.

[73]  J. C. Hall Control of male reproductive behavior by the central nervous system of Drosophila: dissection of a courtship pathway by genetic mosaics. , 1979, Genetics.

[74]  Cyrille Alexandre,et al.  Flybow: genetic multicolor cell labeling for neural circuit analysis in Drosophila melanogaster , 2011, Nature Methods.

[75]  B. Hassan,et al.  A novel method for tissue-specific RNAi rescue in Drosophila , 2009, Nucleic acids research.

[76]  Tom Maniatis,et al.  GAL4 activates transcription in Drosophila , 1988, Nature.

[77]  Daisuke Yamamoto,et al.  Fruitless specifies sexually dimorphic neural circuitry in the Drosophila brain , 2005, Nature.

[78]  J. Belote,et al.  Temperature‐dependent gene silencing by an expressed inverted repeat in Drosophila , 2000, Genesis.

[79]  G. Rubin,et al.  Transposition of cloned P elements into Drosophila germ line chromosomes. , 1982, Science.

[80]  D. Court,et al.  Recombineering: a homologous recombination-based method of genetic engineering , 2009, Nature Protocols.

[81]  V. Hartenstein,et al.  The development of the Drosophila larval brain. , 2008, Advances in experimental medicine and biology.

[82]  Y. Rong,et al.  Gene targeting by homologous recombination in Drosophila. , 2000, Science.

[83]  Tzumin Lee,et al.  Specific Drosophila Dscam Juxtamembrane Variants Control Dendritic Elaboration and Axonal Arborization , 2007, The Journal of Neuroscience.

[84]  Shawn R. Olsen,et al.  Cracking neural circuits in a tiny brain: new approaches for understanding the neural circuitry of Drosophila , 2008, Trends in Neurosciences.

[85]  K. Saigo,et al.  Fate map of the distal portion of Drosophila proboscis as inferred from the expression and mutations of basic patterning genes , 2006, Mechanisms of Development.

[86]  Barry J. Dickson,et al.  Sensory Neurons in the Drosophila Genital Tract Regulate Female Reproductive Behavior , 2009, Neuron.

[87]  A. Ephrussi,et al.  The Ig cell adhesion molecule Basigin controls compartmentalization and vesicle release at Drosophila melanogaster synapses , 2007, The Journal of cell biology.

[88]  E. Suzuki,et al.  Postsynaptic filopodia in muscle cells interact with innervating motoneuron axons , 2000, Nature Neuroscience.

[89]  Michael Ashburner,et al.  The DrosDel Deletion Collection: A Drosophila Genomewide Chromosomal Deficiency Resource , 2007, Genetics.

[90]  Peter Smibert,et al.  Know thy fly. , 2007, Trends in genetics : TIG.

[91]  P. Greengard,et al.  Writing Memories with Light-Addressable Reinforcement Circuitry , 2009, Cell.

[92]  J. C. Yin,et al.  Adaptable doxycycline-regulated gene expression systems for Drosophila. , 2001, Gene.

[93]  In Vivo Light-induced and Basal Phospholipase C Activity in Drosophila Photoreceptors Measured with Genetically Targeted Phosphatidylinositol 4,5-Bisphosphate-sensitive Ion Channels (Kir2.1)* , 2004, Journal of Biological Chemistry.

[94]  Christopher A. Voigt,et al.  The promise of optogenetics in cell biology: interrogating molecular circuits in space and time , 2011, Nature Methods.

[95]  T. Mackay,et al.  Quantitative genetic analyses of complex behaviours in Drosophila , 2004, Nature Reviews Genetics.

[96]  Nele A. Haelterman,et al.  MiMIC: a highly versatile transposon insertion resource for engineering Drosophila melanogaster genes , 2011, Nature Methods.

[97]  Nathan C. Klapoetke,et al.  A High-Light Sensitivity Optical Neural Silencer: Development and Application to Optogenetic Control of Non-Human Primate Cortex , 2010, Front. Syst. Neurosci..

[98]  N. Peabody,et al.  Characterization of the Decision Network for Wing Expansion in Drosophila Using Targeted Expression of the TRPM8 Channel , 2009, The Journal of Neuroscience.

[99]  Ronald L. Davis,et al.  Thirty years of olfactory learning and memory research in Drosophila melanogaster , 2005, Progress in Neurobiology.

[100]  Kendal Broadie,et al.  Living synaptic vesicle marker: Synaptotagmin‐GFP , 2002, Genesis.

[101]  Cell ablation using wild‐type and cold‐sensitive ricin‐a chain in drosophila embryonic mesoderm , 2002, Genesis.

[102]  Devanand S. Manoli,et al.  Manipulation of an Innate Escape Response in Drosophila: Photoexcitation of acj6 Neurons Induces the Escape Response , 2009, PloS one.

[103]  M. McVey,et al.  Removal of the Bloom Syndrome DNA Helicase Extends the Utility of Imprecise Transposon Excision for Making Null Mutations in Drosophila , 2009, Genetics.

[104]  T. Mackay,et al.  Pinocchio, a novel protein expressed in the antenna, contributes to olfactory behavior in Drosophila melanogaster. , 2005, Journal of neurobiology.

[105]  Sen-Lin Lai,et al.  Genetic mosaic with dual binary transcriptional systems in Drosophila , 2006, Nature Neuroscience.

[106]  D. Curtis,et al.  Systematic generation of high-resolution deletion coverage of the Drosophila melanogaster genome , 2004, Nature Genetics.

[107]  G. Davis,et al.  Green fluorescent protein tagging Drosophila proteins at their native genomic loci with small P elements. , 2003, Genetics.

[108]  Arnim Jenett,et al.  The Virtual Insect Brain protocol: creating and comparing standardized neuroanatomy , 2006, BMC Bioinformatics.

[109]  M. Bienz,et al.  LexA chimeras reveal the function of Drosophila Fos as a context-dependent transcriptional activator. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[110]  K. Deisseroth,et al.  eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications , 2008, Brain cell biology.

[111]  Martin Heisenberg,et al.  Targeted expression of tetanus neurotoxin interferes with behavioral responses to sensory input in Drosophila. , 2002, Journal of neurobiology.

[112]  T. Schwarz,et al.  A genetic method for generating Drosophila eyes composed exclusively of mitotic clones of a single genotype. , 1999, Genetics.

[113]  Y. Jan,et al.  Enhancer-driven membrane markers for analysis of nonautonomous mechanisms reveal neuron–glia interactions in Drosophila , 2011, Proceedings of the National Academy of Sciences.

[114]  R. Davis,et al.  The Role of Drosophila Mushroom Body Signaling in Olfactory Memory , 2001, Science.

[115]  P. Garrity,et al.  Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster , 2008, Proceedings of the National Academy of Sciences.

[116]  B. Dickson,et al.  Dscam diversity is essential for neuronal wiring and self-recognition , 2007, Nature.

[117]  A. Spradling,et al.  The Drosophila Gene Disruption Project: Progress Using Transposons With Distinctive Site Specificities , 2011, Genetics.

[118]  F. Leiss,et al.  Characterization of dendritic spines in the Drosophila central nervous system , 2009, Developmental neurobiology.

[119]  Jan Felix Evers,et al.  The development of motor coordination in Drosophila embryos , 2008, Development.

[120]  Kevin P. Keegan,et al.  A dynamic role for the mushroom bodies in promoting sleep in Drosophila , 2006, Nature.

[121]  Michael B. Reiser,et al.  Corrigendum: Two-photon calcium imaging from head-fixed Drosophila during optomotor walking behavior , 2011, Nature Methods.

[122]  Maurice J. Kernan Mechanotransduction and auditory transduction in Drosophila , 2007, Pflügers Archiv - European Journal of Physiology.

[123]  Benjamin H. White,et al.  Neurotrapping: Cellular Screens to Identify the Neural Substrates of Behavior in Drosophila , 2009, Front. Mol. Neurosci..

[124]  Ehud Y Isacoff,et al.  A Genetically Encoded Optical Probe of Membrane Voltage , 1997, Neuron.

[125]  R. Yagi,et al.  Refined LexA transactivators and their use in combination with the Drosophila Gal4 system , 2010, Proceedings of the National Academy of Sciences.

[126]  M. Bate,et al.  Gateway cloning vectors for the LexA-based binary expression system in Drosophila , 2008, Fly.

[127]  Andreas S. Thum,et al.  The Neural Substrate of Spectral Preference in Drosophila , 2008, Neuron.

[128]  S. Hou,et al.  A P-element insertion screen identified mutations in 455 novel essential genes in Drosophila. , 2003, Genetics.

[129]  Function of the Shaw Potassium Channel within the Drosophila Circadian Clock , 2008, PloS one.

[130]  Liqun Luo,et al.  Mosaic Analysis with a Repressible Cell Marker for Studies of Gene Function in Neuronal Morphogenesis , 1999, Neuron.

[131]  An efficient method for recombineering GAL4 and QF drivers , 2011, Fly.

[132]  F. Gabbiani,et al.  A novel neuronal pathway for visually guided escape in Drosophila melanogaster. , 2009, Journal of neurophysiology.

[133]  K. Fischbach,et al.  Identification of regulatory modules mediating specific expression of the roughest gene in Drosophila melanogaster , 2004, Development Genes and Evolution.

[134]  G. Roman,et al.  Conditional expression of UAS‐transgenes in the adult eye with a new gene‐switch vector system , 2002, Genesis.

[135]  N. Perrimon,et al.  Cross-Species RNAi Rescue Platform in Drosophila melanogaster , 2009, Genetics.

[136]  Aravinthan D. T. Samuel,et al.  Running hot and cold: behavioral strategies, neural circuits, and the molecular machinery for thermotaxis in C. elegans and Drosophila. , 2010, Genes & development.

[137]  Kristin Scott,et al.  Limited taste discrimination in Drosophila , 2010, Proceedings of the National Academy of Sciences.

[138]  H. Keshishian,et al.  Molecular genetic approaches to the targeted suppression of neuronal activity , 2001, Current Biology.

[139]  Richard Axel,et al.  A dimorphic pheromone circuit in Drosophila from sensory input to descending output , 2010, Nature.

[140]  J. C. Hall,et al.  Spatial, temporal, and sexually dimorphic expression patterns of the fruitless gene in the Drosophila central nervous system. , 2000, Journal of neurobiology.

[141]  C.-ting Wu,et al.  Site-Specific Transformation of Drosophila via ϕC31 Integrase-Mediated Cassette Exchange , 2006, Genetics.

[142]  Tzumin Lee,et al.  Twin-Spot MARCM to reveal developmental origin and identity of neurons , 2009, Nature Neuroscience.

[143]  L. Luo,et al.  piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. , 2008, Developmental cell.

[144]  Julie H. Simpson,et al.  BrainAligner: 3D Registration Atlases of Drosophila Brains , 2011, Nature Methods.

[145]  D. Yamamoto,et al.  Sexual orientation in Drosophila is altered by the satori mutation in the sex-determination gene fruitless that encodes a zinc finger protein with a BTB domain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[146]  Michele P Calos,et al.  Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. , 2004, Genetics.

[147]  Shin-ya Takemura,et al.  From Form to Function: the Ways to Know a Neuron , 2009, Journal of neurogenetics.

[148]  Haojiang Luan,et al.  Refined Spatial Manipulation of Neuronal Function by Combinatorial Restriction of Transgene Expression , 2006, Neuron.

[149]  J. Chilton Molecular mechanisms of axon guidance. , 2006, Developmental biology.

[150]  X. Morin,et al.  A protein trap strategy to detect GFP-tagged proteins expressed from their endogenous loci in Drosophila , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[151]  N. Perrimon,et al.  Vector and parameters for targeted transgenic RNA interference in Drosophila melanogaster , 2008, Nature Methods.

[152]  R. Gibbs,et al.  Rapid identification of heterozygous mutations in Drosophila melanogaster using genomic capture sequencing. , 2010, Genome research.

[153]  P. Rørth,et al.  A modular misexpression screen in Drosophila detecting tissue-specific phenotypes. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[154]  Lynn Cooley,et al.  Flytrap, a database documenting a GFP protein-trap insertion screen in Drosophila melanogaster , 2004, Nucleic Acids Res..

[155]  Peizhang Xu,et al.  In vivo modification of Na(+),K(+)-ATPase activity in Drosophila. , 2001, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[156]  E. Wimmer,et al.  piggyBac-based insertional mutagenesis and enhancer detection as a tool for functional insect genomics. , 2003, Genetics.

[157]  C. Goodman,et al.  Mutations affecting growth cone guidance in drosophila: Genes necessary for guidance toward or away from the midline , 1993, Neuron.

[158]  G. Davis,et al.  Homeostatic Control of Presynaptic Release Is Triggered by Postsynaptic Membrane Depolarization , 2001, Neuron.

[159]  P. Rørth,et al.  A Sensitized PiggyBac-Based Screen for Regulators of Border Cell Migration in Drosophila , 2007, Genetics.

[160]  Giulio Tononi,et al.  Reduced sleep in Drosophila Shaker mutants , 2005, Nature.

[161]  G. Rubin,et al.  Genetic transformation of Drosophila with transposable element vectors. , 1982, Science.

[162]  Pavel Tomancak,et al.  A toolkit for high-throughput, cross-species gene engineering in Drosophila , 2009, Nature Methods.

[163]  Devanand S. Manoli,et al.  Functional Dissection of the Neural Substrates for Sexual Behaviors in Drosophila melanogaster , 2011, Genetics.

[164]  H. Ueda,et al.  A functional genomics strategy reveals clockwork orange as a transcriptional regulator in the Drosophila circadian clock. , 2007, Genes & development.

[165]  K. Deisseroth,et al.  Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri , 2008, Nature Neuroscience.

[166]  R. Habets,et al.  Jcb: Article , 2022 .

[167]  C. Bökel EMS screens : from mutagenesis to screening and mapping. , 2008, Methods in molecular biology.

[168]  Devanand S. Manoli,et al.  Blueprints for behavior: genetic specification of neural circuitry for innate behaviors , 2006, Trends in Neurosciences.

[169]  V. Hartenstein Morphological diversity and development of glia in Drosophila , 2011, Glia.

[170]  B. Dickson,et al.  Netrins guide Drosophila commissural axons at short range , 2006, Nature Neuroscience.

[171]  E. Bamberg,et al.  Light Activation of Channelrhodopsin-2 in Excitable Cells of Caenorhabditis elegans Triggers Rapid Behavioral Responses , 2005, Current Biology.

[172]  Jian Wang,et al.  Transmembrane/Juxtamembrane Domain-Dependent Dscam Distribution and Function during Mushroom Body Neuronal Morphogenesis , 2004, Neuron.

[173]  Barry J. Dickson,et al.  fruitless Splicing Specifies Male Courtship Behavior in Drosophila , 2005, Cell.

[174]  L. Luo,et al.  Essential Roles of Drosophila RhoA in the Regulation of Neuroblast Proliferation and Dendritic but Not Axonal Morphogenesis , 2000, Neuron.

[175]  G. Beitel,et al.  CaSpeR5, a family of Drosophila transgenesis and shuttle vectors with improved multiple cloning sites. , 2007, BioTechniques.

[176]  C. Goodman,et al.  Targeted neuronal cell ablation in the drosophila embryo: Pathfinding by follower growth cones in the absence of pioneers , 1995, Neuron.

[177]  Stefan R. Pulver,et al.  Temporal dynamics of neuronal activation by Channelrhodopsin-2 and TRPA1 determine behavioral output in Drosophila larvae. , 2009, Journal of neurophysiology.

[178]  S. Benzer BEHAVIORAL MUTANTS OF Drosophila ISOLATED BY COUNTERCURRENT DISTRIBUTION. , 1967, Proceedings of the National Academy of Sciences of the United States of America.

[179]  D. Featherstone,et al.  Genome-wide P-element screen for Drosophila synaptogenesis mutants. , 2006, Journal of neurobiology.

[180]  Cori Bargmann,et al.  GFP Reconstitution Across Synaptic Partners (GRASP) Defines Cell Contacts and Synapses in Living Nervous Systems , 2008, Neuron.

[181]  P. Garrity,et al.  The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. , 2005, Genes & development.

[182]  S. Oehler,et al.  Minos as a Genetic and Genomic Tool in Drosophila melanogaster , 2005, Genetics.

[183]  Gero Miesenböck,et al.  Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins , 1998, Nature.

[184]  J. B. Duffy,et al.  GAL4 system in drosophila: A fly geneticist's swiss army knife , 2002, Genesis.

[185]  C. Bakal,et al.  The Twin Spot Generator for differential Drosophila lineage analysis , 2009, Nature Methods.

[186]  E. Hui,et al.  Strategies for cloning unknown cellular flanking DNA sequences from foreign integrants , 1998, Cellular and Molecular Life Sciences CMLS.

[187]  Guan-Yu Chen,et al.  Three-Dimensional Reconstruction of Brain-wide Wiring Networks in Drosophila at Single-Cell Resolution , 2011, Current Biology.

[188]  G. Rubin,et al.  Targeted mutagenesis by homologous recombination in D. melanogaster. , 2002, Genes & development.

[189]  Shigeo Hayashi,et al.  GETDB, a database compiling expression patterns and molecular locations of a collection of gal4 enhancer traps , 2002, Genesis.

[190]  Barry J. Dickson,et al.  The Drosophila pheromone cVA activates a sexually dimorphic neural circuit , 2008, Nature.

[191]  Hugo J. Bellen,et al.  100 years of Drosophila research and its impact on vertebrate neuroscience: a history lesson for the future , 2010, Nature Reviews Neuroscience.

[192]  A. Spradling,et al.  Constructing deletions with defined endpoints in Drosophila. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[193]  A. Wong,et al.  Two-Photon Calcium Imaging Reveals an Odor-Evoked Map of Activity in the Fly Brain , 2003, Cell.

[194]  W. Gelbart,et al.  Large-Scale Functional Annotation and Expanded Implementations of the P{wHy} Hybrid Transposon in the Drosophila melanogaster Genome , 2009, Genetics.

[195]  Devanand S. Manoli,et al.  Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour , 2005, Nature.

[196]  J. Gould,et al.  Inducible cell ablation in Drosophila by cold-sensitive ricin A chain. , 1992, Development.

[197]  B. Dickson Wired for Sex: The Neurobiology of Drosophila Mating Decisions , 2008, Science.

[198]  E. Marder,et al.  Development of central pattern generating circuits , 2005, Current Opinion in Neurobiology.

[199]  Feng Zhang,et al.  Nociceptive Neurons Protect Drosophila Larvae from Parasitoid Wasps , 2007, Current Biology.

[200]  J. B. Connolly,et al.  Inducible ternary control of transgene expression and cell ablation in Drosophila , 1996, Development Genes and Evolution.

[201]  Thomas C Kaufman,et al.  New research resources at the Bloomington Drosophila Stock Center , 2010, Fly.

[202]  Jie Chen,et al.  A powerful method combining homologous recombination and site-specific recombination for targeted mutagenesis in Drosophila , 2008, Proceedings of the National Academy of Sciences.

[203]  A. Sehgal,et al.  Genetic analysis of sleep. , 2010, Genes & development.

[204]  Norbert Perrimon,et al.  A Drosophila Resource of Transgenic RNAi Lines for Neurogenetics , 2009, Genetics.

[205]  H. Jäckle,et al.  Drosophila tao Controls Mushroom Body Development and Ethanol-Stimulated Behavior through par-1 , 2011, The Journal of Neuroscience.

[206]  K. Broadie,et al.  Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects , 1995, Neuron.

[207]  Hugo J. Bellen,et al.  P[acman]: A BAC Transgenic Platform for Targeted Insertion of Large DNA Fragments in D. melanogaster , 2006, Science.

[208]  A. Brand,et al.  Targeted ablation of glia disrupts axon tract formation in the Drosophila CNS. , 1995, Development.

[209]  Norbert Perrimon,et al.  A genome-scale shRNA resource for transgenic RNAi in Drosophila , 2011, Nature Methods.

[210]  N. Perrimon,et al.  Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. , 1993, Development.

[211]  T. Préat,et al.  Defining the role of Drosophila lateral neurons in the control of circadian rhythms in motor activity and eclosion by targeted genetic ablation and PERIOD protein overexpression , 2001, The European journal of neuroscience.

[212]  A. Simcox,et al.  Multiple O-glucosylation sites on Notch function as a buffer against temperature-dependent loss of signaling , 2011, Development.

[213]  N. Perrimon,et al.  Exploiting position effects and the gypsy retrovirus insulator to engineer precisely expressed transgenes , 2008, Nature Genetics.

[214]  Blocking synaptic transmission with tetanus toxin light chain reveals modes of neurotransmission in the PDF-positive circadian clock neurons of Drosophila melanogaster. , 2011, Journal of insect physiology.

[215]  Karl-Friedrich Fischbach,et al.  Optic lobe development. , 2008, Advances in experimental medicine and biology.

[216]  J. Newberg,et al.  Identification of EMS-Induced Mutations in Drosophila melanogaster by Whole-Genome Sequencing , 2009, Genetics.

[217]  B. Dickson,et al.  A receptor that mediates the post-mating switch in Drosophila reproductive behaviour , 2008, Nature.

[218]  Christopher J. Potter,et al.  A versatile in vivo system for directed dissection of gene expression patterns , 2011, Nature Methods.

[219]  Dana Carroll,et al.  Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. , 2002, Genetics.

[220]  Jeffrey C. Hall,et al.  Neuroanatomy of cells expressing clock genes in Drosophila: Transgenic manipulation of the period and timeless genes to mark the perikarya of circadian pacemaker neurons and their projections , 2000, The Journal of comparative neurology.

[221]  D. Satoh,et al.  Polarity and intracellular compartmentalization of Drosophila neurons , 2007, Neural Development.

[222]  Benjamin H. White,et al.  A conditional tissue-specific transgene expression system using inducible GAL4 , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[223]  T. Alderson Chemically Induced Delayed Germinal Mutation in Drosophila , 1965, Nature.

[224]  W. Quinn,et al.  The amnesiac Gene Product Is Expressed in Two Neurons in the Drosophila Brain that Are Critical for Memory , 2000, Cell.

[225]  R. Carthew,et al.  Use of dsRNA-Mediated Genetic Interference to Demonstrate that frizzled and frizzled 2 Act in the Wingless Pathway , 1998, Cell.

[226]  M. F. Ceriani,et al.  Neuronal death in Drosophila triggered by GAL4 accumulation , 2007, The European journal of neuroscience.

[227]  Henri Korn,et al.  Neurobiology of the Mauthner cell , 1978 .

[228]  R. Greenspan,et al.  Excitatory and Inhibitory Switches for Courtship in the Brain of Drosophila melanogaster , 2004, Current Biology.

[229]  Ian R. Wickersham,et al.  Monosynaptic Restriction of Transsynaptic Tracing from Single, Genetically Targeted Neurons , 2007, Neuron.

[230]  Ronald L. Davis,et al.  P{Switch}, a system for spatial and temporal control of gene expression in Drosophila melanogaster , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[231]  C. Alexandre,et al.  Segment boundary formation in Drosophila embryos , 2003, Development.

[232]  Stephen S. Gisselbrecht,et al.  New fluorescent protein reporters for use with the drosophila gal4 expression system and for vital detection of balancer chromosomes , 2002, Genesis.

[233]  Kristin Scott,et al.  Motor Control in a Drosophila Taste Circuit , 2009, Neuron.

[234]  G. Rubin,et al.  Analysis of genetic mosaics in developing and adult Drosophila tissues. , 1993, Development.

[235]  T. Kaufman,et al.  A New Resource for Characterizing X-Linked Genes in Drosophila melanogaster: Systematic Coverage and Subdivision of the X Chromosome With Nested, Y-Linked Duplications , 2010, Genetics.

[236]  Jeffrey C. Hall,et al.  Control of Male Sexual Behavior and Sexual Orientation in Drosophila by the fruitless Gene , 1996, Cell.

[237]  Juergen A. Knoblich,et al.  Genome-Wide Analysis of Self-Renewal in Drosophila Neural Stem Cells by Transgenic RNAi , 2011, Cell stem cell.

[238]  Shin-ya Takemura,et al.  Synaptic circuits of the Drosophila optic lobe: The input terminals to the medulla , 2008, The Journal of comparative neurology.

[239]  R. A. Bohm,et al.  A genetic mosaic approach for neural circuit mapping in Drosophila , 2010, Proceedings of the National Academy of Sciences.

[240]  K. White,et al.  Versatile P(acman) BAC Libraries for Transgenesis Studies in Drosophila melanogaster , 2009, Nature Methods.

[241]  B. Dickson,et al.  High-resolution, high-throughput SNP mapping in Drosophila melanogaster , 2008, Nature Methods.

[242]  H. Steller,et al.  Ablation of Drosophila photoreceptor cells by conditional expression of a toxin gene. , 1991, Genes & development.

[243]  H. Bellen,et al.  The Arp2/3 complex and WASp are required for apical trafficking of Delta into microvilli during cell fate specification of sensory organ precursors , 2009, Nature Cell Biology.

[244]  Michael N Nitabach,et al.  Electrical Silencing of Drosophila Pacemaker Neurons Stops the Free-Running Circadian Clock , 2002, Cell.

[245]  Karel Svoboda,et al.  From cudgel to scalpel: toward precise neural control with optogenetics , 2011, Nature Methods.

[246]  Matthias Landgraf,et al.  Genetically encoded dendritic marker sheds light on neuronal connectivity in Drosophila , 2010, Proceedings of the National Academy of Sciences.

[247]  A. Fiala,et al.  Genetically Expressed Cameleon in Drosophila melanogaster Is Used to Visualize Olfactory Information in Projection Neurons , 2002, Current Biology.

[248]  L. Luo,et al.  Using the Q system in Drosophila melanogaster , 2011, Nature Protocols.

[249]  M. Nitabach,et al.  Electrical Hyperexcitation of Lateral Ventral Pacemaker Neurons Desynchronizes Downstream Circadian Oscillators in the Fly Circadian Circuit and Induces Multiple Behavioral Periods , 2006, The Journal of Neuroscience.

[250]  R. Maeda,et al.  An optimized transgenesis system for Drosophila using germ-line-specific φC31 integrases , 2007, Proceedings of the National Academy of Sciences.

[251]  Y. Sharma,et al.  PPTGAL, a convenient Gal4 P‐element vector for testing expression of enhancer fragments in drosophila , 2002, Genesis.

[252]  Decision Making: Singin' in the Brain , 2011, Neuron.

[253]  R. Carthew,et al.  Heritable gene silencing in Drosophila using double-stranded RNA , 2000, Nature Biotechnology.

[254]  Y. Jan,et al.  Growing Dendrites and Axons Differ in Their Reliance on the Secretory Pathway , 2007, Cell.

[255]  Roger A Hoskins,et al.  The Carnegie Protein Trap Library: A Versatile Tool for Drosophila Developmental Studies , 2007, Genetics.

[256]  S. Rao,et al.  Visualization of neuropeptide expression, transport, and exocytosis in Drosophila melanogaster. , 2001, Journal of neurobiology.

[257]  David J. Anderson,et al.  Light Activation of an Innate Olfactory Avoidance Response in Drosophila , 2007, Current Biology.

[258]  Walther Akemann,et al.  Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins , 2010, Nature Methods.

[259]  Feng Chen,et al.  A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac , 2004, Nature Genetics.

[260]  Raghavan Varadarajan,et al.  Design and isolation of temperature-sensitive mutants of Gal4 in yeast and Drosophila. , 2007, Journal of molecular biology.

[261]  W. Gelbart,et al.  Research resources for Drosophila: the expanding universe , 2005, Nature Reviews Genetics.

[262]  Jay Hirsh,et al.  Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. , 2003, Journal of neurobiology.

[263]  Kristin Scott,et al.  Imaging Taste Responses in the Fly Brain Reveals a Functional Map of Taste Category and Behavior , 2006, Neuron.

[264]  G. Boulianne,et al.  Green fluorescent protein as a vital marker and reporter of gene expression in Drosophila. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[265]  G. Nagel,et al.  Light-Induced Activation of Distinct Modulatory Neurons Triggers Appetitive or Aversive Learning in Drosophila Larvae , 2006, Current Biology.

[266]  Michael Bate,et al.  Altered Electrical Properties in DrosophilaNeurons Developing without Synaptic Transmission , 2001, The Journal of Neuroscience.

[267]  S. Tsunoda,et al.  Shal/Kv4 Channels Are Required for Maintaining Excitability during Repetitive Firing and Normal Locomotion in Drosophila , 2011, PloS one.

[268]  Julie H. Simpson,et al.  Mapping and manipulating neural circuits in the fly brain. , 2009, Advances in genetics.

[269]  Kei Ito,et al.  Neural architecture of the primary gustatory center of Drosophila melanogaster visualized with GAL4 and LexA enhancer‐trap systems , 2010, The Journal of comparative neurology.

[270]  J. Levine,et al.  Specialized cells tag sexual and species identity in Drosophila melanogaster , 2009, Nature.

[271]  Sebastian Rumpf,et al.  Control of the Postmating Behavioral Switch in Drosophila Females by Internal Sensory Neurons , 2009, Neuron.

[272]  Salil S. Bidaye,et al.  Neuronal Control of Drosophila Courtship Song , 2011, Neuron.

[273]  Benjamin H White,et al.  Dissection of synaptic excitability phenotypes by using a dominant-negative Shaker K+ channel subunit. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[274]  Botond Roska,et al.  Tuning FlaSh: redesign of the dynamics, voltage range, and color of the genetically encoded optical sensor of membrane potential. , 2002, Biophysical journal.

[275]  Jai Y. Yu,et al.  Cellular Organization of the Neural Circuit that Drives Drosophila Courtship Behavior , 2010, Current Biology.

[276]  Y. Jan,et al.  dunce, a mutant of Drosophila deficient in learning. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[277]  W. Gehring,et al.  Spatial and temporal targeting of gene expression in Drosophila by means of a tetracycline-dependent transactivator system. , 1998, Development.

[278]  Wei Dong,et al.  Directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering , 2009, Proceedings of the National Academy of Sciences.

[279]  Alexander Borst,et al.  Fluorescence Changes of Genetic Calcium Indicators and OGB-1 Correlated with Neural Activity and Calcium In Vivo and In Vitro , 2008, The Journal of Neuroscience.

[280]  Devanand S. Manoli,et al.  Median bundle neurons coordinate behaviours during Drosophila male courtship , 2004, Nature.

[281]  H. Bellen,et al.  Emerging technologies for gene manipulation in Drosophila melanogaster , 2005, Nature Reviews Genetics.

[282]  Jai Y. Yu,et al.  Sexual Dimorphism in the Fly Brain , 2010, Current Biology.

[283]  G. Rubin,et al.  Refinement of Tools for Targeted Gene Expression in Drosophila , 2010, Genetics.

[284]  J. Douglas Armstrong,et al.  BrainTrap: a database of 3D protein expression patterns in the Drosophila brain , 2010, Database J. Biol. Databases Curation.

[285]  G. Cao,et al.  Phase Coupling of a Circadian Neuropeptide With Rest/Activity Rhythms Detected Using a Membrane-Tethered Spider Toxin , 2008, PLoS biology.

[286]  E. Kravitz,et al.  Targeted Manipulation of Serotonergic Neurotransmission Affects the Escalation of Aggression in Adult Male Drosophila melanogaster , 2010, PloS one.

[287]  T. Holmes,et al.  Pigment Dispersing Factor-Dependent and -Independent Circadian Locomotor Behavioral Rhythms , 2008, The Journal of Neuroscience.

[288]  B. Dickson,et al.  Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. , 2000, Development.

[289]  M. Nitabach,et al.  Functional Dissection of a Neuronal Network Required for Cuticle Tanning and Wing Expansion in Drosophila , 2006, The Journal of Neuroscience.

[290]  Hongkui Zeng,et al.  A Drosophila circadian clock. , 1996, Cold Spring Harbor symposia on quantitative biology.

[291]  Wei Zhang,et al.  A toolbox for light control of Drosophila behaviors through Channelrhodopsin 2‐mediated photoactivation of targeted neurons , 2007, The European journal of neuroscience.

[292]  F. Kawasaki,et al.  Active Zone Localization of Presynaptic Calcium Channels Encoded by the cacophony Locus of Drosophila , 2004, The Journal of Neuroscience.

[293]  Aaron DiAntonio,et al.  Synaptic Development: Insights from Drosophila This Review Comes from a Themed Issue on Development Edited Synapse Development Live Imaging of Glutamate Receptor Clustering Synaptic Terminal Development Synaptic Terminal Stability , 2022 .

[294]  G. Miesenböck,et al.  Sex-Specific Control and Tuning of the Pattern Generator for Courtship Song in Drosophila , 2008, Cell.

[295]  D. Kretzschmar,et al.  A Gateway MultiSite Recombination Cloning Toolkit , 2011, PloS one.

[296]  V. Ambros,et al.  Drosophila let-7 microRNA is required for remodeling of the neuromusculature during metamorphosis. , 2008, Genes & development.

[297]  C. Cirelli Searching for sleep mutants of Drosophila melanogaster. , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

[298]  H. Tanimoto,et al.  Cellular configuration of single octopamine neurons in Drosophila , 2010, The Journal of comparative neurology.

[299]  J. Ewer,et al.  Construction and Characterization of Deletions With Defined End Points in Drosophila Using P Elements in Trans , 2009, Genetics.

[300]  D. Hartl,et al.  Transgene Coplacement and high efficiency site-specific recombination with the Cre/loxP system in Drosophila. , 1996, Genetics.

[301]  K. Vranizan,et al.  Ethanol-regulated genes that contribute to ethanol sensitivity and rapid tolerance in Drosophila. , 2010, Alcoholism, clinical and experimental research.

[302]  J. Truman,et al.  Light and peptidergic eclosion hormone neurons stimulate a rapid eclosion response that masks circadian emergence in Drosophila , 2008, Journal of Experimental Biology.

[303]  J. Kramer,et al.  GAL4 causes developmental defects and apoptosis when expressed in the developing eye of Drosophila melanogaster. , 2003, Genetics and molecular research : GMR.

[304]  Alexander Borst,et al.  Candidate Glutamatergic Neurons in the Visual System of Drosophila , 2011, PloS one.

[305]  G. Miesenböck,et al.  Rational Optimization and Imaging In Vivo of a Genetically Encoded Optical Voltage Reporter , 2008, The Journal of Neuroscience.

[306]  A. Sehgal,et al.  Identification of SLEEPLESS, a Sleep-Promoting Factor , 2008, Science.

[307]  Y. Rong,et al.  The past, present and future of gene targeting in Drosophila , 2010, Fly.

[308]  E. Wimmer,et al.  piggyBac-based insertional mutagenesis in the presence of stably integrated P elements in Drosophila , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[309]  M. Suster,et al.  Refining GAL4‐driven transgene expression in Drosophila with a GAL80 enhancer‐trap , 2004, Genesis.

[310]  M. Porteus,et al.  Mammalian gene targeting with designed zinc finger nucleases. , 2006, Molecular therapy : the journal of the American Society of Gene Therapy.

[311]  James C. Choi,et al.  Shaw potassium channel genes in Drosophila. , 2005, Journal of neurobiology.

[312]  M. Ashburner,et al.  The DrosDel Collection , 2004, Genetics.

[313]  Konrad Basler,et al.  Organizing activity of wingless protein in Drosophila , 1993, Cell.

[314]  N. Nassif,et al.  Targeted gene replacement in Drosophila via P element-induced gap repair , 1991, Science.

[315]  T. Kitamoto Conditional disruption of synaptic transmission induces male–male courtship behavior in Drosophila , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[316]  W. Gehring,et al.  Detection in situ of genomic regulatory elements in Drosophila. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[317]  I. Meinertzhagen The organisation of invertebrate brains: cells, synapses and circuits , 2010 .

[318]  Haojiang Luan,et al.  Combinatorial methods for refined neuronal gene targeting , 2007, Current Opinion in Neurobiology.

[319]  Bassem A. Hassan,et al.  Recombineering-mediated tagging of Drosophila genomic constructs for in vivo localization and acute protein inactivation , 2008, Nucleic acids research.

[320]  J. Gall,et al.  Efficient gene targeting in Drosophila by direct embryo injection with zinc-finger nucleases , 2008, Proceedings of the National Academy of Sciences.

[321]  M. Koganezawa,et al.  The Shaping of Male Courtship Posture by Lateralized Gustatory Inputs to Male-Specific Interneurons , 2010, Current Biology.

[322]  James W Truman,et al.  Disruption of a Behavioral Sequence by Targeted Death of Peptidergic Neurons in Drosophila , 1997, Neuron.

[323]  Stephan J. Sigrist,et al.  Bruchpilot, a Protein with Homology to ELKS/CAST, Is Required for Structural Integrity and Function of Synaptic Active Zones in Drosophila , 2006, Neuron.

[324]  Andreas Hess,et al.  A Genome-wide Drosophila Screen for Heat Nociception Identifies α2δ3 as an Evolutionarily Conserved Pain Gene , 2010, Cell.

[325]  A. Dornan,et al.  GAL4 enhancer trap targeting of the Drosophila sex determination gene fruitless , 2005, Genesis.

[326]  Hitoshi Sakano,et al.  Topographic mapping--the olfactory system. , 2010, Cold Spring Harbor perspectives in biology.

[327]  M. Ramaswami,et al.  Probable mechanisms underlying interallelic complementation and temperature-sensitivity of mutations at the shibire locus of Drosophila melanogaster. , 1998, Genetics.

[328]  M. Bibikova,et al.  Efficient Gene Targeting in Drosophila With Zinc-Finger Nucleases , 2006, Genetics.

[329]  P. Verstreken,et al.  Huntingtin-interacting protein 14, a palmitoyl transferase required for exocytosis and targeting of CSP to synaptic vesicles , 2007, The Journal of cell biology.

[330]  K. Fischbach,et al.  The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure , 1989, Cell and Tissue Research.

[331]  Sreekanth H. Chalasani,et al.  Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators , 2009, Nature Methods.

[332]  Juan Huang,et al.  Successive and Targeted DNA Integrations in the Drosophila Genome by Bxb1 and φC31 Integrases , 2011, Genetics.

[333]  E. Bamberg,et al.  Ultra light-sensitive and fast neuronal activation with the Ca2+-permeable channelrhodopsin CatCh , 2011, Nature Neuroscience.

[334]  Dana Carroll,et al.  Enhancing Gene Targeting with Designed Zinc Finger Nucleases , 2003, Science.

[335]  L. Stevens,et al.  Investigating the function of follicular subpopulations during Drosophila oogenesis through hormone-dependent enhancer-targeted cell ablation. , 2000, Development.

[336]  Susana Q. Lima,et al.  Remote Control of Behavior through Genetically Targeted Photostimulation of Neurons , 2005, Cell.

[337]  Sunil Q. Mehta,et al.  Sec15, a component of the exocyst, promotes notch signaling during the asymmetric division of Drosophila sensory organ precursors. , 2005, Developmental cell.

[338]  Benjamin H. White,et al.  Focusing Transgene Expression in Drosophila by Coupling Gal4 With a Novel Split-LexA Expression System , 2011, Genetics.

[339]  Julie H. Simpson,et al.  Drosophila Brainbow: a recombinase-based fluorescent labeling technique to subdivide neural expression patterns , 2011, Nature Methods.

[340]  Tzumin Lee,et al.  Endodomain Diversity in the Drosophila Dscam and Its Roles in Neuronal Morphogenesis , 2009, The Journal of Neuroscience.

[341]  T. Wardill,et al.  Overexpressing Temperature-Sensitive Dynamin Decelerates Phototransduction and Bundles Microtubules in Drosophila Photoreceptors , 2009, The Journal of Neuroscience.

[342]  B. Dickson,et al.  A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila , 2007, Nature.

[343]  P. Tomançak,et al.  In Vivo RNAi Rescue in Drosophila melanogaster with Genomic Transgenes from Drosophila pseudoobscura , 2010, PloS one.

[344]  Liang Liang,et al.  The Q System: A Repressible Binary System for Transgene Expression, Lineage Tracing, and Mosaic Analysis , 2010, Cell.

[345]  D. Dacey,et al.  Colour coding in the primate retina: diverse cell types and cone-specific circuitry , 2003, Current Opinion in Neurobiology.

[346]  Kathryn L. Pepple,et al.  Two-step selection of a single R8 photoreceptor: a bistable loop between senseless and rough locks in R8 fate , 2008, Development.

[347]  M. Ramaswami,et al.  Synaptic Localization and Restricted Diffusion of a Drosophila Neuronal Synaptobrevin - Green Fluorescent Protein Chimera in Vivo , 2000, Journal of neurogenetics.

[348]  H. Bellen,et al.  Ero1L, a thiol oxidase, is required for Notch signaling through cysteine bridge formation of the Lin12-Notch repeats in Drosophila melanogaster , 2008, The Journal of cell biology.

[349]  K. Deisseroth,et al.  Millisecond-timescale, genetically targeted optical control of neural activity , 2005, Nature Neuroscience.

[350]  Michael A. Henninger,et al.  High-Performance Genetically Targetable Optical Neural Silencing via Light-Driven Proton Pumps , 2010 .

[351]  Lei Zhou,et al.  Cooperative functions of the reaper and head involution defective genes in the programmed cell death of Drosophila central nervous system midline cells. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[352]  Matthias Landgraf,et al.  Structural Homeostasis: Compensatory Adjustments of Dendritic Arbor Geometry in Response to Variations of Synaptic Input , 2008, PLoS biology.

[353]  D. Kvitsiani,et al.  Neural Circuitry that Governs Drosophila Male Courtship Behavior , 2005, Cell.

[354]  G. Rubin,et al.  The BDGP Gene Disruption Project , 2004, Genetics.

[355]  W. Hillen,et al.  Tetracycline-inducible systems for Drosophila , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[356]  G. Rubin,et al.  Tools for neuroanatomy and neurogenetics in Drosophila , 2008, Proceedings of the National Academy of Sciences.

[357]  S. Elledge,et al.  Isolation of temperature-sensitive diphtheria toxins in yeast and their effects on Drosophila cells. , 1992, Development.

[358]  A. Bejsovec,et al.  Directionality of wingless protein transport influences epidermal patterning in the Drosophila embryo. , 1999, Development.

[359]  Ronald L. Davis,et al.  Spatiotemporal Rescue of Memory Dysfunction in Drosophila , 2003, Science.

[360]  Erik T. Bieschke,et al.  Doxycycline-induced transgene expression during Drosophila development and aging , 1998, Molecular and General Genetics MGG.

[361]  R. Maeda,et al.  Initiator Elements Function to Determine the Activity State of BX-C Enhancers , 2010, PLoS genetics.

[362]  A. Brand,et al.  Targeted neuronal ablation: the role of pioneer neurons in guidance and fasciculation in the CNS of Drosophila. , 1997, Development.

[363]  Ronald L. Davis,et al.  Spatial and Temporal Control of Gene Expression in Drosophila Using the Inducible GeneSwitch GAL4 System. I. Screen for Larval Nervous System Drivers , 2008, Genetics.

[364]  Y. Jan,et al.  Efficient Ends-Out Gene Targeting In Drosophila , 2008, Genetics.

[365]  Daniel St Johnston,et al.  The art and design of genetic screens: Drosophila melanogaster , 2002, Nature Reviews Genetics.

[366]  A. Borst,et al.  A genetically encoded calcium indicator for chronic in vivo two-photon imaging , 2008, Nature Methods.