Glial investment of the adult and developing antennal lobe of Drosophila

Journal of Comparative Neurology

Volumn 509, Issue 5, 2008, Pages 526-550

  Oland, Lynne A ^a   Biebelhausen, John P ^a   Tolbert, Leslie P ^a  

^a UNIVERSITY OF ARIZONA   (United States)

Author keywords

Glial cells; Glomeruli; Olfactory bulb; Olfactory lobe

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ANIMAL CELL; ANTENNA; ARTICLE; CELL MATURATION; CONFOCAL MICROSCOPY; DROSOPHILA; ELECTRON MICROSCOPY; GLIA CELL; MANDUCA SEXTA; NERVE FIBER; NEUROPIL; NONHUMAN; OLFACTORY BULB; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AGE FACTORS; ANIMALS; BRAIN; DROSOPHILA MELANOGASTER; NEUROGLIA; OLFACTORY PATHWAYS;

EID: 48249133339     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21762     Document Type: Article

References (112)

1. Alfonso TB, Jones BW. 2002. Gcm2 promotes glial cell differentiation and is required with glial cells missing for macrophage development in Drosophila. Dev Biol 248:369-383.
2. Allen NJ, Barres BA. 2005. Signaling between glia and neurons: focus on synaptic plasticity. Curr Opin Neurobiol 15:542-548.
3. Ang LH, Kim J, Stepensky V, Hing H. 2003. Dock and pak regulate olfactory axon pathfinding in Drosophila. Development 130:1307-1316.
4. Au WW, Treloar HB, Greer CA. 2002. Sublaminar organization of the mouse olfactory bulb nerve layer. J Comp Neurol 446:68-80.
5. Bailey MS, Shipley MT. 1993. Astrocyte subtypes in the rat olfactory bulb: morphological heterogeneity and differential laminar distribution. J Comp Neurol 328:501-526.
6. Bailey MS, Puche AC, Shipley MT. 1999. Development of the olfactory bulb: evidence for glia-neuron interactions in glomerular formation. J Comp Neurol 415:423-448.
7. 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.
8. Bhalerao S, Sen A, Stocker R, Rodrigues V. 2003. Olfactory neurons expressing identified receptor genes project to subsets of glomeruli within the antennal lobe of Drosophila melanogaster. J Neurobiol 54:577-592.
9. Bieber AJ, Snow PM, Hortsch M, Patel NH, Jacobs JR, Traquina ZR, Schilling J, Goodman CS. 1989. Drosophila neuroglian: a member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell 59:447-460.
10. Borycz J, Borycz JA, Loubani M, Meinertzhagen IA. 2002. Tan and ebony genes regulate a novel pathway for transmitter metabolism at fly photoreceptor terminals. J Neurosci 22:10549-10557.
11. Brown S. 2001. Ultrastructural analysis of activity-dependent volume changes in the antennal lobe of the worker honey bee Apis mellifera. Dissertation, University of Otago, Dunedin, New Zealand.
12. Byrd CA, Burd GD. 1991. Development of the olfactory bulb in the clawed frog, Xenopus laevis: a morphological and quantitative analysis. J Comp Neurol 314:79-90.
13. Campbell G, Goring H, Lin T, Spana E, Andersson S, Doe C, Tomlinson A. 1994. RK2, a glial-specific homeodomain protein required for embryonic nerve cord condensation and viability in Drosophila. Development 120:2957-2966.
14. Chao TI, Kasa P, Wolff JR. 1997. Distribution of astroglia in glomeruli of the rat main olfactory bulb: exclusion from the sensory subcompartment of neuropil. J Comp Neurol 388:191-210.
15. Chiu K, Greer CA. 1996. Immunocytochemical analyses of astrocyte development in the olfactory bulb. Brain Res Dev Brain Res 95:28-37.
16. Chotard C, Salecker I. 2004. Neurons and glia: team players in axon guidance. Trends Neurosci 27:655-661.
17. Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR. 1999. A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327-338.
18. Coles JA. 1989. Functions of glial cells in the retina of the honeybee drone. Glia 2:1-9.
19. Couto A, Alenius M, Dickson BJ. 2005. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535-1547.
20. DeBruyne M, Foster K, Carlson JR. 2001. Odor coding in the Drosophila antenna. Neuron 30:537-552.
21. Devaud J-M, Acebes A, Ramaswami M, Ferrus A. 2003. Structural and functional changes in the olfactory pathway of adult Drosophila take place at a critical age. J Neurobiol 56:13-23.
22. Dubin AE, Harris GL. 1997. Voltage-activated and odor-modulated conductances in olfactory neurons of Drosophila melanogaster. J Neurobiol 32:123-137.
23. Edenfield G, Stork T, Klämbt C. 2005. Neuron-glia interaction in the insect nervous system. Curr Opin Neurobiol 15:34-39.
24. Edwards JS, Tolbert LP. 1998. Insect neuroglia. In: Harrison FW, Locke M, editors. Microscopic anatomy of invertebrates. Vol 11B: Insecta. New York: Wiley-Liss. p 449-466.
25. Endo K, Aoki T, Yoda Y, Kimura K, Hama C. 2007. Notch signal organizes the Drosophila olfactory circuitry by diversifying the sensory neuronal lineages. Nat Neurosci 10:153-159.
26. Ernst KD, Boeckh J. 1983. A neuroanatomical study on the organization of the central antennal pathways in insects. III. Neuroanatomical characterization of physiologically defined response types of deutocerebral neurons in Periplaneta americana. Cell Tissue Res 229:1-22.
27. Ernst KD, Boeckh J, Boeckh V. 1977. A neuroanatomical study on the organization of the central antennal pathways in insects. Cell Tissue Res 176:285-306.
28. Fellin T, Carnignoto G. 2004. Neurone-to-astrocyte signalling in the brain represents a distinct multifunction unit. J Physiol 559:3-15.
29. Fishilevich E, Vosshall LB. 2005. Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15:1548-1553.
30. Freeman MR. 2006. Sculpting the nervous system: glial control of neuronal development. Curr Opin Neurobiol 16:119-125.
31. Freeman MR, Doherty J. 2006. Glial cell biology in Drosophila and vertebrates. Trends Neurosci 29:82-90.
32. Freeman MR, Delrow J, Kim J, Johnson E, Doe CQ. 2003. Unwrapping glial biology: Gem target genes regulating glial development, diversification, and function. Neuron 38:567-580.
33. Gascuel J, Masson C. 1991. Developmental study of afferented and deafferented bee antennal lobes. J Neurobiol 22:795-810.
34. Gibson NJ, Tolbert LP. 2006. Activation of epidermal growth factor receptor mediates receptor axon sorting and extension in the developing olfactory system of the moth Manduca sexta. J Comp Neurol 495:554-552.
35. Godenschwege TA, Reisch D, Diegelmann S, Elberle K, Funk N, Heisenberg M, Hoppe V, Hoppe J, Klagges BRE, Martin J-R, Nikitina EA, Putz G, Reifegerste R, Reisch N, Rister J, Schaupp M, Scholz H, Schwaerzel M, Wernet U, Zars TD, Buchner S, Buchner E. 2004. Flies lacking all synapsins are unexpectedly healthy but are impaired in complex behaviour. Eur J Neurosci 20:611-622.
36. Goriely AR, Secomb TW, Tolbert LP. 2002. Effect of the glial envelope on extracellular K(+) diffusion in olfactory glomeruli. J Neurophysiol 87:1712-1722.
37. 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.
38. Halassa MM, Fellin T, Haydon PG. 2007. The tripartite synapse: roles for gliotransmission in health and disease. Trends in Mol Med 13:54-63.
39. Hall SG, Bieber AJ. 1997. Mutations in the Drosophila neuroglian cell adhesion molecule affect motor neuron pathfinding and peripheral nervous system patterning. J Neurobiol 32:325-340.
40. 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 glia function in the embryonic nervous system of Drosophila melanogaster. Development 121:317-332.
41. Heil JE, Oland LA, Lohr C. 2007. Acetylcholine-mediated axon-glia signaling in the developing insect olfactory system. Eur J Neurosci 26:1227-1241.
42. Hildebrand JG, Montague RA. 1986. Functional organization of olfactory pathways in the central nervous system of Manduca sexta. In: Payne TL, Birch MC, Kennedy CEJ, editors. Mechanisms in insect olfaction. Oxford: Oxford University Press. p 279-285.
43. Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595-631.
44. Homberg U, Christensen TA, Hildebrand JG. 1989. Structure and Function of the deutocerebrum in insects. Annu Rev Ent 34:477-501.
45. Hortsch M, Bieber AJ, Patel NH, Goodman CS. 1990. Differential splicing generates a nervous system-specific form of Drosophila neuroglian. Neuron 4:697-709.
46. Hummel T, Zipursky SL. 2004. Afferent induction of olfactory glomeruli requires N-Cadherin. Neuron 42:77-88.
47. Hummel T, Vasconcelos ML, Clemens JC, Fishilevich Y, Vosshall LB, Zipursky SL. 2003. Axonal targeting of olfactory receptor neurons in Drosophila is controlled by Dscam. Neuron 37:221-231.
48. Ignell R, Anton S, Hansson BS. 2001. The antennal lobe of orthoptera - anatomy and evolution. Brain Behav Evol 57:1-17.
49. 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.
50. Jefferis GS, Marin EC, Stocker RF, Luo L. 2001. Target neuron prespecification in the olfactory map of Drosophila. Nature 414:204-208.
51. Jefferis GS, Vyas RM, Berdnik D, Ramaekers A, Stocker RF, Tanaka NK, Ito K, Luo L. 2004. Developmental origin of wiring specificity in the olfactory system of Drosophila. Development 131:117-130.
52. Jhaveri D, Rodrigues V. 2002. Sensory neurons of the Atonal lineage pioneer the formation of glomeruli within the adult Drosophila olfactory lobe. Development 129:1251-1260.
53. Jhaveri D, Sen A, Rodrigues V. 2000. Mechanisms underlying olfactory neuronal connectivity in Drosophila - the atonal lineage organizes the periphery while sensory neurons and glia pattern the olfactory lobe. Dev Biol 226:73-87.
54. Kaneko M, Nighorn A. 2003. Interaxonal Eph-ephrin signaling may mediate sorting of olfactory sensory axons in Manduca sexta. J Neurosci 23:11523-11538.
55. Kasowski HJ, Kim H, Greer CA. 1999. Compartimentai organization of the olfactory bulb glomerulus. J Comp Neurol 407:261-274.
56. Klagges BR, Heimbeck G, Godenschwege TA, Hofbauer A, Pflugfelder GO, Reifegerste R, Reisch D, Schaupp M, Buchner S, Buchner E. 1996. Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J Neurosci 16:3154-3165.
57. Kofuji P, Newman EA. 2004. Potassium buffering in the central nervous system. Neuroscience 129:1045-1056.
58. Komiyama T, Sweeney LB, Schuldiner O, Garcia KC, Luo L. 2007. Graded expression of semaphorin-1a cell-autonomously directs dendritic targeting of olfactory projection neurons. Cell 128:399-410.
59. Kuffler SW, Nicholls JG, Orkand RK. 1966. Physiological properties of glial cells in the central nervous system of Amphibia. J Neurophys 29:768-787.
60. Laissue PP, Reiter C, Hiesinger PR, Halter S, Fischbach KF, Stocker RF. 1999. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J Comp Neurol 405:543-552.
61. Lienhard MC, Stocker RF. 1991.The development of the sensory neuron pattern in the antennal disc of wild-type and mutant (lz3, ss*) Drosophila melanogaster. Development 112:1063-1075.
62. Lohr C, Deitmer JW. 1999. Dendritic calcium transients in the leech giant glial cell in situ. Glia 26:109-118.
63. MacDonald JM, Beach MG, Porpiglia E, Sheehan AE, Watts RJ, Freeman MR. 2006. The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron 50:869-881.
64. Marin EC, Jefferis GS, Komiyama T, Zhu H, Luo L. 2002. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109:243-255.
65. Marin EC, Watts RJ, Tanaka NK, Ito K, Luo L. 2005. Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 132:725-737.
66. Meinertzhagen IA, O'Neil SD. 1991. Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J Comp Neurol 305:232-263.
67. Nezlin LP, Heermann S, Schild D, Rössler W. 2003. Organization of glomeruli in the main olfactory bulb of Xenopus laevis tadpoles. J Comp Neurol 464:257-268.
68. Oland LA, Evans S. 2000. The tracheal system of the developing primary olfactory pathway of Manduca sexta: trachea do not play a guidance or targeting role for ingrowing receptor axons. Arthropod Struct Dev 29:185-196.
69. Oland LA, Tolbert LP. 2003. Key interactions between neurons and glial cells during neural development in insects. Annu Rev Entomol 48:89-110.
70. Oland LA, Pott WM, Higgins MR, Tolbert LP. 1998. Targeted ingrowth and glial relationships of olfactory receptor axons in the primary olfactory pathway of an insect. J Comp Neurol 398:119-138.
71. 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.
72. Oland LA, Biebelhausen JP, Tolbert LP. 2007. Development of the glial investment of glomeruli in the Drosophila olfactory lobe. Chem Senses (in press).
73. Parker RJ, Auld VJ. 2006. Roles of glia in the Drosophila nervous system. Semin Cell Dev Biol 17:66-77.
74. Pereanu W, Shy D, Hartenstein V. 2005. Morphogenesis and proliferation of the larval brain glia in Drosophila. Dev Biol 283:191-203.
75. Pereanu W, Spindler S, Cruz L, Hartenstein V. 2007. Tracheal development in the Drosophila brain is constrained by glial cells. Dev Biol 302:169-180.
76. Peters A, Palay SL, Webster H deF. 1991. The fine structure of the nervous system. New York: Oxford University Press.
77. Pinching AJ, Powell TP. 1971. The neuropil of the glomeruli of the olfactory bulb. J Cell Sci 9:347-377.
78. Raisman G. 1985. Specialized neuroglial arrangement may explain the capacity of vomeronasal axons to reinnervate central neurons. Neuroscience 14:237-254.
79. Ray K, Rodrigues V. 1995. Cellular events during development of the olfactory sense organs in Drosophila melanogaster. Dev Biol 167:426-438.
80. Read RD, Goodfellow PJ, Mardis ER, Novak N, Armstrong JR, Cagan RL. 2005. A Drosophila model of multiple endocrine neoplasia type 2. Genetics 171:1057-1081.
81. Rössler W, Oland LA, Higgins MR, Hildebrand JG, Tolbert LP. 1999. Development of a glia-rich axon-sorting zone in the olfactory pathway of the moth Manduca sexta. J Neurosci 19:9865-9877.
82. Rössler W, Kuduz J, Schürmann FW, Schild D. 2002. Aggregation of f-actin in olfactory glomeruli: a common feature of glomeruli across phyla. Chem Senses 27:803-810.
83. Roy B, Singh AP, Shetty C, Chaudhary V, North A, Landgraf M, Vijay-Raghavan K, Rodrigues V. 2007. Metamorphosis of an identified serotonergic neuron in the Drosophila olfactory system. Neural Dev 2:20.
84. Schröter U, Malun D. 2000. Formation of antennal lobe and mushroom body neuropils during metamorphosis in the honeybee, Apis mellifera. J Comp Neurol 422:229-245.
85. Seal RP, Daniels GM, Wolfgang WJ, Forte MA, Amara SG. 1998. Identification and characterization of a cDNA encoding a neuronal glutamate transporter from Drosophila melanogaster. Receptors Channels 6:51-64.
86. Sen A, Shetty C, Jhaveri D, Rodrigues V. 2005. Distinct types of glial cells populate the Drosophila antenna. BMC Dev Biol 5:25.
87. Shepherd D, Tyrer NM. 1985. Inhibition of GABA uptake potentiates the effects of exogenous GABA on locust skeletal muscle. Comp Biochem Physiol C 82:315-321.
88. Silbering AF, Galizia CG. 2007. Processing of odor mixtures in the Drosophila antennal lobe reveals both global inhibition and glomerulus-specific interactions. J Neurosci 27:11966-11977.
89. Soustelle L, Besson MT, Rival T, Birman S. 2002. Terminal glial differentiation involves regulated expression of the excitatory amino acid transporters in the Drosophila embryonic CNS. Dev Biol 248:294-306.
90. Stocker RF. 1979. Fine structural comparison of the antennal nerve in the homeotic mutant Antennapedia with the wild-type antennal and second leg nerves of Drosophila melanogaster. J Morphol 160:209-222.
91. Stocker RF, Lienhard MC, Borst A, Fischbach KF. 1990. Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262:9-34.
92. Stocker RF, Tissot M, Gendre N. 1995. Morphogenesis and cellular proliferation pattern in the developing antennal lobe of Drosophila melanogaster. Roux's Arch Dev Biol 205:62-72.
93. Strausfeld NJ. 1976. Atlas of an insect brain. New York: Springer.
94. Sun B, Xu P, Salvaterra PM. 1999. Dynamic visualization of nervous system in live Drosophila. Proc Natl Acad Sci U S A 96:10438-10443.
95. Sun B, Xu P, Wang W, Salvaterra PM. 2001. In vivo modification of Na(+),K(+)-ATPase activity in Drosophila. Comp Biochem Physiol B Biochem Mol Biol 130:521-536.
96. Tissot M, Gendre N, Hawken A, Störtkuhl KF, Stocker RF. 1997. Larval chemosensory projections and invasion of adult afferents in the antennal lobe of Drosophila. J Neurobiol 32:281-297.
97. Tolbert LP. 1989. Afferent axons from the antenna influence the number and placement of intrinsic synapses in the antennal lobes of Manduca sexta. Synapse 3:83-95.
98. Tolbert LP, Hildebrand JG. 1981. Organization and synaptic ultrastructure of glomeruli in the antennal lobes of the moth Manduca sexta: a study using thin sections and freeze-fracture. Proc Roy Soc Lond B 213:279-301.
99. Tolbert LP, Oland LA, Tucker ES, Gibson NJ, Higgins MR, Lipscomb BW. 2004. Bidirectional influences between neurons and glial cells in the developing olfactory system. Prog Neurobiol 73:73-105.
100. Treloar HB, Purcell AL, Greer CA. 1999. Glomerular formation in the developing rat olfactory bulb. J Comp Neurol 413:289-304.
101. Treloar HB, Feinstein P, Mombaerts P, Greer CA. 2002. Specificity of glomerular targeting by olfactory sensory axons. J Neurosci 22:2469-2477.
102. Tsacopoulos M, Magistretti PJ. 1996. Metabolic coupling-between glia and neurons. J Neurosci 16:877-885.
103. Tsacopoulos M, Evequoz-Mercier V, Perrottet P, Buchner E. 1988. Honeybee retinal glial cells transform glucose and supply the neurons with metabolic substrate. Proc Natl Acad Sci U S A 85:8727-8731.
104. Tsacopoulos M, Veuthey AL, Saravelos SG, Perrottet P, Tsoupras G. 1994. Glial cells transform glucose to alanine, which fuels the neurons in the honeybee retina. J Neurosci 14:1339-1351.
105. Valverde F. 1999. Building an olfactory glomerulus. J Comp Neurol 415:419-422.
106. Valverde F, Lopez-Mascaraque L. 1991. Neuroglial arrangements in the olfactory glomeruli of the hedgehog. J Comp Neurol 307:658-674.
107. Valverde F, Santacana M, Heredia M. 1992. Formation of an olfactory glomerulus: morphological aspects of development and organization. Neuroscience 49:255-275.
108. Vickers NJ, Poole K, Linn CE Jr. 2003. Consequences of interspecies antennal imaginai disc transplantation on organization of olfactory glomeruli and pheromone blend discrimination. J Comp Neurol 466:377-388.
109. Wang JW, Wong AM, Flores J, Vosshall LB, Axel R. 2003. Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112:271-282.
110. Willey TJ. 1973. The ultrastructure of the cat olfactory bulb. J Comp Neurol 152:211-232.
111. Xiong W-C, Okano H, Patel NH, Blendy JA, Montell C. 1994. Repo encodes a glial-specific homeo-domain protein required in the Drosophila nervous system. Genes Dev 8:981-994.
112. Yao Y, Wu Y, Yin C, Ozawa R, Aigaki T, Wouda RR, Noordermeer JN, Fradkin LG, Hing H. 2007. Antagonistic roles of Wnt5 and the Drl receptor in patterning the Drosophila antennal lobe. Nat Neurosci 10:1423-1432.