Crucial roles of Pox neuro in the developing ellipsoid body and antennal lobes of the Drosophila brain

PLoS ONE

Volumn 12, Issue 4, 2017, Pages

  Minocha, Shilpi ^a,b   Boll, Werner ^a   Noll, Markus ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AXON; BRAIN; BRDU ASSAY; CELL BODY; DIFFERENTIATION; DORSAL REGION; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; HUMAN; HUMAN CELL; INTERNEURON; LARVAL STAGE; METAMORPHOSIS; MUSHROOM BODY; NERVE CELL CULTURE; NEURITE; NEUROPIL; NONHUMAN; SPINAL CORD LATERAL HORN; ANIMAL; CYTOLOGY; DROSOPHILA MELANOGASTER; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; MALE; METABOLISM; MUTATION; NERVE CELL;

DROSOPHILA PROTEIN; NERVE PROTEIN; PAIRED BOX TRANSCRIPTION FACTOR; POXN PROTEIN, DROSOPHILA;

ANIMALS; BRAIN; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LARVA; MALE; MUTATION; NERVE TISSUE PROTEINS; NEURONS; PAIRED BOX TRANSCRIPTION FACTORS;

EID: 85018806678     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0176002     Document Type: Article

References (116)

1. Truman JW (1990) Metamorphosis of the central nervous system of Drosophila. J Neurobiol 21: 1072-1084. https://doi.org/10.1002/neu.480210711 PMID: 1979610
2. Ito K, Hotta Y (1992) Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Dev Biol 149: 134-148. PMID: 1728583
3. Levine RB, Morton DB, Restifo LL (1995) Remodeling of the insect nervous system. Curr Opin Neurobiol 5: 28-35. PMID: 7773002
4. Consoulas C, Duch C, Bayline RJ, Levine RB (2000) Behavioral transformations during metamorphosis: Remodeling of neural and motor systems. Brain Res Bull 53: 571-583. PMID: 11165793
5. Consoulas C, Restifo LL, Levine RB (2002) Dendritic remodeling and growth of motoneurons during metamorphosis of Drosophila melanogaster. J Neurosci 22: 4906-4917. PMID: 12077188
6. Tissot M, Stocker RF (2000) Metamorphosis in Drosophila and other insects: the fate of neurons throughout the stages. Prog Neurobiol 62: 89-111. PMID: 10821983
7. Marin EC, Watts RJ, Tanaka NK, Ito K, Luo L (2005) Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 132: 725-737. https://doi.org/10.1242/dev.01614 PMID: 15659487
8. Power ME (1943) The brain of Drosophila melanogaster. J Morphol 72: 517-559.
9. Homberg U (1987) Structure and functions of the central complex in insects. In Arthropod brain: its evolution, development, structure, and functions (Gupta AP, ed), pp. 347-367. New York: Wiley & Sons.
10. Hanesch U, Fischbach K-F, Heisenberg M (1989) Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res 257: 343-366.
11. Strausfeld NJ (1999) A brain region in insects that supervises walking. Prog Brain Res 123: 273-284. PMID: 10635723
12. Loesel R, Nässel DR, Strausfeld NJ (2002) Common design in a unique midline neuropil in the brains of arthropods. Arthropod Struct Dev 31: 77-91. https://doi.org/10.1016/S1467-8039(02)00017-8 PMID: 18088972
13. Homberg U (2008) Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct Dev 37: 347-362. https://doi.org/10.1016/j.asd.2008.01.008 PMID: 18502176
14. Renn SCP, Armstrong JD, Yang M, Wang Z, An X, Kaiser K, et al. (1999) Genetic analysis of the Drosophila ellipsoid body neuropil: organization and development of the central complex. J Neurobiol 41: 189-207. PMID: 10512977
15. Stocker RF, Lienhard MC, Borst A, Fischbach K-F (1990) Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262: 9-34. PMID: 2124174
16. Stocker RF, Heimbeck G, Gendre N, de Belle JS (1997) Neuroblast ablation in Drosophila P[GAL4] lines reveals origins of olfactory interneurons. J Neurobiol 32: 443-456. PMID: 9110257
17. Ito K, Sass H, Urban J, Hofbauer A, Schneuwly S (1997) GAL4-responsive UAS-tau as a tool for studying the anatomy and development of the Drosophila central nervous system. Cell Tissue Res 290: 1-10. PMID: 9377629
18. Lai S-L, Awasaki T, Ito K, Lee T (2008) Clonal analysis of Drosophila antennal lobe neurons: diverse neuronal architectures in the lateral neuroblast lineage. Development 135: 2883-2893. https://doi.org/10.1242/dev.024380 PMID: 18653555
19. Boll W, Noll M (2002) The Drosophila Pox neuro gene: control of male courtship behavior and fertility as revealed by a complete dissection of all enhancers. Development 129: 5667-5681. PMID: 12421707
20. Bopp D, Jamet E, Baumgartner S, Burri M, Noll M (1989) Isolation of two tissue-specific Drosophila paired box genes, Pox meso and Pox neuro. EMBO J 8: 3447-3457. PMID: 2573516
21. Noll M (1993) Evolution and role of Pax genes. Curr Opin Genet Dev 3: 595-605. PMID: 8241771
22. Dambly-Chaudière C, Jamet E, Burri M, Bopp D, Basler K, Hafen E, et al. (1992) The paired box gene pox neuro: a determinant of poly-innervated sense organs in Drosophila. Cell 69: 159-172. PMID: 1348214
23. Awasaki T, Kimura K-i (1997) pox neuro is required for development of chemosensory bristles in Drosophila. J Neurobiol 32: 707-721. PMID: 9183748
24. Awasaki T, Kimura K-i (2001) Multiple function of poxn gene in larval PNS development and in adult appendage formation of Drosophila. Dev Genes Evol 211: 20-29. PMID: 11277402
25. Krstic D, Boll W, Noll M (2009) Sensory integration regulating male courtship behavior in Drosophila. PLoS ONE 4: e4457. https://doi.org/10.1371/journal.pone.0004457 PMID: 19214231
26. Jiang Y, Boll W, Noll M (2015) Pox neuro control of cell lineages that give rise to larval poly-innervated external sensory organs in Drosophila. Dev Biol 397:162-174. https://doi.org/10.1016/j.ydbio.2014. 10.013 PMID: 25446278
27. Tanaka NK, Endo K, Ito K (2012) Organization of antennal lobe-associated neurons in adult Drosophila melanogaster brain. J Comp Neurol 520: 4067-4130. https://doi.org/10.1002/cne.23142 PMID: 22592945
28. Jefferis GSXE, Marin EC, Stocker RF, Luo L (2001) Target neuron prespecification in the olfactory map of Drosophila. Nature 414: 204-208. https://doi.org/10.1038/35102574 PMID: 11719930
29. Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451-461. PMID: 10197526
30. Bainbridge SP, BownesM (1981) Staging the metamorphosis of Drosophila melanogaster. J Embryol Exp Morphol 66: 57-80. PMID: 6802923
31. Ramaekers A, Magnenat E, Marin EC, Gendre N, Jefferis GSXE, Luo L, et al. (2005) Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr Biol 15: 982-992. https://doi.org/10.1016/j.cub.2005.04.032 PMID: 15936268
32. Bearer EL (2003) Overview of image analysis, image importing, and image processing using freeware. Curr Protoc Mol Biol 14.15: 1-9.
33. Eliceiri KW, Rueden C (2005) Tools for visualizing multidimensional images from living specimens. Photochem Photobiol 81: 1116-1122. https://doi.org/10.1562/2004-11-22-IR-377 PMID: 15807634
34. Carmona R, Macías D, Guadix JA, Portillo V, Pérez-Pomares JM, Muñoz-Chápuli R (2007) A simple technique of image analysis for specific nuclear immunolocalization of proteins. J Microsc 225: 96-99. https://doi.org/10.1111/j.1365-2818.2007.01719.x PMID: 17286699
35. Collins TJ (2007) ImageJ for microscopy. BioTechniques 43 Suppl: 25-30.
36. Lachmanovich E, Shvartsman DE, Malka Y, Botvin C, Henis YI, Weiss AM (2003) Co-localization analysis of complex formation among membrane proteins by computerized fluorescence microscopy: application to immunofluorescence co-patching studies. J Microsc 212: 122-131. PMID: 14629561
37. Truman JW, Bate M (1988) Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev Biol 125: 145-157. PMID: 3119399
38. McGuire SE, Le PT, Osborn AJ, Matsumoto K, Davis RL (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302: 1765-1768. https://doi.org/10.1126/science.1089035 PMID: 14657498
39. McGuire SE, Mao Z, Davis RL (2004) Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci STKE 2004: pI6.
40. Komiyama T, Johnson WA, Luo L, Jefferis GSXE (2003) From lineage to wiring specificity: POU domain transcription factors control precise connections of Drosophila olfactory projection neurons. Cell 112: 157-167. PMID: 12553905
41. Urbach R (2007) A procephalic territory in Drosophila exhibiting similarities and dissimilarities compared to the vertebrate midbrain/hindbrain boundary region. Neural Dev 2: 23. https://doi.org/10.1186/1749-8104-2-23 PMID: 17983473
42. Hirth F, Kammermeier L, Frei E, Walldorf U, Noll M, Reichert H (2003) An urbilaterian origin of the tripartite brain: developmental genetic insights from Drosophila. Development 130: 2365-2373. PMID: 12702651
43. Robinow S, White K (1988) The locus elav of Drosophila melanogaster is expressed in neurons at all developmental stages. Dev Biol 126: 294-303. PMID: 3127258
44. 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. PMID: 7926782
45. Halter DA, Urban J, Rickert C, Ner SS, Ito K, Travers AA, et al. (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. PMID: 7768175
46. Chu-Lagraff Q, Wright DM, McNeil LK, Doe CQ (1991) The prospero gene encodes a divergent homeodomain protein that controls neuronal identity in Drosophila. Development Suppl 2: 79-85.
47. Li L, Vaessin H (2000) Pan-neural Prospero terminates cell proliferation during Drosophila neurogenesis. Genes Dev 14: 147-151. PMID: 10652268
48. Choksi SP, Southall TD, Bossing T, Edoff K, de Wit E, Fischer BE, et al. (2006) Prospero acts as a binary switch between self-renewal and differentiation in Drosophila neural stem cells. Dev Cell 11: 775-789. https://doi.org/10.1016/j.devcel.2006.09.015 PMID: 17141154
49. Colonques J, Ceron J, Reichert H, Tejedor FJ (2011) A transient expression of prospero promotes cell cycle exit of Drosophila postembryonic neurons through the regulation of dacapo. PLoS ONE 6: e19342. https://doi.org/10.1371/journal.pone.0019342 PMID: 21552484
50. Doe CQ, Chu-LaGraff Q, Wright DM, Scott MP (1991) The prospero gene specifies cell fates in the Drosophila central nervous system. Cell 65: 451-464. PMID: 1673362
51. Vaessin H, Grell E, Wolff E, Bier E, Jan LY, Jan YN (1991) prospero is expressed in neuronal precursors and encodes a nuclear protein that is involved in the control of axonal outgrowth in Drosophila. Cell 67: 941-953. PMID: 1720353
52. Maurange C, Cheng L, Gould AP (2008) Temporal transcription factors and their targets schedule the end of neural proliferation in Drosophila. Cell 133: 891-902. https://doi.org/10.1016/j.cell.2008.03.034 PMID: 18510932
53. Woods DF, Bryant PJ (1991) The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66: 451-464. PMID: 1651169
54. Zito K, Fetter RD, Goodman CS, Isacoff EY (1997) Synaptic clustering of Fasciclin II and Shaker: essential targeting sequences and role of Dlg. Neuron 19: 1007-1016. PMID: 9390515
55. Masuda-Nakagawa LM, Tanaka NK, O'Kane CJ (2005) Stereotypic and random patterns of connectivity in the larval mushroom body calyx of Drosophila. Proc Natl Acad Sci USA 102: 19027-19032. https://doi.org/10.1073/pnas.0509643102 PMID: 16357192
56. Grenningloh G, Rehm EJ, Goodman CS (1991) Genetic analysis of growth cone guidance in Drosophila: Fasciclin II functions as a neuronal recognition molecule. Cell 67: 45-57. PMID: 1913818
57. Nassif C, Noveen A, Hartenstein V (2003) Early development of the Drosophila brain: III. The pattern of neuropile founder tracts during the larval period. J Comp Neurol 455: 417-434. https://doi.org/10.1002/cne.10482 PMID: 12508317
58. Hofbauer A (1991) Eine Bibliothek monoklonaler Antikörper gegen das Gehirn von Drosophila melanogaster. Habilitation thesis. University of Würzburg, Würzburg, Germany.
59. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, Dürrbeck H, et al. (2006) Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 49: 833-844. https://doi.org/10.1016/j.neuron.2006.02.008 PMID: 16543132
60. Jefferis GSXE, Vyas RM, Berdnik D, Ramaekers A, Stocker RF, Tanaka NK, et al. (2004) Developmental origin of wiring specificity in the olfactory system of Drosophila. Development 131: 117-130. https://doi.org/10.1242/dev.00896 PMID: 14645123
61. Young JM, Armstrong JD (2010) Structure of the adult central complex in Drosophila: organization of distinct neuronal subsets. J Comp Neurol 518: 1500-1524. https://doi.org/10.1002/cne.22284 PMID: 20187142
62. 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. https://doi.org/10.1523/JNEUROSCI.4708-05.2006 PMID: 16707805
63. Larsen C, Shy D, Spindler SR, Fung S, Pereanu W, Younossi-Hartenstein A, et al. (2009) Patterns of growth, axonal extension and axonal arborization of neuronal lineages in the developing Drosophila brain. Dev Biol 335: 289-304. https://doi.org/10.1016/j.ydbio.2009.06.015 PMID: 19538956
64. Pereanu W, Kumar A, Jennett A, Reichert H, Hartenstein V (2010) Development-based compartmentalization of the Drosophila central brain. J Comp Neurol 518: 2996-3023. https://doi.org/10.1002/cne.22376 PMID: 20533357
65. Nassif C, Noveen A, Hartenstein V (1998) Embryonic development of the Drosophila brain. I. Pattern of pioneer tracts. J Comp Neurol 402: 10-31. PMID: 9831043
66. Younossi-Hartenstein A, Salvaterra PM, Hartenstein V (2003) Early development of the Drosophila brain: IV. Larval neuropile compartments defined by glial septa. J Comp Neurol 455: 435-450. https://doi.org/10.1002/cne.10483 PMID: 12508318
67. Younossi-Hartenstein A, Nguyen B, Shy D, Hartenstein V (2006) Embryonic origin of the Drosophila brain neuropile. J Comp Neurol 497: 981-998. https://doi.org/10.1002/cne.20884 PMID: 16802336
68. Python F, Stocker RF (2002) Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons. J Comp Neurol 445: 374-387. PMID: 11920714
69. Python F, Stocker RF (2002) Immunoreactivity against choline acetyltransferase, γ- aminobutyric acid, histamine, octopamine, and serotonin in the larval chemosensory system of Drosophila melanogaster. J Comp Neurol 453: 157-167. https://doi.org/10.1002/cne.10383 PMID: 12373781
70. Younossi-Hartenstein A, Nassif C, Green P, Hartenstein V (1996) Early neurogenesis of the Drosophila brain. J Comp Neurol 370: 313-329. PMID: 8799858
71. Urbach R, Schnabel R, Technau GM (2003) The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development 130: 3589-3606. PMID: 12835378
72. Urbach R, Technau GM (2003) Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 130: 3621-3637. PMID: 12835380
73. Prokop A, Technau GM (1991) The origin of postembryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster. Development 111: 79-88. PMID: 1901786
74. Das A, Gupta T, Davla S, Prieto-Godino LL, Diegelmann S, Reddy OV, et al. (2013) Neuroblast lineage- specific origin of the neurons of the Drosophila larval olfactory system. Dev Biol 373: 322-337. https://doi.org/10.1016/j.ydbio.2012.11.003 PMID: 23149077
75. Truman JW (1996) Steroid receptors and nervous system metamorphosis in insects. Dev Neurosci 18: 87-101. PMID: 8840088
76. Zhou B, Williams DW, Altman J, Riddiford LM, Truman JW (2009) Temporal patterns of broad isoform expression during the development of neuronal lineages in Drosophila. Neural Dev 4:39. https://doi.org/10.1186/1749-8104-4-39 PMID: 19883497
77. Spindler SR, Hartenstein V (2010) The Drosophila neural lineages: a model system to study brain development and circuitry. Dev Genes Evol 220: 1-10. https://doi.org/10.1007/s00427-010-0323-7 PMID: 20306203
78. Ceron J, González C, Tejedor FJ (2001) Patterns of cell division and expression of asymmetric cell fate determinants in postembryonic neuroblast lineages of Drosophila. Dev Biol 230: 125-138. https://doi.org/10.1006/dbio.2000.0110 PMID: 11161567
79. Zhu S, Lin S, Kao C-F, Awasaki T, Chiang A-S, Lee T (2006) Gradients of the Drosophila Chinmo BTB-zinc finger protein govern neuronal temporal identity. Cell 127: 409-422. https://doi.org/10.1016/j.cell.2006.08.045 PMID: 17055440
80. Wong AM, Wang JW, Axel R (2002) Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109: 229-241. PMID: 12007409
81. Marin EC, Jefferis GSXE, Komiyama T, Zhu H, Luo L (2002) Representation of the glomerular olfactory map in the Drosophila brain. Cell 109: 243-255. PMID: 12007410
82. Okada R, Awasaki T, Ito K (2009) Gamma-aminobutyric acid (GABA)-mediated neural connections in the Drosophila antennal lobe. J Comp Neurol 514: 74-91. https://doi.org/10.1002/cne.21971 PMID: 19260068
83. Shang Y, Claridge-Chang A, Sjulson L, Pypaert M, Miesenböck G (2007) Excitatory local circuits and their implications for olfactory processing in the fly antennal lobe. Cell 128: 601-612. https://doi.org/10.1016/j.cell.2006.12.034 PMID: 17289577
84. Chou Y-H, Spletter ML, Yaksi E, Leong JCS, Wilson RI, Luo L (2010) Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nature Neurosci 13: 439-449. https://doi.org/10.1038/nn.2489 PMID: 20139975
85. Das A, Chiang A, Davla S, Priya R, Reichert H, Raghavan KV, et al. (2011) Identification and analysis of a glutamatergic local interneuron lineage in the adult Drosophila olfactory system. Neur Sys Circ 1:4.
86. Hartenstein V, Rudloff E, Campos-Ortega JA (1987) The pattern of proliferation of the neuroblasts in the wild-type embryo of Drosophila melanogaster. Roux's Arch Dev Biol 196: 473-485.
87. Lin S, Lai S-L, Yu H-H, Chihara T, Luo L, Lee T (2010) Lineage-specific effects of Notch/Numb signaling in postembryonic development of the Drosophila brain. Development 137: 43-51. https://doi.org/10.1242/dev.041699 PMID: 20023159
88. Das A, Sen S, Lichtneckert R, Okada R, Ito K, Rodrigues V, et al. (2008) Drosophila olfactory local interneurons and projection neurons derive from a common neuroblast lineage specified by the empty spiracles gene. Neural Dev 3:33. https://doi.org/10.1186/1749-8104-3-33 PMID: 19055770
89. Wolff T, Iyer NA, Rubin GM (2015) Neuroarchitecture and neuroanatomy of the Drosophila central complex: a GAL4-based dissection of protocerebral bridge neurons and circuits. J Comp Neurol 523: 997-1037. https://doi.org/10.1002/cne.23705 PMID: 25380328
90. Martín-Peña A, Acebes A, Rodríguez J-R, Chevalier V, Casas-Tinto S, Triphan T, et al. (2014) Cell types and coincident synapses in the ellipsoid body of Drosophila. Eur J Neurosci 39:1586-1601. https://doi.org/10.1111/ejn.12537 PMID: 24605774
91. Truman JW, Moats W, Altman J, Marin EC, WilliamsDW(2010) Role of Notch signaling in establishing the hemilineages of secondary neurons in Drosophila melanogaster. Development 137: 53-61. https://doi.org/10.1242/dev.041749 PMID: 20023160
92. Ito M, Masuda N, Shinomiya K, Endo K, Ito K (2013) Systematic analysis of neural projections reveals clonal composition of the Drosophila brain. Curr Biol 23: 644-655. https://doi.org/10.1016/j.cub.2013. 03.015 PMID: 23541729
93. 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. PMID: 9043058
94. Lovick JK, Ngo KT, Omoto JJ, Wong DC, Nguyen JD, Hartenstein V (2013) Postembryonic lineages of the Drosophila brain: I. Development of the lineage-associated fiber tracts. Dev. Biol. 384: 228-257. https://doi.org/10.1016/j.ydbio.2013.07.008 PMID: 23880429
95. Wong DC, Lovick JK, Ngo KT, Borisuthirattana W, Omoto JJ, Hartenstein V (2013) Postembryonic lineages of the Drosophila brain: II. Identification of lineage projection patterns based on MARCM clones. Dev. Biol. 384: 258-289. https://doi.org/10.1016/j.ydbio.2013.07.009 PMID: 23872236
96. Yang JS, Awasaki T, Yu H-H, He Y, Ding P, Kao J-C, Lee T (2013) Diverse neuronal lineages make stereotyped contributions to the Drosophila locomotor control center, the central complex. J Comp Neurol 521: 2645-2662. https://doi.org/10.1002/cne.23339 PMID: 23696496
97. Yu H-H, Awasaki T, Schroeder MD, Long F, Yang JS, He Y, et al. (2013) Clonal development and organization of the adult Drosophila central brain. Curr Biol 23: 633-643. https://doi.org/10.1016/j.cub.2013.02.057 PMID: 23541733
98. Spindler SR, Hartenstein V (2011) Bazooka mediates secondary axon morphology in Drosophila brain lineages. Neural Dev 6:16. https://doi.org/10.1186/1749-8104-6-16 PMID: 21524279
99. Dumstrei K, Wang F, Nassif C, Hartenstein V (2003) Early development of the Drosophila brain: V. Pattern of postembryonic neuronal lineages expressing DE-cadherin. J Comp Neurol 455: 451-562. https://doi.org/10.1002/cne.10484 PMID: 12508319
100. Komiyama T, Luo L (2007) Intrinsic control of precise dendritic targeting by an ensemble of transcription factors. Curr Biol 17: 278-285. https://doi.org/10.1016/j.cub.2006.11.067 PMID: 17276922
101. Zhu H, Hummel T, Clemens JC, Berdnik D, Zipursky SL, Luo L (2006) Dendritic patterning by Dscam and synaptic partner matching in the Drosophila antennal lobe. Nature Neurosc 9: 349-355.
102. Wilson RI, Laurent G (2005) Role of GABAergic inhibition in shaping odor-evoked spatiotemporal patterns in the Drosophila antennal lobe. J Neurosci 25: 9069-9079. https://doi.org/10.1523/JNEUROSCI.2070-05.2005 PMID: 16207866
103. Jefferis GSXE, Potter CJ, Chan AM, Marin EC, Rohlfing T, Maurer CR Jr, Luo L (2007) Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128: 1187-1203. https://doi.org/10.1016/j.cell.2007.01.040 PMID: 17382886
104. Strausfeld NJ (1998) Crustacean - insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates. Brain Behav Evol 52: 186-206. PMID: 9787219
105. Martin J-R, Faure P, Ernst R (2001) The power law distribution for walking-time intervals correlates with the ellipsoid-body in Drosophila.
106. Strauss R, Heisenberg M (1993) A higher control center of locomotor behavior in the Drosophila brain. J Neurosci 13: 1852-1861. PMID: 8478679
107. 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. PMID: 7965387
108. Strauss R (2002) The central complex and the genetic dissection of locomotor behaviour. Curr Opin Neurobiol 12: 633-638. PMID: 12490252
109. Neuser K, Triphan T, Mronz M, Poeck B, Strauss R (2008) Analysis of a spatial orientation memory in Drosophila. Nature 453: 1244-1247. https://doi.org/10.1038/nature07003 PMID: 18509336
110. Kuntz S, Poeck B, Sokolowski MB, Strauss R (2012) The visual orientation memory of Drosophila requires Foraging (PKG) upstream of Ignorant (RSK2) in ring neurons of the central complex. Learn Mem 19: 337-340. https://doi.org/10.1101/lm.026369.112 PMID: 22815538
111. Thran J, Poeck B, Strauss R (2013) Serum Response Factor-mediated gene regulation in a Drosophila visual working memory. Curr Biol 23: 1756-1763. https://doi.org/10.1016/j.cub.2013.07.034 PMID: 24012317
112. 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 Tiss Res 288: 159-176.
113. Homberg U, Vitzthum H, Müller M, Binkle U (1999) Immunocytochemistry of GABA in the central complex of the locust Schistocerca gregaria: identification of immunoreactive neurons and colocalization with neuropeptides. J Comp Neurol 409: 495-507. PMID: 10379833
114. Strausfeld NJ (2009) Brain organization and the origin of insects: an assessment. Proc R Soc B 276: 1929-1937. https://doi.org/10.1098/rspb.2008.1471 PMID: 19324805
115. 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 176: 67-86.
116. Jäger RF, Fischbach KF (1987) Some improvements of the Heisenberg-Böhl method for mass histology of Drosophila heads. Dros Inf Serv 66: 162-165.