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Postembryonic development of astrocyte-like glia of the central complex in the grasshopper Schistocerca gregaria

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Abstract

Central complex modules in the postembryonic brain of the grasshopper Schistocerca gregaria are enveloped by Repo-positive/glutamine-synthetase-positive astrocyte-like glia. Such cells constitute Rind-Neuropil Interface glia. We have investigated the postembryonic development of these glia and their anatomical relationship to axons originating from the w, x, y, z tract system of the pars intercerebralis. Based on glutamine synthetase immunolabeling, we have identified four morphological types of cells: bipolar type 1 glia delimit the central body but only innervate its neuropil superficially; monopolar type 2 glia have a more columnar morphology and direct numerous gliopodia into the neuropil where they arborize extensively; monopolar type 3 glia are found predominantly in the region between the noduli and the central body and have a dendritic morphology and their gliopodia project deeply into the central body neuropil where they arborize extensively; multipolar type 4 glia link the central body neuropil with neighboring neuropils of the protocerebrum. These glia occupy type-specific distributions around the central body. Their gliopodia develop late in embryogenesis, elongate and generally become denser during subsequent postembryonic development. Gliopodia from putatively type 3 glia within the central body have been shown to lie closely apposed to individual axons of identified columnar fiber bundles from the w, x, y, z tract system of the central complex. This anatomical association might offer a substrate for neuron/glia interactions mediating postembryonic maturation of the central complex.

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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 

  • Baumann PM, Oland LA, Tolbert LP (1996) Glial cells stabilize axonal protoglomeruli in the developing olfactory lobe of the moth Manduca sexta. J Comp Neurol 373:118–128

    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 

  • Boyan GS, Reichert H (2011) Mechanisms for complexity in the brain: generating the insect central complex. Trends Neurosci 34:247–257

    Article  PubMed  CAS  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 G, Loser M, Williams L, Liu Y (2011) Astrocyte-like glia associated with the embryonic development of the central complex in the grasshopper Schistocerca gregaria. Dev Genes Evol 221:141–155

    Article  PubMed  Google Scholar 

  • Boyan GS, Liu Y, Loser M (2012) A cellular network of dye-coupled glia associated with the embryonic central complex in the grasshopper Schistocerca gregaria. Dev Genes Evol 222:125–138

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Cantera R (1993) Glial cells in adult and developing prothoracic ganglion of the hawk moth Manduca sexta. Cell Tissue Res 272:93–108

    Article  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. Annu Rev Entomol 35:597–621

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Cayre M, Strambi C, Strambi A (1994) Neurogenesis in an adult insect brain and its hormonal control. Nature 368:57–59

    Article  CAS  Google Scholar 

  • Cayre M, Strambi C, Charpin P, Augier R, Meyer MR, Edwards JS, Strambi A (1996) Neurogenesis in adult insect mushroom bodies. J Comp Neurol 371:300–310

    Article  PubMed  CAS  Google Scholar 

  • Cayre M, Scotto-Lomassese S, Malaterre J, Strambi C, Strambi A (2007) Understanding the regulation and function of adult neurogenesis: contribution from an insect model, the house cricket. Chem Senses 32:385–395

    Article  PubMed  Google Scholar 

  • Chapman RF (1982) The insects: structure and function. Hodder and Stoughton, London

    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 

  • Edwards TN, Meinertzhagen IA (2010) The functional organisation of glia in the adult brain of Drosophila and other insects. Prog Neurobiol 90:471–497

    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 

  • Goodman CS (1984) Landmarks and labels that help developing neurons find their way. BioScience 34:300–307

    Article  Google Scholar 

  • Goodman CS (1996) Mechanisms and molecules that control growth cone guidance. Annu Rev Neurosci 19:341–377

    Article  PubMed  CAS  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 Laboratory, Cold Spring Harbor, NY, pp 1131–1206

    Google Scholar 

  • Goodman CS, Spitzer NC (1980) Embryonic development of neurotransmitter receptors in grasshoppers. In: Sattelle DB, Hall LM, Hildebrand JG (eds) Receptors for neurotransmitters, hormones and pheromones in insects. Elsevier/North-Holland Biomedical, Amsterdam, pp 195–207

    Google Scholar 

  • Goodman CS, Spitzer NC (1981) The development of electrical properties of identified neurons in grasshopper embryos. J Physiol (Lond) 313:385–413

    CAS  Google Scholar 

  • Goodman CS, O’Shea M, Caman R, Spitzer NC (1979) Embryonic development of identified neurons: temporal pattern of morphological and biochemical differentiation. Science 204:1219–1222

    Article  PubMed  CAS  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 (2011) Morphological diversity and development of glia in Drosophila. Glia 59:1237–1252

    Article  PubMed  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  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 

  • Herbert Z, Rauser S, Williams L, Kapan N, Güntner M, Walch A, Boyan G (2010) Developmental expression of neuromodulators in the central complex of the grasshopper Schistocerca gregaria. J Morphol 271:1509–1526

    Article  PubMed  CAS  Google Scholar 

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

    Article  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 

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

    Article  PubMed  CAS  Google Scholar 

  • Ito K, Urban J, Technau GM (1995) Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux’s Arch Dev Biol 204:284–307

    Article  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  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 

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

    Article  PubMed  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 

  • Koussa MA, Tolbert LP, Oland LA (2010) Development of a glial network in the olfactory nerve: role of calcium and neuronal activity. Neuron Glia Biol 6:245–261

    Article  PubMed  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 

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

    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. Roux’s 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 

  • Panov AA (1963) The origin and fate of neuroblasts, neurons and neuroglial cells in the central nervous system of the china oak silkworm, Antheraea pernyi Guer (Lepidoptera, Attacidae). Entomol Rev URSS 42:186–191

    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 

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

    Article  PubMed  CAS  Google Scholar 

  • Pipa RL (1961) Studies on the hexapod nervous system. III. Histology and histochemistry of cockroach neuroglia. J Comp Neurol 116:15–24

    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 

  • 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 

  • Schmidt J, Deitmar JW (1996) Photoinactivation of the giant neuropil glial cells in the leech Hirudo medicinalis: effects on neuronal activity and synaptic transmission. J Neurophysiol 76:2861–2871

    PubMed  CAS  Google Scholar 

  • Schofield PK, Treherne JE (1984) Localization of the blood-brain barrier of an insect: electrical model and analysis. J Exp Biol 109:319–331

    Google Scholar 

  • Schofield PK, Swales LS, Trehern JE (1984) Potentials associated with the blood-brain barrier of an insect: recordings from identified neuroglia. J Exp Biol 109:307–318

    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 

  • 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 

  • Siegl T, Schachtner J, Holstein GR, Homberg U (2009) NO/cGMP signalling: L:-citrulline and cGMP immunostaining in the central complex of the desert locust Schistocerca gregaria. Cell Tissue Res 337:327–340

    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 (2012) Arthropod brains. Harvard University Press, Cambridge

    Google Scholar 

  • Swales LS, Lane NJ (1985) Embyronic development of glial cells and their junctions in the locust central nervous system. J Neurosci 5:117–127

    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 

  • 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

    Article  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 (1995) Insect glial cells and their relationships with neurons. In: Vernadakis A, Roots B (eds) Neuron-glia interrelationships during phylogeny: plasticity and regeneration. Humana, Totowa, pp 49–77

    Chapter  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 

  • 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 

  • Wigglesworth VB (1959) The histology of the nervous system of an insect, Rhodnius prolixus (Hemiptera). II. The central ganglia. Q J Microsc Sci 100:299–313

    Google Scholar 

  • Williams JLD (1972) Some observations on the neuronal organisation of the supra-oesophageal ganglion in Schistocerca gregaria Forskål with particular reference to the central complex. PhD Thesis, University of Wales

  • 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 

  • 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 

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Acknowledgments

We thank M. Loser for assistance with GS immunolabeling, Dr. Yu Liu for critical comments on the manuscript and Karin Fischer for excellent technical assistance.

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

    George Boyan, Leslie Williams & Stefanie Götz

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  1. George Boyan
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  2. Leslie Williams
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  3. Stefanie Götz
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Correspondence to George Boyan.

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This work was supported by the Deutsche Forschungsgemeinschaft (BO 1434/3-5).

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Supplemetary Fig. 1

Reproducibility of data (arrow with V ventral). Confocal images of horizontal brain slices at the level of the central body (CB; outlined by a dashed white line) in three adult preparations (a–c) following glutamine synthetase (GS) immunolabling reveal consistent morphology of RNI types 1, 2 and 4 astrocyte-like glia (open/white arrowheads). Bar 46 μm (JPEG 41 kb)

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Boyan, G., Williams, L. & Götz, S. Postembryonic development of astrocyte-like glia of the central complex in the grasshopper Schistocerca gregaria . Cell Tissue Res 351, 361–372 (2013). https://doi.org/10.1007/s00441-012-1535-0

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