Neuroarchitecture of Aminergic Systems in the Larval Ventral Ganglion of Drosophila melanogaster

Biogenic amines are important signaling molecules in the central nervous system of both vertebrates and invertebrates. In the fruit fly Drosophila melanogaster, biogenic amines take part in the regulation of various vital physiological processes such as feeding, learning/memory, locomotion, sexual behavior, and sleep/arousal. Consequently, several morphological studies have analyzed the distribution of aminergic neurons in the CNS. Previous descriptions, however, did not determine the exact spatial location of aminergic neurite arborizations within the neuropil. The release sites and pre-/postsynaptic compartments of aminergic neurons also remained largely unidentified. We here used gal4-driven marker gene expression and immunocytochemistry to map presumed serotonergic (5-HT), dopaminergic, and tyraminergic/octopaminergic neurons in the thoracic and abdominal neuromeres of the Drosophila larval ventral ganglion relying on Fasciclin2-immunoreactive tracts as three-dimensional landmarks. With tyrosine hydroxylase- (TH) or tyrosine decarboxylase 2 (TDC2)-specific gal4-drivers, we also analyzed the distribution of ectopically expressed neuronal compartment markers in presumptive dopaminergic TH and tyraminergic/octopaminergic TDC2 neurons, respectively. Our results suggest that thoracic and abdominal 5-HT and TH neurons are exclusively interneurons whereas most TDC2 neurons are efferent. 5-HT and TH neurons are ideally positioned to integrate sensory information and to modulate neuronal transmission within the ventral ganglion, while most TDC2 neurons appear to act peripherally. In contrast to 5-HT neurons, TH and TDC2 neurons each comprise morphologically different neuron subsets with separated in- and output compartments in specific neuropil regions. The three-dimensional mapping of aminergic neurons now facilitates the identification of neuronal network contacts and co-localized signaling molecules, as exemplified for DOPA decarboxylase-synthesizing neurons that co-express crustacean cardioactive peptide and myoinhibiting peptides.

[1]  R. Hodgetts,et al.  A neuropeptide hormone cascade controls the precise onset of post-eclosion cuticular tanning in Drosophila melanogaster , 2007, Development.

[2]  S. Goodwin,et al.  Compartmentalization of neuronal and peripheral serotonin synthesis in Drosophila melanogaster , 2007, Genes, brain, and behavior.

[3]  B. Brembs,et al.  Flight Initiation and Maintenance Deficits in Flies with Genetically Altered Biogenic Amine Levels , 2007, The Journal of Neuroscience.

[4]  J. Hirsh,et al.  Trace amines differentially regulate adult locomotor activity, cocaine sensitivity, and female fertility in Drosophila melanogaster , 2007, Developmental neurobiology.

[5]  C. Carr,et al.  Tag team action at the synapse , 2007, EMBO reports.

[6]  J. Dolly,et al.  Synaptobrevin I mediates exocytosis of CGRP from sensory neurons and inhibition by botulinum toxins reflects their anti-nociceptive potential , 2007, Journal of Cell Science.

[7]  U. Homberg,et al.  Neuroarchitecture of Peptidergic Systems in the Larval Ventral Ganglion of Drosophila melanogaster , 2007, PloS one.

[8]  M. Adams,et al.  Complex steroid-peptide-receptor cascade controls insect ecdysis. , 2007, General and comparative endocrinology.

[9]  M. Pankratz,et al.  Comparative Neuroanatomy and Genomics of hugin and Pheromone Biosynthesis Activating Neuropeptide (PBAN) , 2007, Fly.

[10]  Sonja M. Wojcik,et al.  Regulation of Membrane Fusion in Synaptic Excitation-Secretion Coupling: Speed and Accuracy Matter , 2007, Neuron.

[11]  Yueqing Peng,et al.  Dopamine-Mushroom Body Circuit Regulates Saliency-Based Decision-Making in Drosophila , 2007, Science.

[12]  Alexander Borst,et al.  Synaptic organization of lobula plate tangential cells in Drosophila: γ‐Aminobutyric acid receptors and chemical release sites , 2007, The Journal of comparative neurology.

[13]  A. A. Alekseev,et al.  Dopamine and octopamine regulate 20-hydroxyecdysone level in vivo in Drosophila. , 2007, Archives of insect biochemistry and physiology.

[14]  T. Farooqui Octopamine-Mediated Neuromodulation of Insect Senses , 2007, Neurochemical Research.

[15]  C. Nichols 5‐HT2 receptors in Drosophila are expressed in the brain and modulate aspects of circadian behaviors , 2007, Developmental neurobiology.

[16]  C. Wegener,et al.  Neurotransmitter‐induced changes in the intracellular calcium concentration suggest a differential central modulation of CCAP neuron subsets in Drosophila , 2007, Developmental neurobiology.

[17]  Peri T Kurshan,et al.  Locomotor activity is regulated by D2‐like receptors in Drosophila: An anatomic and functional analysis , 2007, Developmental neurobiology.

[18]  Daniel Karlsson,et al.  Specification of Neuronal Identities by Feedforward Combinatorial Coding , 2007, PLoS biology.

[19]  R. Predel,et al.  Peptidomics of identified neurons demonstrates a highly differentiated expression pattern of FXPRLamides in the neuroendocrine system of an insect , 2007, The Journal of comparative neurology.

[20]  J. Veenstra,et al.  The neuropeptide SIFamide modulates sexual behavior in Drosophila. , 2007, Biochemical and biophysical research communications.

[21]  Chung-Hui Yang,et al.  Projections of Drosophila multidendritic neurons in the central nervous system: links with peripheral dendrite morphology , 2007, Development.

[22]  H. Atwood,et al.  Modular neuropile organization in the Drosophila larval brain facilitates identification and mapping of central neurons , 2006, The Journal of comparative neurology.

[23]  M. O'Donnell,et al.  Changes in fluid secretion rate alter net transepithelial transport of MRP2 and P-glycoprotein substrates in Malpighian tubules of Drosophila melanogaster. , 2006, Archives of insect biochemistry and physiology.

[24]  Paul J Shaw,et al.  Waking Experience Affects Sleep Need in Drosophila , 2006, Science.

[25]  K. White,et al.  Sex-Peptide-Regulated Female Sexual Behavior Requires a Subset of Ascending Ventral Nerve Cord Neurons , 2006, Current Biology.

[26]  F. Hauser,et al.  A review of neurohormone GPCRs present in the fruitfly Drosophila melanogaster and the honey bee Apis mellifera , 2006, Progress in Neurobiology.

[27]  V. Hartenstein The neuroendocrine system of invertebrates: a developmental and evolutionary perspective. , 2006, The Journal of endocrinology.

[28]  Kei Ito,et al.  Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula‐specific pathways , 2006, The Journal of comparative neurology.

[29]  M. Adams,et al.  A Command Chemical Triggers an Innate Behavior by Sequential Activation of Multiple Peptidergic Ensembles , 2006, Current Biology.

[30]  C. Elliott,et al.  Neuromuscular organization and aminergic modulation of contractions in the Drosophila ovary , 2006, BMC Biology.

[31]  U. Homberg,et al.  Neuropeptides in interneurons of the insect brain , 2006, Cell and Tissue Research.

[32]  Quan Yuan,et al.  A Sleep-Promoting Role for the Drosophila Serotonin Receptor 1A , 2006, Current Biology.

[33]  K. Rexer,et al.  Morphology and metamorphosis of the peptidergic Va neurons and the median nerve system of the fruit fly, Drosophila melanogaster , 2006, Cell and Tissue Research.

[34]  Robin L. Cooper,et al.  Direct influence of serotonin on the larval heart of Drosophila melanogaster , 2006, Journal of Comparative Physiology B.

[35]  M. Pankratz,et al.  Neuromedin U and Its Putative Drosophila Homolog hugin , 2006, PLoS biology.

[36]  R. Predel,et al.  Direct mass spectrometric peptide profiling and fragmentation of larval peptide hormone release sites in Drosophila melanogaster reveals tagma‐specific peptide expression and differential processing , 2006, Journal of neurochemistry.

[37]  Á. Acebes,et al.  Tachykinin-related peptides modulate odor perception and locomotor activity in Drosophila , 2006, Molecular and Cellular Neuroscience.

[38]  M. Landgraf,et al.  Development of Drosophila motoneurons: specification and morphology. , 2006, Seminars in cell & developmental biology.

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

[40]  Y. Hamasaka,et al.  Mapping of serotonin, dopamine, and histamine in relation to different clock neurons in the brain of Drosophila , 2006, The Journal of comparative neurology.

[41]  Y. Hamasaka,et al.  Chronobiological analysis and mass spectrometric characterization of pigment-dispersing factor in the cockroach Leucophaea maderae , 2005, Journal of insect science.

[42]  Y. Hamasaka,et al.  GABA modulates Drosophila circadian clock neurons via GABAB receptors and decreases in calcium. , 2005, Journal of neurobiology.

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

[44]  E. M. Blumenthal Modulation of tyramine signaling by osmolality in an insect secretory epithelium. , 2005, American journal of physiology. Cell physiology.

[45]  J. Ewer Behavioral actions of neuropeptides in invertebrates: Insights from Drosophila , 2005, Hormones and Behavior.

[46]  E. Bae,et al.  Drosophila GPCR Han Is a Receptor for the Circadian Clock Neuropeptide PDF , 2005, Neuron.

[47]  P. Taghert,et al.  PDF Receptor Signaling in Drosophila Contributes to Both Circadian and Geotactic Behaviors , 2005, Neuron.

[48]  P. Evans,et al.  Insect octopamine receptors: a new classification scheme based on studies of cloned Drosophila G-protein coupled receptors , 2005, Invertebrate Neuroscience.

[49]  B. Condron,et al.  Development and sensitivity to serotonin of Drosophila serotonergic varicosities in the central nervous system. , 2005, Developmental biology.

[50]  Hui-yun Chang,et al.  A splice variant of the Drosophila vesicular monoamine transporter contains a conserved trafficking domain and functions in the storage of dopamine, serotonin, and octopamine. , 2005, Journal of neurobiology.

[51]  R. Levine,et al.  Role of the neuropeptide CCAP in Drosophila cardiac function. , 2005, Journal of neurobiology.

[52]  M. Pankratz,et al.  Candidate Gustatory Interneurons Modulating Feeding Behavior in the Drosophila Brain , 2005, PLoS biology.

[53]  Sang Ki Park,et al.  Dopamine Is a Regulator of Arousal in the Fruit Fly , 2005, The Journal of Neuroscience.

[54]  R. Pendleton,et al.  A developmental role for catecholamines in Drosophila behavior , 2005, Pharmacology Biochemistry and Behavior.

[55]  R. Greenspan,et al.  Dopaminergic Modulation of Arousal in Drosophila , 2005, Current Biology.

[56]  Xiangzhong Zheng,et al.  Serotonin Modulates Circadian Entrainment in Drosophila , 2005, Neuron.

[57]  H. Pflüger,et al.  Evolutionary aspects of octopaminergic systems with emphasis on arthropods. , 2005 .

[58]  J. Mustard,et al.  Molecular biology of the invertebrate dopamine receptors. , 2005, Archives of insect biochemistry and physiology.

[59]  P. Evans,et al.  Rapid, Nongenomic Responses to Ecdysteroids and Catecholamines Mediated by a Novel Drosophila G-Protein-Coupled Receptor , 2005, The Journal of Neuroscience.

[60]  W. Neckameyer,et al.  Stress affects dopaminergic signaling pathways in Drosophila melanogaster , 2005, Stress.

[61]  W. Neckameyer,et al.  Serotonin synthesis by two distinct enzymes in Drosophila melanogaster. , 2005, Archives of insect biochemistry and physiology.

[62]  J. Hirsh,et al.  Two Functional but Noncomplementing Drosophila Tyrosine Decarboxylase Genes , 2005, Journal of Biological Chemistry.

[63]  P. Taghert,et al.  A novel diuretic hormone receptor in Drosophila: evidence for conservation of CGRP signaling , 2005, Journal of Experimental Biology.

[64]  J. C. Hall,et al.  Comparative analysis of Corazonin‐encoding genes (Crz's) in Drosophila species and functional insights into Crz‐expressing neurons , 2005, The Journal of comparative neurology.

[65]  Liliane Schoofs,et al.  Peptidomic analysis of the larval Drosophila melanogaster central nervous system by two-dimensional capillary liquid chromatography quadrupole time-of-flight mass spectrometry. , 2005, Journal of mass spectrometry : JMS.

[66]  G. Rutter,et al.  Mechanisms of Dense Core Vesicle Recapture following “Kiss and Run” (“Cavicapture”) Exocytosis in Insulin-secreting Cells* , 2004, Journal of Biological Chemistry.

[67]  W. Neckameyer,et al.  Substrate regulation of serotonin and dopamine synthesis in Drosophila , 2004, Invertebrate Neuroscience.

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

[69]  Yueqing Peng,et al.  Long‐term but not short‐term blockade of dopamine release in Drosophila impairs orientation during flight in a visual attention paradigm , 2004, The European journal of neuroscience.

[70]  Liliane Schoofs,et al.  SIFamide is a highly conserved neuropeptide: a comparative study in different insect species. , 2004, Biochemical and biophysical research communications.

[71]  J. Littleton,et al.  Synaptotagmins are trafficked to distinct subcellular domains including the postsynaptic compartment , 2004, The Journal of cell biology.

[72]  Christian Wegener,et al.  Peptidomics of CNS‐associated neurohemal systems of adult Drosophila melanogaster: A mass spectrometric survey of peptides from individual flies , 2004, The Journal of comparative neurology.

[73]  J. Ewer,et al.  Use of targetable gfp-tagged neuropeptide for visualizing neuropeptide release following execution of a behavior. , 2004, Journal of neurobiology.

[74]  M. Adams,et al.  Corazonin receptor signaling in ecdysis initiation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[75]  David R Soll,et al.  Tyramine and octopamine have opposite effects on the locomotion of Drosophila larvae. , 2004, Journal of neurobiology.

[76]  S. Baraban,et al.  Interneuron Diversity series: Interneuronal neuropeptides – endogenous regulators of neuronal excitability , 2004, Trends in Neurosciences.

[77]  D. Nässel,et al.  Identification of a proctolin preprohormone gene (Proct) of Drosophila melanogaster: expression and predicted prohormone processing. , 2004, Journal of neurobiology.

[78]  Y. Hamasaka,et al.  Acetylcholine increases intracellular Ca2+ via nicotinic receptors in cultured PDF-containing clock neurons of Drosophila. , 2004, Journal of neurophysiology.

[79]  L. Schoofs,et al.  Expression of a novel neuropeptide, NVGTLARDFQLPIPNamide, in the larval and adult brain of Drosophila melanogaster , 2003, Journal of neurochemistry.

[80]  Ronald L. Davis,et al.  Octopamine receptor OAMB is required for ovulation in Drosophila melanogaster. , 2003, Developmental biology.

[81]  M. Monastirioti Distinct octopamine cell population residing in the CNS abdominal ganglion controls ovulation in Drosophila melanogaster. , 2003, Developmental biology.

[82]  M. Heisenberg,et al.  Dopamine and Octopamine Differentiate between Aversive and Appetitive Olfactory Memories in Drosophila , 2003, The Journal of Neuroscience.

[83]  Kei Ito,et al.  Cautionary observations on preparing and interpreting brain images using molecular biology‐based staining techniques , 2003, Microscopy research and technique.

[84]  D. Nässel,et al.  Neuronal expression of tachykinin‐related peptides and gene transcript during postembryonic development of Drosophila , 2003, The Journal of comparative neurology.

[85]  T. Roeder,et al.  Tyramine and octopamine: antagonistic modulators of behavior and metabolism. , 2003, Archives of insect biochemistry and physiology.

[86]  H. Nijhout The control of body size in insects. , 2003, Developmental biology.

[87]  Matthias Landgraf,et al.  Charting the Drosophila neuropile: a strategy for the standardised characterisation of genetically amenable neurites. , 2003, Developmental biology.

[88]  T. Wen,et al.  Developmental Control of Foraging and Social Behavior by the Drosophila Neuropeptide Y-like System , 2003, Neuron.

[89]  C. Helfrich-Förster,et al.  Targeted ablation of CCAP neuropeptide-containing neurons of Drosophila causes specific defects in execution and circadian timing of ecdysis behavior , 2003, Development.

[90]  J. Littleton,et al.  Is synaptotagmin the calcium sensor? , 2003, Current Opinion in Neurobiology.

[91]  D. O'Dowd,et al.  GABA Receptors Containing Rdl Subunits Mediate Fast Inhibitory Synaptic Transmission in Drosophila Neurons , 2003, The Journal of Neuroscience.

[92]  K. Han,et al.  Expression of a D1 dopamine receptor dDA1/DmDOP1 in the central nervous system of Drosophila melanogaster. , 2003, Gene expression patterns : GEP.

[93]  P. Taghert,et al.  The bHLH protein Dimmed controls neuroendocrine cell differentiation in Drosophila , 2003, Development.

[94]  M. Suster,et al.  Targeted expression of tetanus toxin reveals sets of neurons involved in larval locomotion in Drosophila. , 2003, Journal of neurobiology.

[95]  Susan E. St. Pierre,et al.  Specification of Neuropeptide Cell Identity by the Integration of Retrograde BMP Signaling and a Combinatorial Transcription Factor Code , 2003, Cell.

[96]  E. M. Blumenthal Regulation of chloride permeability by endogenously produced tyramine in the Drosophila Malpighian tubule. , 2003, American journal of physiology. Cell physiology.

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

[98]  Florence Friggi-Grelin,et al.  Tissue‐specific developmental requirements of Drosophila tyrosine hydroxylase isoforms , 2003, Genesis.

[99]  Brian Mulloney,et al.  Architectonics of crayfish ganglia , 2003, Microscopy research and technique.

[100]  Matthias Landgraf,et al.  Genetic Specification of Axonal Arbors atonal Regulates robo3 to Position Terminal Branches in the Drosophila Nervous System , 2003, Neuron.

[101]  J. Littleton,et al.  Synaptotagmin I Functions as a Calcium Sensor to Synchronize Neurotransmitter Release , 2002, Neuron.

[102]  T. Godenschwege,et al.  Compartmentalization of Central Neurons inDrosophila: A New Strategy of Mosaic Analysis Reveals Localization of Presynaptic Sites to Specific Segments of Neurites , 2002, The Journal of Neuroscience.

[103]  R. Predel,et al.  Identical cellular distribution of all abundant neuropeptides in the major abdominal neurohemal system of an insect (Periplaneta Americana) , 2002, The Journal of comparative neurology.

[104]  A. Komatsu,et al.  A trace amine, tyramine, functions as a neuromodulator in Drosophila melanogaster , 2002, Neuroscience Letters.

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

[106]  H. Sariola,et al.  The Drosophila hugin gene codes for myostimulatory and ecdysis-modifying neuropeptides , 2002, Mechanisms of Development.

[107]  D. Nässel Neuropeptides in the nervous system of Drosophila and other insects: multiple roles as neuromodulators and neurohormones , 2002, Progress in Neurobiology.

[108]  Yuh Nung Jan,et al.  Tiling of the Drosophila epidermis by multidendritic sensory neurons. , 2002, Development.

[109]  J. Veenstra,et al.  Two nitridergic peptides are encoded by the gene capability in Drosophila melanogaster. , 2002, American journal of physiology. Regulatory, integrative and comparative physiology.

[110]  Arnold De Loof,et al.  Insulin-related peptides and their conserved signal transduction pathway , 2002, Peptides.

[111]  T. Tully,et al.  Effects of Tyrosine Hydroxylase Mutants on Locomotor Activity in Drosophila: A Study in Functional Genomics , 2002, Behavior genetics.

[112]  R. Jurenka,et al.  Pyrokinin/PBAN-like peptides in the central nervous system of Drosophila melanogaster , 2001, Cell and Tissue Research.

[113]  A. Baumann,et al.  Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. , 2001, Archives of insect biochemistry and physiology.

[114]  R. Predel Peptidergic neurohemal system of an insect: Mass spectrometric morphology , 2001, The Journal of comparative neurology.

[115]  D. Nässel,et al.  Pigment-dispersing factor in the locust abdominal ganglia may have roles as circulating neurohormone and central neuromodulator. , 2001, Journal of neurobiology.

[116]  G. Pollack,et al.  Mechanisms of frequency-specific responses of omega neuron 1 in crickets (Teleogryllus oceanicus): a polysynaptic pathway for song? , 2001, The Journal of experimental biology.

[117]  D. Nässel,et al.  Intestinal peptides as circulating hormones: release of tachykinin-related peptide from the locust and cockroach midgut. , 2001, The Journal of experimental biology.

[118]  E. Marder,et al.  The roles of co-transmission in neural network modulation , 2001, Trends in Neurosciences.

[119]  M. Williamson,et al.  Molecular cloning, genomic organization, and expression of a C-type (Manduca sexta-type) allatostatin preprohormone from Drosophila melanogaster. , 2001, Biochemical and biophysical research communications.

[120]  R. Predel,et al.  Myoinhibitory neuropeptides in the American cockroach☆ , 2001, Peptides.

[121]  J. Broeck Neuropeptides and their precursors in the fruitfly, Drosophila melanogaster☆ , 2001, Peptides.

[122]  I A Meinertzhagen,et al.  Visualization of synaptic markers in the optic neuropils of Drosophila using a new constrained deconvolution method , 2001, The Journal of comparative neurology.

[123]  S Schrader,et al.  Central projections of Drosophila sensory neurons in the transition from embryo to larva , 2000, The Journal of comparative neurology.

[124]  H. Dowse,et al.  Native and heterologous neuropeptides are cardioactive in Drosophila melanogaster. , 2000, Journal of insect physiology.

[125]  D. Coates,et al.  Expression and Functional Characterization of aDrosophila Neuropeptide Precursor with Homology to Mammalian Preprotachykinin A* , 2000, The Journal of Biological Chemistry.

[126]  T. Brody,et al.  Drosophila melanogasterG Protein–Coupled Receptors , 2000, The Journal of cell biology.

[127]  M. Williamson,et al.  Molecular cloning and genomic organization of an allatostatin preprohormone from Drosophila melanogaster. , 2000, Biochemical and biophysical research communications.

[128]  J. C. Hall,et al.  Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[129]  D. Yamamoto,et al.  A tyramine receptor gene mutation causes a defective olfactory behavior in Drosophila melanogaster. , 2000, Gene.

[130]  J. Hirsh,et al.  Ectopic G-protein expression in dopamine and serotonin neurons blocks cocaine sensitization in Drosophila melanogaster , 2000, Current Biology.

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

[132]  Jeffrey C. Hall,et al.  A pdf Neuropeptide Gene Mutation and Ablation of PDF Neurons Each Cause Severe Abnormalities of Behavioral Circadian Rhythms in Drosophila , 1999, Cell.

[133]  J. Dow,et al.  Isolation and characterization of a leucokinin-like peptide of Drosophila melanogaster. , 1999, The Journal of experimental biology.

[134]  Y. Kidokoro,et al.  Octopamine inhibits synaptic transmission at the larval neuromuscular junction in Drosophila melanogaster , 1999, Brain Research.

[135]  S. Birman,et al.  Differential Regulation of Drosophila Tyrosine Hydroxylase Isoforms by Dopamine Binding and cAMP-dependent Phosphorylation* , 1999, The Journal of Biological Chemistry.

[136]  M. Monastirioti,et al.  Biogenic amine systems in the fruit fly Drosophila melanogaster , 1999, Microscopy research and technique.

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

[138]  R. Cooper,et al.  Dopaminergic modulation of motor neuron activity and neuromuscular function in Drosophila melanogaster. , 1999, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[139]  P. Taghert,et al.  Functional Redundancy of FMRFamide-Related Peptides at theDrosophila Larval Neuromuscular Junction , 1998, The Journal of Neuroscience.

[140]  M. Palkovits,et al.  Localization and Dynamic Regulation of Biogenic Amine Transporters in the Mammalian Central Nervous System , 1998, Frontiers in Neuroendocrinology.

[141]  J. C. Hall,et al.  Isolation and Chronobiological Analysis of a Neuropeptide Pigment-Dispersing Factor Gene in Drosophila melanogaster , 1998, Journal of biological rhythms.

[142]  K. Han,et al.  A Novel Octopamine Receptor with Preferential Expression inDrosophila Mushroom Bodies , 1998, The Journal of Neuroscience.

[143]  N. Strausfeld,et al.  The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. , 1998, Learning & memory.

[144]  P. Taghert,et al.  A peritracheal neuropeptide system in insects: release of myomodulin-like peptides at ecdysis. , 1998, The Journal of experimental biology.

[145]  N. Grant,et al.  Are exocytosis mechanisms neurotransmitter specific? , 1997, Neurochemistry International.

[146]  Prof. Dr. José A. Campos-Ortega,et al.  The Embryonic Development of Drosophila melanogaster , 1997, Springer Berlin Heidelberg.

[147]  G. Gäde,et al.  Hormonal regulation in insects: facts, gaps, and future directions. , 1997, Physiological reviews.

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

[149]  P. Cooper,et al.  Distribution of sulfakinin-like peptides in the central and sympathetic nervous system of the American cockroach, Periplaneta americana (L.) and the field cricket, Teleogryllus commodus (Walker). , 1997, Tissue & cell.

[150]  C. Helfrich-Förster,et al.  Development of pigment‐dispersing hormone‐immunoreactive neurons in the nervous system of Drosophila melanogaster , 1997, The Journal of comparative neurology.

[151]  D. Nässel Advances in the immunocytochemical localization of neuroactive substances in the insect nervous system , 1996, Journal of Neuroscience Methods.

[152]  J. Truman,et al.  Increases in cyclic 3′,5′‐guanosine monophosphate (cGMP) occur at ecdysis in an evolutionarily conserved crustacean cardioactive peptide‐immunoreactive insect neuronal network , 1996, The Journal of comparative neurology.

[153]  M. Monastirioti,et al.  Characterization of Drosophila Tyramine β-HydroxylaseGene and Isolation of Mutant Flies Lacking Octopamine , 1996, The Journal of Neuroscience.

[154]  U. Homberg,et al.  Distribution of Dip‐allatostatin I‐like immunoreactivity in the brain of the locust Schistocerca gregaria with detailed analysis of immunostaining in the central complex , 1996, The Journal of comparative neurology.

[155]  Ronald L. Davis,et al.  DAMB, a Novel Dopamine Receptor Expressed Specifically in Drosophila Mushroom Bodies , 1996, Neuron.

[156]  D. Nässel,et al.  Neuropeptides, amines and amino acids in an elementary insect ganglion: Functional and chemical anatomy of the unfused abdominal ganglion , 1996, Progress in Neurobiology.

[157]  Paul S. Katz,et al.  Intrinsic neuromodulation: altering neuronal circuits from within , 1996, Trends in Neurosciences.

[158]  B. Stay,et al.  Immunocytochemical localization of Diploptera punctata allatostatin‐like peptide in Drosophila melanogaster , 1995, The Journal of comparative neurology.

[159]  K. Fuxe,et al.  Intercellular communication in the brain: Wiring versus volume transmission , 1995, Neuroscience.

[160]  V. M. Pickel,et al.  The vesicular monoamine transporter 2 is present in small synaptic vesicles and preferentially localizes to large dense core vesicles in rat solitary tract nuclei. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[161]  M. Monastirioti,et al.  Octopamine immunoreactivity in the fruit fly Drosophila melanogaster , 1995, The Journal of comparative neurology.

[162]  H. Niznik,et al.  A primordial dopamine D1‐like adenylyl cyclase‐linked receptor from Drosophila melanogaster displaying poor affinity for benzazepines , 1995, FEBS letters.

[163]  P. Stevenson,et al.  Localization of octopaminergic neurones in insects. , 1995, Comparative biochemistry and physiology. Part A, Physiology.

[164]  Olaf Breidbach,et al.  The Nervous Systems of Invertebrates: An Evolutionary and Comparative Approach , 1995, Experientia Supplementum.

[165]  T. Südhof,et al.  Synaptotagmin I: A major Ca2+ sensor for transmitter release at a central synapse , 1994, Cell.

[166]  J. Hirsh,et al.  A novel and major isoform of tyrosine hydroxylase in Drosophila is generated by alternative RNA processing. , 1994, The Journal of biological chemistry.

[167]  J. Veenstra Isolation and structure of the Drosophila corazonin gene. , 1994, Biochemical and biophysical research communications.

[168]  J. Hirsh,et al.  Temporal and spatial development of serotonin and dopamine neurons in the Drosophila CNS. , 1994, Developmental biology.

[169]  Daniel J. Garland,et al.  An immunocytochemical study of the FMRFamide neuropeptide gene products in Drosophila , 1993, The Journal of comparative neurology.

[170]  J. Truman,et al.  Isolation, characterization and expression of the eclosion hormone gene of Drosophila melanogaster. , 1993, European journal of biochemistry.

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

[172]  D. Nässel,et al.  Segmental peptidergic innervation of abdominal targets in larval and adult dipteran insects revealed with an antiserum against leucokinin I , 1992, Cell and Tissue Research.

[173]  D. Nässel,et al.  Neurons in the cockroach nervous system reacting with antisera to the neuropeptide leucokinin I , 1992, The Journal of comparative neurology.

[174]  M. Hörner,et al.  Octopamine-immunoreactive neurons in the central nervous system of the cricket, Gryllus bimaculatus , 1992, Cell and Tissue Research.

[175]  H. Pflüger,et al.  Octopamine immunoreactive cell populations in the locust thoracic‐abdominal nervous system , 1992, The Journal of comparative neurology.

[176]  J. Veenstra Presence of corazonin in three insect species, and isolation and identification of [His7]corazonin from Schistocerca americana , 1991, Peptides.

[177]  I. Kupfermann Functional studies of cotransmission. , 1991, Physiological reviews.

[178]  J. Bacon,et al.  The vasopressin-like immunoreactive (VPLI) neurons of the locust, Locusta migratoria. II. Physiology , 1991, Journal of Comparative Physiology A.

[179]  P. Taghert,et al.  In situ hybridization analysis of the FMRFamide neuropeptide gene in Drosophila. I. Restricted expression in embryonic and larval stages , 1991, The Journal of comparative neurology.

[180]  Lena Schneider,et al.  Interspecific comparison of a Drosophila gene encoding FMRFamide- related neuropeptides , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[181]  R. Scheller,et al.  Organization and expression of the Drosophila FMRFamide-related prohormone gene. , 1990, DNA and cell biology.

[182]  D. Nässel,et al.  Substance P‐, FMRFamide‐, and gastrin/cholecystokinin‐like immunoreactive neurons in the thoraco‐abdominal ganglia of the flies Drosophila and Calliphora , 1990, The Journal of comparative neurology.

[183]  D. Nässel,et al.  Vasopressin‐ and proctolin‐like immunoreactive efferent neurons in blowfly abdominal ganglia: Development and ultrastructure , 1989, The Journal of comparative neurology.

[184]  P. Bräunig Identification of a single prothoracic ‘dorsal unpaired median’ (DUM) neuron supplying locust mouthpart nerves , 1988, Journal of Comparative Physiology A.

[185]  R. Keller,et al.  Immunocytochemical localization of CCAP, a novel crustacean cardioactive peptide, in the nervous system of the shore crab, Carcinus maenas L. , 1988, Cell and Tissue Research.

[186]  Hans-Joachim Pflüger,et al.  The Organization of Mechanosensory Neuropiles in Locust Thoracic Ganglia , 1988 .

[187]  P. Taghert,et al.  Isolation and characterization of a Drosophila gene that encodes multiple neuropeptides related to Phe-Met-Arg-Phe-NH2 (FMRFamide). , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[188]  K. White,et al.  Serotonin‐containing neurons in Drosophila melanogaster: Development and distribution , 1988, The Journal of comparative neurology.

[189]  H. Keshishian,et al.  Identification of the neuropeptide transmitter proctolin in Drosophila larvae: characterization of muscle fiber-specific neuromuscular endings , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[190]  V. Budnik,et al.  Genetic dissection of dopamine and serotonin synthesis in the nervous system of Drosophila melanogaster. , 1987, Journal of neurogenetics.

[191]  C. Zahnow,et al.  The ultrastructure of nerve endings containing pigment-dispersing hormone (PDH) in crustacean sinus glands: Identification by an antiserum against a synthetic PDH , 1987, Cell and Tissue Research.

[192]  J. Marsh,et al.  Developmental expression and spatial distribution of dopa decarboxylase in Drosophila. , 1987, Developmental biology.

[193]  E. Marder,et al.  Distribution and partial characterization of FMRFamide‐like peptides in the stomatogastric nervous systems of the rock crab, Cancer borealis, and the spiny lobster, Panulirus interruptus , 1987, The Journal of comparative neurology.

[194]  K. White,et al.  Neuropeptide‐Fmrfamide‐Like immunoreactivity in drosophila: Development and distribution , 1986, The Journal of comparative neurology.

[195]  K. White,et al.  Development of serotonin-containing neurons in Drosophila mutants unable to synthesize serotonin , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[196]  J. Bacon,et al.  Ectopic neurons and the organization of insect sensory systems , 1985, Journal of Comparative Physiology A.

[197]  S. Maddrell EXCRETION IN THE BLOOD-SUCKING BUG, RHODNIUS PROLIXUS STAL. 3. THE CONTROL OF THE RELEASE OF THE DIURETIC HORMONE. , 1964, The Journal of experimental biology.

[198]  J. C. Li,et al.  Development in DROSOPHILA MELANOGASTER. , 1927, Genetics.

[199]  N. Maidment,et al.  Overexpression of the Drosophila vesicular monoamine transporter increases motor activity and courtship but decreases the behavioral response to cocaine , 2006, Molecular Psychiatry.

[200]  D. Soll,et al.  Coordination and modulation of locomotion pattern generators in Drosophila larvae: effects of altered biogenic amine levels by the tyramine beta hydroxlyase mutation. , 2006, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[201]  R. Hodgetts,et al.  Dopa decarboxylase: a model gene-enzyme system for studying development, behavior, and systematics. , 2006, Annual review of entomology.

[202]  R. Huey,et al.  Waking Experience Affects Sleep Need in Drosophila , 2006 .

[203]  T. Roeder Tyramine and octopamine: ruling behavior and metabolism. , 2005, Annual review of entomology.

[204]  D. Z̆itn̆an 3.1 – Neuroendocrine Regulation of Insect Ecdysis , 2005 .

[205]  D. Nässel,et al.  Aminergic neurons in the brain of blowflies and Drosophila: dopamine- and tyrosine hydroxylase-immunoreactive neurons and their relationship with putative histaminergic neurons , 2004, Cell and Tissue Research.

[206]  J. Meldolesi,et al.  Requirements for the identification of dense-core granules. , 2004, Trends in cell biology.

[207]  R. Hodgetts,et al.  Dopa decarboxylase from Drosophila melanogaster , 2004, Molecular and General Genetics MGG.

[208]  H. Penzlin,et al.  Immunocytochemical identification of proctolinlike immunoreactivity in the terminal ganglion and hindgut of the cockroach Periplaneta americana (L.) , 2004, Cell and Tissue Research.

[209]  Kostas Iatrou,et al.  comprehensive molecular insect science , 2004 .

[210]  H. Penzlin,et al.  The distribution of a proctolin-like immunoreactive material in the terminal ganglion of the cockroach, Periplaneta americana L. , 2004, Cell and Tissue Research.

[211]  P. Taghert,et al.  Drosophila neuropeptide signaling. , 2003, Advances in genetics.

[212]  P. Bräunig,et al.  Comparative aspects of peptidergic signaling pathways in the nervous systems of arthropods. , 1995, EXS.

[213]  W. Kutsch,et al.  Homologous Structures in the Nervous Systems of Arthropoda , 1994 .

[214]  K. White,et al.  Drosophila tyrosine hydroxylase is encoded by the pale locus. , 1993, Journal of neurogenetics.

[215]  G. A. Kerkut,et al.  Comprehensive insect physiology, biochemistry, and pharmacology , 1985 .

[216]  N. Strausfeld Atlas of an Insect Brain , 1976, Springer Berlin Heidelberg.