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Astrocyte-like glia associated with the embryonic development of the central complex in the grasshopper Schistocerca gregaria

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Abstract

In this study we employed the expression of the astrocyte-specific enzyme glutamine synthetase, in addition to the glia-specific marker Repo, to characterize glia cell types associated with the embryonic development of the central complex in the grasshopper Schistocerca gregaria. Double labeling experiments reveal that all glutamine synthetase-positive cells associated with the central complex are also Repo-positive and horseradish peroxidase-negative, confirming they are glia. Early in embryogenesis, prior to development of the central complex, glia form a continuous population extending from the pars intercerebralis into the region of the commissural fascicles. Subsequently, these glia redisperse to envelop each of the modules of the central complex. No glial somata are found within the central complex neuropils themselves. Since glutamine synthetase is expressed cortically in glia, it allows their processes as well as their soma locations to be visualized. Single cell reconstructions reveal one population of glia as directing extensive ensheathing processes around central complex neuropils such as the central body, while another population projects columnar-like arborizations within the central body. Such arborizations are only seen in central complex modules after their neuroarchitecture has been established suggesting that the glial arborizations project onto a prior scaffold of neurons or tracheae.

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References

  • Awasaki T, Lai S-L, Ito K, Lee T (2008) Organization and postembryonic development of glial cells in the adult central brain of Drosophila. J Neurosci 28:13742–13753

    Article  PubMed  CAS  Google Scholar 

  • Bastiani MJ, Goodman CS (1986) Guidance of neuronal growth cones in the grasshopper embryo. III. Recognition of specific glial pathways. J Neurosci 6:3542–3551

    PubMed  CAS  Google Scholar 

  • Bayraktar OA, Boone JQ, Drummond ML, Doe CQ (2010) Drosophila type II neuroblast lineages keep Prospero levels low to generate large clones that contribute to the adult brain central complex. Neural Dev 5:26

    Article  PubMed  CAS  Google Scholar 

  • Bear MF, Connors BW, Paradiso MA (2007) Neuroscience. Exploring the brain, 3rd edn. Lippincott Williams & Wilkins, Philadelphia

  • Bello BC, Izergina N, Caussinus E, Reichert H (2008) Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev 3:5

    Article  PubMed  CAS  Google Scholar 

  • Bentley D, Keshishian H, Shankland M, Torian-Raymond A (1979) Quantitative staging of embryonic development of the grasshopper, Schistocerca nitens. J Embryol Exp Morphol 54:47–74

    PubMed  CAS  Google Scholar 

  • Booth GE, Kinrade EFV, Hidalgo A (2000) Glia maintain follower neuron survival during Drosophila CNS development. Development 127:237–244

    PubMed  CAS  Google Scholar 

  • Boyan GS, Williams JLD (1997) Embryonic development of the pars intercerebralis/central complex of the grasshopper. Dev Genes Evol 207:317–329

    Article  Google Scholar 

  • Boyan G, Williams L, Meier T (1993) Organization of the commissural fibers in the adult brain of the locust. J Comp Neurol 332:358–377

    Article  PubMed  CAS  Google Scholar 

  • Boyan GS, Therianos S, Williams JLD, Reichert H (1995) Axogenesis in the embryonic brain of the grasshopper Schistocerca gregaria: an identified cell analysis of early brain development. Development 121:75–86

    PubMed  CAS  Google Scholar 

  • Boyan GS, Williams JL, Herbert Z (2008a) Fascicle switching generates a chiasmal neuroarchitecture in the embryonic central body of the grasshopper Schistocerca gregaria. Arthr Struct Dev 37:539–544

    Article  CAS  Google Scholar 

  • Boyan GS, Williams JL, Herbert Z (2008b) An ontogenetic analysis of locustatachykinin-like expression in the central complex of the grasshopper Schistocerca gregaria. Arthr Struct Dev 37:480–491

    Article  CAS  Google Scholar 

  • Boyan G, Williams L, Legl A, Herbert Z (2010) Proliferative cell types in embryonic lineages of the central complex of the grasshopper Schistocerca gregaria. Cell Tissue Res 341:259–277

    Article  PubMed  Google Scholar 

  • Breidbach O, Dennis R, Marx J, Görlach C, Wiegandt H, Wegerhoff R (1992) Insect glial cells show differential expression of a glycolipid-derived, glucuronic acid-containing epitope throughout neurogenesis: detection during postembryogenesis and regeneration in the central nervous system of Tenebrio molitor. L Neurosci Lett 147:5–8

    Article  CAS  Google Scholar 

  • Buchanan R, Benzer S (1993) Defective glia in the Drosophila brain degeneration mutant drop dead. Neuron 10:839–850

    Article  PubMed  CAS  Google Scholar 

  • Cantera R, Trujillo-Cenoz O (1996) Glial cells in insect ganglia. Micr Res Tech 35:285–293

    Article  CAS  Google Scholar 

  • Carlson SD, Saint Marie RL (1990) Structure and function of insect glia. Ann Rev Entomol 35:597–621

    Article  Google Scholar 

  • Carlson SD, Juang JL, Hilgers SL, Garment MB (2000) Blood barriers of the insect. Ann Rev Entomol 45:151–174

    Article  CAS  Google Scholar 

  • Condron BG, Patel NH, Zinn K (1994) engrailed controls glial/neuronal cell fate decisions at the midline of the central nervous system. Neuron 13:541–554

    Article  PubMed  CAS  Google Scholar 

  • Crews ST, Thomas JB, Goodman CS (1988) The Drosophila single-minded gene encodes a nuclear protein with sequence similarity to the per gene product. Cell 52:143–151

    Article  PubMed  CAS  Google Scholar 

  • Doe CQ (2008) Neural stem cells: balancing self-renewal with differentiation. Development 135:1575–1587

    Article  PubMed  CAS  Google Scholar 

  • Doe CQ, Goodman CS (1985a) Early events in insect neurogenesis. I. Development and segmental differences in the pattern of neuronal precursor cells. Dev Biol 111:193–205

    Article  PubMed  CAS  Google Scholar 

  • Doe CQ, Goodman CS (1985b) Early events in insect neurogenesis. II. The role of cell interactions and cell lineage in the determination of neuronal precursor cells. Dev Biol 111:206–219

    Article  PubMed  CAS  Google Scholar 

  • Ebens AJ, Garren H, Cheyette BN, Zipursky SL (1993) The Drosophila anachronism locus: a glycoprotein secreted by glia inhibits neuroblast proliferation. Cell 74:15–27

    Article  PubMed  CAS  Google Scholar 

  • Edenfeld G, Volohonsky G, Krukkert K, Naffin E, Lammel U, Grimm A, Engelen D, Reuveny A, Volk T, Klämbt C (2006) The splicing factor Crooked Neck associates with the RNA-binding protein HOW to control glial cell maturation in Drosophila. Neuron 52:969–980

    Article  PubMed  CAS  Google Scholar 

  • el Jundi B, Heinze S, Lenschow C, Kurylas A, Rohlfing T, Homberg U (2010) The locust standard brain: a 3D standard of the central complex as a platform for neural network analysis. Front Syst Neurosci 3:21

    PubMed  Google Scholar 

  • Gocht D, Wagner S, Heinrich R (2009) Recognition, presence, and survival of locust central nervous glia in situ and in vitro. Micr Res Tech 72:385–397

    Article  Google Scholar 

  • Goodman CS, Doe CQ (1994) Embryonic development of the Drosophila central nervous system. In: Bate M, Martinez-Arias A (eds) The development of Drosophila, vol 1. Cold Spring Harbor Press, New York, pp 1131–1206

    Google Scholar 

  • Haase A, Stern M, Wächtler K, Bicker G (2001) A tissue-specific marker of Ecdysozoa. Dev Genes Evol 211:428–433

    Article  PubMed  CAS  Google Scholar 

  • Hähnlein I, Bicker G (1996) Morphology of neuroglia in the antennal lobes and mushroom bodies of the brain of the honeybee. J Comp Neurol 367:235–245

    Article  PubMed  Google Scholar 

  • Hähnlein I, Bicker G (1997) Glial patterning during postembryonic development of central neuropiles in the brain of the honeybee. Dev Genes Evol 207:29–41

    Article  PubMed  Google Scholar 

  • Halter DA, Urban J, Rickert C, Ner SS, Ito K, Travers AA, Technau GM (1995) The homeobox gene repo is required for the differentiation and maintenance of glial function in the embryonic nervous system of Drosophila melanogaster. Development 121:317–322

    PubMed  CAS  Google Scholar 

  • Hartenstein V, Nassif C, Lekven A (1998) Embryonic development of the Drosophila brain. II. Pattern of glia cells. J Comp Neurol 402:32–47

    Article  PubMed  CAS  Google Scholar 

  • Hartenstein V, Spindler S, Pereanu W, Fung S (2008) The development of the Drosophila larval brain. Adv Exp Med Biol 628:1–31

    Article  PubMed  Google Scholar 

  • Harzsch S, Hansson BS (2008) Brain architecture in the terrestrial hermit crab Coenobita clypeatus (Anomura, Coenobitidae), a crustacean with a good aerial sense of smell. BMC Neurosci 9:58

    Article  PubMed  CAS  Google Scholar 

  • Heinze S, Homberg U (2007) Maplike representation of celestial e-vector orientations in the brain of an insect. Science 315:995–997

    Article  PubMed  CAS  Google Scholar 

  • Heinze S, Homberg U (2008) Neuroarchitecture of the central complex of the desert locust: intrinsic and columnar neurons. J Comp Neurol 511:454–478

    Article  PubMed  Google Scholar 

  • Hidalgo A (2003) Neuron–glia interactions during axon guidance in Drosophila. Biochem Soc Trans 31:50–55

    Article  PubMed  CAS  Google Scholar 

  • Hidalgo A, Booth GE (2000) Glia dictate pioneer axon trajectories in the Drosophila embryonic CNS. Development 127:393–402

    PubMed  CAS  Google Scholar 

  • Homberg U (2002) Neurotransmitters and neuropeptides in the brain of the locust. Microsc Res Tech 56:189–209

    Article  PubMed  CAS  Google Scholar 

  • Hosoya T, Takizawa K, Nitta K, Hotta Y (1995) Glial cells missing: a binary switch between neuronal and glial determination in Drosophila. Cell 82:1025–1036

    Article  PubMed  CAS  Google Scholar 

  • Hoyle G (1986) Glial cells of an insect ganglion. J Comp Neurol 246:85–103

    Article  PubMed  CAS  Google Scholar 

  • Ilius M, Wolf R, Heisenberg M (1994) The central complex of Drosophila melanogaster is involved in flight control: studies on mutants and mosaics of the gene ellipsoid body open. J Neurogenet 9:189–206

    Article  PubMed  CAS  Google Scholar 

  • Ito K, Awasaki T (2008) Clonal unit architecture of the adult fly brain. In: Technau GM (ed) Brain development in Drosophila melanogaster. Springer, New York, pp 137–158

    Google Scholar 

  • Ito K, Urban J, Technau GM (1994) Distribution, classification and development of Drosophila glial cells during late embryogenesis. Roux’s Arch Dev Biol 204:284–307

    Article  Google Scholar 

  • Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto D (1997) The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124:761–771

    PubMed  CAS  Google Scholar 

  • Izergina N, Balmer J, Bello B, Reichert H (2009) Postembryonic development of transit amplifying neuroblast lineages in the Drosophila brain. Neural Dev 4:44

    Article  PubMed  CAS  Google Scholar 

  • Jacobs JR, Goodman CS (1989) Embryonic development of axon pathways in the Drosophila CNS. I. A glial scaffold appears before the first growth cones. J Neurosci 9:2402–2411

    PubMed  CAS  Google Scholar 

  • Jan LY, Jan YN (1982) Antibodies to horseradish-peroxidase as specific neuronal markers in Drosophila and grasshopper embryos. Proc Natl Acad Sci USA 79:2700–2704

    Article  PubMed  CAS  Google Scholar 

  • Jones BW, Fetter RD, Tear G, Goodman CS (1995) Glial cells missing: a genetic switch that controls glial versus neuronal fate. Cell 82:1013–23

    Article  PubMed  CAS  Google Scholar 

  • Klaes A, Menne T, Stollewerk A, Scholz H, Klämbt C (1994) The Ets transcription factors encoded by the Drosophila gene pointed direct glial cell differentiation in the embryonic CNS. Cell 78:149–160

    Article  PubMed  CAS  Google Scholar 

  • Klämbt C (2009) Modes and regulation of glial migration in vertebrates and invertebrates. Nat Rev Neurosci 10:769–779

    Article  PubMed  CAS  Google Scholar 

  • Klämbt C, Goodman CS (1991) The diversity and pattern of glia during axon pathway formation in the Drosophila embryo. Glia 4:205–213

    Article  PubMed  Google Scholar 

  • Klämbt C, Jacobs JR, Goodman CS (1991) The midline of the Drosophila central nervous system: a model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell 64:801–815

    Article  PubMed  Google Scholar 

  • Kretzschmar D, Pflugfelder GO (2002) Glia in development, function, and neurodegeneration of the adult insect brain. Brain Res Bull 57:121–31

    Article  PubMed  CAS  Google Scholar 

  • Learte AR, Hidalgo A (2007) The role of glial cells in axon guidance, fasciculation and targeting. Adv Exp Med Biol 621:156–166

    Article  PubMed  Google Scholar 

  • Liu G, Seiler H, Wen A, Zars T, Ito K, Wolf M, Heisenberg M, Liu L (2006) Distinct memory traces for two visual features in the Drosophila brain. Nature 439:551–556

    Article  PubMed  CAS  Google Scholar 

  • Loesel R, Weigel S, Braunig P (2006) A simple fluorescent double staining method for distinguishing neuronal from non-neuronal cells in the insect central nervous system. J Neurosci Meth 155:202–206

    Article  CAS  Google Scholar 

  • Martinez-Hernandez A, Bell KP, Norenberg MD (1977) Glutamine synthetase: glial localization in brain. Science 195:1356–1358

    Article  PubMed  CAS  Google Scholar 

  • Müller M, Homberg U, Kühn A (1997) Neuroarchitecture of the lower division of the central body in the brain of the locust (Schistocerca gregaria). Cell Tissue Res 288:159–176

    Article  PubMed  Google Scholar 

  • Naimski P, Bierzyimageski A, Fikus M (1980) Quantitative fluorescent analysis of different conformational forms of DNA bound to the dye 4′,6-diamidine-2-phenylindole, and separated by gel electrophoresis. Anal Biochem 106:471–475

    Article  PubMed  CAS  Google Scholar 

  • Neuser K, Triphan T, Mronz M, Poeck B, Strauss R (2008) Analysis of a spatial orientation memory in Drosophila. Nature 453:1244–1247

    Article  PubMed  CAS  Google Scholar 

  • Noordermeer JN, Kopczynski CC, Fetter RD, Bland KS, Chen W-Y, Goodman CS (1998) Wrapper, a novel member of the Ig superfamily, is expressed by midline glia and is required for them to ensheath commissural axons in Drosophila. Neuron 21:991–1001

    Article  PubMed  CAS  Google Scholar 

  • Nordlander RH, Edwards JS (1969) Postembryonic brain development in the monarch butterfly, Danaus plexippus plexippus, L. I Cellular events during brain morphogenesis. Wilh Roux’Archiv 162:197–217

    Article  Google Scholar 

  • Oland LA, Tolbert LP (1987) Glial patterns during early development of antennal lobes of Manduca sexta: a comparison between normal lobes and lobes deprived of antennal axons. J Comp Neurol 255:196–207

    Article  PubMed  CAS  Google Scholar 

  • Oland LA, Tolbert LP (1989) Patterns of glial proliferation during formation of olfactory glomeruli in an insect. Glia 2:10–24

    Article  PubMed  CAS  Google Scholar 

  • Oland LA, Marrero HG, Burger I (1999) Glial cells in the developing and adult olfactory lobe of the moth Manduca sexta. Cell Tissue Res 297:527–545

    Article  PubMed  CAS  Google Scholar 

  • Page DT (2004) A mode of arthropod brain evolution suggested by Drosophila commissure development. Evol Dev 6:25–31

    Article  PubMed  Google Scholar 

  • Pereanu W, Hartenstein V (2006) Neural lineages of the Drosophila brain: a three-dimensional digital atlas of the pattern of lineage location and projection at the late larval stage. J Neurosci 26:5534–5553

    Article  PubMed  CAS  Google Scholar 

  • Pereanu W, Shy D, Hartenstein V (2005) Morphogenesis and proliferation of the larval brain glia in Drosophila. Dev Biol 283:191–203

    Article  PubMed  CAS  Google Scholar 

  • Pereanu W, Younossi-Hartenstein A, Lovick J, Spindler S, Hartenstein V (2010) A lineage-based analysis of the development of the central complex of the Drosophila brain. J Comp Neurol. doi:10.1002/cne.22542

    PubMed  Google Scholar 

  • Pielage J, Klämbt C (2001) Glial cells aid axonal target selection. Trends Neurosci 24:432–433

    Article  PubMed  CAS  Google Scholar 

  • Poeck B, Fischer S, Gunning D, Zipursky SL, Salecker I (2001) Glial cells mediate target layer selection of retinal axons in the developing visual system of Drosophila. Neuron 29:99–113

    Article  PubMed  CAS  Google Scholar 

  • Rangarajan R, Gong Q, Gaul U (1999) Migration and function of glia in the developing Drosophila eye. Development 126:3285–3292

    PubMed  CAS  Google Scholar 

  • Reichert H, Boyan G (1997) Building a brain: developmental insights in insects. Trends Neurosci 20:258–263

    Article  PubMed  CAS  Google Scholar 

  • Renn SCN, Armstrong JD, Yang M, Wang Z, An X, Kaiser K, Taghert PH (1999) Genetic analysis of the Drosophila ellipsoid body neuropil: organization and development of the central complex. J Neurobiol 41:189–207

    Article  PubMed  CAS  Google Scholar 

  • Saitoh F, Toshiyuki A (2010) Proteasomal degradation of glutamine synthetase regulates Schwann cell differentiation. J Neurosci 30:1204–1212

    Article  PubMed  CAS  Google Scholar 

  • Scholz H, Sadlowski E, Klaes A, Klämbt C (1997) Control of midline glia development in the embryonic Drosophila CNS. Mech Dev 62:79–91

    Article  PubMed  CAS  Google Scholar 

  • Seaver EC, Carpenter EM, Bastiani MJ (1996) REGA-1 is a GPI-linked member of the immunoglobulin superfamily present on restricted regions of sheath cell processes in grasshopper. Development 122:567–578

    PubMed  CAS  Google Scholar 

  • Seeger M, Tear G, Ferres-Marco D, Goodman CS (1993) Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10:409–426

    Article  PubMed  CAS  Google Scholar 

  • Sepp KJ, Auld VJ (2003) Reciprocal interactions between neurons and glia are required for Drosophila peripheral nervous system development. J Neurosci 23:8221–8230

    PubMed  CAS  Google Scholar 

  • Sepp KJ, Schulte J, Auld VJ (2001) Peripheral glia direct axon guidance across the CNS/PNS transition zone. Dev Biol 238:47–63

    Article  PubMed  CAS  Google Scholar 

  • Silies M, Yuva Y, Engelen D, Aho A, Stork T, Klämbt C (2007) Glial cell migration in the eye disc. J Neurosci 27:13130–13139

    Article  PubMed  CAS  Google Scholar 

  • Snow PM, Patel NH, Harrelson AL, Goodman CS (1987) Neural-specific carbohydrate moiety shared by many surface glycoproteins in Drosophila and grasshopper embryos. J Neurosci 7:4137–4144

    PubMed  CAS  Google Scholar 

  • Sonnenfeld MJ, Jacobs JR (1995) Apoptosis of the midline glia during Drosophila embryogenesis: a correlation with axon contact. Development 121:569–578

    PubMed  CAS  Google Scholar 

  • Stevenson PA, Kutsch W (1986) Basic circuitry of an adult-specific motor program completed with embryogenesis. Naturwissenschaften 73:741–743

    Article  Google Scholar 

  • Strausfeld NJ (2009) Brain organization and the origin of insects: an assessment. Proc R Soc B 276:1929–1937

    Article  PubMed  Google Scholar 

  • Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12:633–638

    Article  PubMed  CAS  Google Scholar 

  • Strauss R, Heisenberg M (1993) A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13:1852–1861

    PubMed  CAS  Google Scholar 

  • Strauss R, Hanesch U, Kinkelin M, Wolf R, Heisenberg M (1992) No-bridge of Drosophila melanogaster: portrait of a structural brain mutant of the central complex. J Neurogenet 8:125–155

    Article  PubMed  CAS  Google Scholar 

  • Therianos S, Leuzinger S, Hirth F, Goodman CS, Reichert H (1995) Embryonic development of the Drosophila brain: formation of commissural and descending pathways. Development 121:3849–3860

    PubMed  CAS  Google Scholar 

  • Thomas JB, Crews ST, Goodman CS (1988) Molecular genetics of the single-minded locus: a gene involved in the development of the Drosophila nervous system. Cell 52:133–141

    Article  PubMed  CAS  Google Scholar 

  • van der Hel WS, Notenboom RGE, Bos IWM, van Rijen PC, van Veelen CWM, de Graan PNE (2005) Reduced glutamine synthetase in hippocampal areas with neuron loss in temporal lobe epilepsy. Neurology 64:326–333

    PubMed  Google Scholar 

  • Vanhems E (1985) An in vitro autoradiographic study of gliogenesis in the embryonic locust brain. Dev Brain Res 23:269–275

    Article  Google Scholar 

  • Vanhems E, Delbos M (1987) Differentiation of glial cells and neurite outgrowth obtained from embryonic locust central nervous system explants. Brain Res 411:129–138

    Article  PubMed  CAS  Google Scholar 

  • Vanhems E, Girardie J (1983) Undifferentiated cells present in the pars intercerebralis of larval and adult locusts are glial precursors. Autoradiographic and ultrastructural study in vivo and in vitro. Dev Brain Res 10:177–185

    Article  Google Scholar 

  • Viktorin G, Riebli N, Popkova A, Giangrande A, Reichert H (2011) Multipotent neural stem cells generate glial cells of the central complex through transit amplifying intermediate progenitors in Drosophila brain development. Development (in press)

  • Ward M, Jobling A, Puthussery T, Foster L, Fletcher E (2004) Localization and expression of the glutamate transporter, excitatory amino acid transporter 4, within astrocytes of the rat retina. Cell Tissue Res 315:305–310

    Article  PubMed  CAS  Google Scholar 

  • Wedler FC, Horn BR (1976) Catalytic mechanisms of glutamine synthetase enzymes. J Biol Chem 251:7530–7538

    PubMed  CAS  Google Scholar 

  • Williams JLD (1975) Anatomical studies of the insect central nervous system: a ground-plan of the midbrain and an introduction to the central complex in the locust, Schistocerca gregaria (Orthoptera). J Zool Lond 176:67–86

    Article  Google Scholar 

  • Williams JLD, Guentner M, Boyan GS (2005) Building the central complex of the grasshopper Schistocerca gregaria: temporal topology organizes the neuroarchitecture of the w, x, y, z tracts. Arthr Struct Dev 34:97–110

    Article  Google Scholar 

  • Xiong W, Okano H, Patel N, Blendy J, Montell C (1994) Repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev 8:981–994

    Article  PubMed  CAS  Google Scholar 

  • Young JM, Armstrong JD (2010a) Structure of the adult central complex in Drosophila: organization of distinct neuronal subsets. J Comp Neurol 518:1500–1524

    Article  PubMed  CAS  Google Scholar 

  • Young JM, Armstrong JD (2010b) Building the central complex in Drosophila: the generation and development of distinct subsets. J Comp Neurol 518:1525–1541

    Article  PubMed  CAS  Google Scholar 

  • Zak NB, Wides RJ, Schejter ED, Raz E, Shilo BZ (1990) Localization of the DER/flb protein in embryos: implications on the faint little ball lethal phenotype. Development 109:865–839

    PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Karin Fischer and Dr. Olga Alexandrova for excellent technical assistance. Grant sponsor: Deutsche Forschungsgemeinschaft (BO 1434/3-5).

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  1. Developmental Neurobiology Group, Biocenter, Ludwig-Maximilians-Universität, Grosshadernerstr. 2, 82152, Martinsried, Germany

    George Boyan, Michael Loser, Leslie Williams & Yu Liu

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  1. George Boyan
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  2. Michael Loser
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Correspondence to George Boyan.

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Communicated by V. Hartenstein

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Boyan, G., Loser, M., Williams, L. et al. Astrocyte-like glia associated with the embryonic development of the central complex in the grasshopper Schistocerca gregaria . Dev Genes Evol 221, 141–155 (2011). https://doi.org/10.1007/s00427-011-0366-4

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