Postembryonic lineages of the Drosophila brain: I. Development of the lineage-associated fiber tracts

Developmental Biology

Volumn 384, Issue 2, 2013, Pages 228-257

  Lovick, Jennifer K ^a   Ngo, Kathy T ^a   Omoto, Jaison J ^a   Wong, Darren C ^a   Nguyen, Joseph D ^a   Hartenstein, Volker ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain; Circuitry; Drosophila; Lineage; Mapping; Metamorphosis

Indexed keywords

FRACTALKINE; NERVE CELL ADHESION MOLECULE;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; CELL LINEAGE; CONTROLLED STUDY; DROSOPHILA; LARVAL DEVELOPMENT; LARVAL STAGE; METAMORPHOSIS; NERVE FIBER; NEUROBLAST; NEUROPIL; NONHUMAN; PRIORITY JOURNAL; PUPATION;

EID: 84887610279     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.07.008     Document Type: Article

References (114)

1. Ashburner M. Drosophila. A Laboratory Manual 1989, 214-217. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. Bate C.M. Embryogenesis of an insect nervous system I. A map of the thoracic and abdominal neuroblasts in Locusta migratoria. J. Embryol. Exp. 1976, 35:107-123.
3. Bausenwein B., Dittrich A.P., Fischbach K.F. The optic lobe of Drosophila melanogaster. II. Sorting of retinotopic pathways in the medulla. Cell Tissue Res. 1992, 267:17-28.
4. Bayraktar O.A., Boone J.Q., Drummond M.L., Doe C.Q. Drosophila type II neuroblast lineages keep Prospero levels low to generate large clones that contribute to the adult brain central complex. Neural Dev. 2010, 5:26.
5. Bello B.C., Izergina N., Caussinus E., Reichert H. Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural Dev. 2008, 3:5.
6. Bieber A.J., Snow P.M., Hortsch M., Patel N.H., Jacobs J.R., Traquina Z.R., Schilling J., Goodman C.S. Drosophila neuroglian: a member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell 1989, 59:447-460.
7. Booker R., Truman J.W. Postembryonic neurogenesis in the CNS of the tobacco hornworm, Manduca sexta. I. Neuroblast arrays and the fate of their progeny during metamorphosis. Journal of Comparative Neurology 1987, 255:548-559.
8. Boone J.Q., Doe C.Q. Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells. Dev. Neurobiol. 2008, 68:1185-1195.
9. Bossing T., Udolph G., Doe C.Q., Technau G.M. The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Dev. Biol. 1996, 179:41-64.
10. Boyan G., Reichert H., Hirth F. Commissure formation in the embryonic insect brain. Arthropod Struct. Dev. 2003, 32:61-77.
11. Boyan G.S., Ball E.E. The grasshopper, Drosophila and neuronal homology (advantages of the insect nervous system for the neuroscientist). Prog. Neurobiol. 1993, 41:657-682.
12. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
13. Brand A.H., Livesey F.J. Neural stem cell biology in vertebrates and invertebrates: more alike than different?. Neuron 2011, 70:719-729.
14. Broadus J., Skeath J.B., Spana E.P., Bossing T., Technau G., Doe C.Q. New neuroblast markers and the origin of the aCC/pCC neurons in the Drosophila central nervous system. Mech. Dev. 1995, 53:393-402.
15. Cardona A., Saalfeld S., Arganda I., Pereanu W., Schindelin J., Hartenstein V. Identifying neuronal lineages of Drosophila by sequence analysis of axon tracts. J. Neurosci. 2010, 30:7538-7553.
16. Cardona A., Saalfeld S., Preibisch S., Schmid B., Cheng A., Pulokas J., Tomancak P., Hartenstein V. An integrated micro- and macroarchitectural analysis of the Drosophila brain by computer-assisted serial section electron microscopy. PLoS Biol. 2010, 8:e1000502.
17. Cardona A., Saalfeld S., Schindelin J., Arganda-Carreras I., Preibisch S., Longair M., Tomancak P., Hartenstein V., Douglas R.J. TrakEM2 software for neural circuit reconstruction. PLoS One 2012, 7:e38011.
18. Chang T., Younossi-Hartenstein A., Hartenstein V. Development of neural lineages derived from the sine oculis positive eye field of Drosophila. Arthropod Struct. Dev. 2003, 2003:303-317.
19. Chen J.S., Chen M.G. Modification of the Bodian technique applied to insect nerves. Stain Technol. 1969, 44:50-51.
20. Chiang A.S., Lin C.Y., Chuang C.C., Chang H.M., Hsieh C.H., Yeh C.W., Shih C.T., Wu J.J., Wang G.T., Chen Y.C., Wu C.C., Chen G.Y., Ching Y.T., Lee P.C., Lin C.Y., Lin H.H., Wu C.C., Hsu H.W., Huang Y.A., Chen J.Y., Chiang H.J., Lu C.F., Ni R.F., Yeh C.Y., Hwang J.K. Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr. Biol. 2011, 21:1-11.
21. Crittenden J.R., Skoulakis E.M., Han K.A., Kalderon D., Davis R.L. Tripartite mushroom body architecture revealed by antigenic markers. Learn. Memory 1998, 5:38-51.
22. Das A., Sen S., Lichtneckert R., Okada R., Ito K., Rodrigues V., Reichert H. Drosophila olfactory local interneurons and projection neurons derive from a common neuroblast lineage specified by the empty spiracles gene. Neural Dev. 2008, 3:33.
23. Das A., Gupta T., Davla S., Prieto-Godino L.L., Diegelmann S., Reddy O.V., Raghavan K.V., Reichert H., Lovick J., Hartenstein V. Neuroblast lineage-specific origin of the neurons of the Drosophila larval olfactory system. Dev. Biol. 2013, 373:322-337.
24. de la Escalera S., Bockamp E.O., Moya F., Piovant M., Jiménez F. Characterization and gene cloning of neurotactin, a Drosophila transmembrane protein related to cholinesterases. EMBO J. 1990, 9:3593-3601.
25. Doe C.Q. Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system. Development 1992, 116:855-863.
26. Doe C.Q., Goodman C.S. Early events in insect neurogenesis. I. Development and segmental differences in the pattern of neuronal precursor cells. Dev. Biol. 1985, 111:193-205.
27. Dreyer D., Vitt H., Dippel S., Goetz B., El Jundi B., Kollmann M., Huetteroth W., Schachtner J. 3D standard brain of the red flour beetle Tribolium Castaneum: a tool to study metamorphic development and adult plasticity. Front. Syst. Neurosci. 2010, 4:1-13.
28. Duman-Scheel M., Patel N.H. Analysis of molecular marker expression reveals neuronal homology in distantly related arthropods. Development 1999, 126:2327-2334.
29. Dumstrei K., Wang F., Nassif C., Hartenstein V. Early development of the Drosophila brain: V. Pattern of postembryonic neuronal lineages expressing DE-cadherin. J. Comp. Neurol. 2003, 455:451-462.
30. Dumstrei K., Wang F., Hartenstein V. Role of DE-cadherin in neuroblast proliferation, neural morphogenesis, and axon tract formation in Drosophila larval brain development. J. Neurosci. 2003, 23:3325-3335.
31. Farris S.M. Evolution of insect mushroom bodies: old clues, new insights. Arthropod Struct. Dev. 2005, 34:211-234.
32. Fischbach K.F., Dittrich A.P.M. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res. 1989, 258:441-475.
33. Fung S., Wang F., Spindler S.R., Hartenstein V. Drosophila E-cadherin and its binding partner Armadillo/beta-catenin are required for axonal pathway choices in the developing larval brain. Dev. Biol. 2009, 332:371-382.
34. Galizia C.G., Rossler W. Parallel olfactory systems in insects: anatomy and function. Annu. Rev. Entomol. 2010, 55:399-420.
35. Hanesch U., Fischbach K.F., Heisenberg M. Neuronal architecture of the central complex in Drosophila melanogaster. Cell Tissue Res. 1989, 257:343-366.
36. Hartenstein V., Campos-Ortega J.A. Early neurogenesis in wild-type Drosophila melanogaster. Roux's Arch. Dev. Biol. 1984, 193:308-325.
37. Hartenstein V., Spindler S., Pereanu W., Fung S. The development of the Drosophila larval brain. Adv. Exp. Med. Biol. 2008, 628:1-31.
38. Hassan B.A., Bermingham N.A., He Y., Sun Y., Jan Y.N., Zoghbi H.Y., Bellen H.J. atonal regulates neurite arborization but does not act as a proneural gene in the Drosophila brain. Neuron 2000, 25:549-561.
39. Helfrich-Förster C., Shafer O.T., Wülbeck C., Grieshaber E., Rieger D., Taghert P. Development and morphology of the clock-gene-expressing lateral neurons of Drosophila melanogaster. J. Comp. Neurol. 2007, 500:47-70.
40. Homberg U. Evolution of the central complex in the arthropod brain with respect to the visual system. Arthropod Struct. Dev. 2008, 37:347-362.
41. Hortsch M., Patel N.H., Bieber A.J., Traquina Z.R., Goodman C.S. Drosophila neurotactin, a surface glycoprotein with homology to serine esterases is dynamically expressed during embryogenesis. Development 1990, 110:1327-1340.
42. Huetteroth W., El Jundi B., El Jundi S., Schachtner J. 3D-reconstructions and virtual 4D-visualization to study metamorphic brain development in the sphinx moth Manduca sexta. Front Syst. Neurosci. 2010, 4:1-15.
43. Huser A., Rohwedder A., Apostolopoulou A.A., Widmann A., Pfitzenmaier J.E., Maiolo E.M., Selcho M., Pauls D., von Essen A., Gupta T., Sprecher S.G., Birman S., Riemensperger T., Stocker R.F., Thum A.S. The serotonergic central nervous system of the Drosophila larva: anatomy and behavioral function. PLoS One 2012, 7:e47518.
44. Ignell R., Dekker T., Ghaninia M., Hansson B.S. Neuronal architecture of the mosquito deutocerebrum. J. Comp. Neurol. 2005, 493:207-240.
45. Ito K., Awano W., Suzuki K., Hiromi Y., Yamamoto D. 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 1997, 124:761-771.
46. Ito K., Awasaki T. Clonal unit architecture of the adult fly brain. Adv. Exp. Med. Biol. 2008, 628:137-158.
47. Ito M., Masuda N., Shinomiya K., Endo K., Ito K. Systematic analysis of neural projections reveals clonal composition of the Drosophila brain. Curr. Biol. 2013, 23(8):644-655.
48. Iwai Y., Usui T., Hirano S., Steward R., Masatoshi T., Uemura T. Axon patterning requires D N-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron 1997, 19:77-89.
49. Izergina N., Balmer J., Bello B., Reichert H. Postembryonic development of transit amplifying neuroblast lineages in the Drosophila brain. Neural. Dev. 2009, 4:44.
50. Jarvis E., Bruce H.S., Patel N.H. Evolving specialization of the arthropod nervous system. Proc. Nat. Acad. Sci. U.S.A. 2012, 109:10634-10639.
51. Jefferis G.S., Marin E.C., Stocker R.F., Luo L. Target neuron prespecification in the olfactory map of Drosophila. Nature 2001, 414:204-208.
52. Jefferis G.S., Marin E.C., Watts R.J., Luo L. Development of neuronal connectivity in Drosophila antennal lobes and mushroom bodies. Curr. Opin. Neurobiol. 2002, 12:80-86.
53. Jiang Y., Reichert H. Programmed cell death in type II neuroblast lineages is required for central complex development in the Drosophila brain. Neural Dev. 2012, 7:3.
54. Kumar A., Fung S., Lichtneckert R., Reichert H., Hartenstein V. Arborization pattern of engrailed-positive neural lineages reveal neuromere boundaries in the Drosophila brain neuropil. J. Comp. Neurol. 2009, 517:87-104.
55. Kumar A., Bello B., Reichert H. Lineage-specific cell death in postembryonic brain development of Drosophila. Development 2009, 136:3433-3442.
56. Kunz T., Kraft K.F., Technau G.M., Urbach R. Origin of Drosophila mushroom body neuroblasts and generation of divergent embryonic lineages. Development 2012, 139(14):2510-2522.
57. Lai S.L., Awasaki T., Ito K., Lee T. Clonal analysis of Drosophila antennal lobe neurons: diverse neuronal architectures in the lateral neuroblast lineage. Development 2008, 135:2883-2893.
58. Larsen C., Shy D., Spindler S.R., Fung S., Pereanu W., Younossi-Hartenstein A., Hartenstein V. Patterns of growth, axonal extension, and axonal arborization of neuronal lineages in the developing Drosophila brain. Dev. Biol. 2009, 335:289-304.
59. Lee T., Luo L. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci 2001, 24:251-254.
60. Levine R.B. Changes in neuronal circuits during insect metamorphosis. J. Exp. Biol. 1984, 112:27-44.
61. Levine R.B., Truman J.W. Dendritic reorganization of abdominal motoneurons during metamorphosis of the moth, Manduca sexta. J. Neurosci. 1985, 5:2424-2431.
62. Libersat F., Duch C. Morphometric analysis of dendritic remodeling in an identified motoneuron during postembryonic development. J. Comp. Neurol. 2002, 450:153-166.
63. Lichtneckert R., Nobs L., Reichert H. Empty spiracles is required for the development of olfactory projection neuron circuitry in Drosophila. Development 2008, 135:2415-2424.
64. Lin S., Kao C.F., Yu H.H., Huang Y., Lee T. Lineage analysis of Drosophila lateral antennal lobe neurons reveals notch-dependent binary temporal fate decisions. PLoS Biol. 2012, 10:1-17.
65. Mao Z., Davis R.L. Eight different types of dopaminergic neurons innervate the Drosophila mushroom body neuropil: anatomical and physiological heterogeneity. Front. Neural Circuits 2009, 3:5.
66. Mysore K., Flister S., Muller P., Rodrigues V., Reichert H. Brain development in the yellow fever mosquito Aedes aegypti: a comparative immunocytochemical analysis using cross-reacting antibodies from Drosophila melanogaster. Dev. Genes Evol. 2011, 221:281-296.
67. Nordlander R.H., Edwards J.S. Postembryonic brain development in the monarch butterfly, Danaus plexippus plexippus, L. I. Cellular events during brain morphogenesis. Wilhelm Roux' Archiv. 1969, 162:197-217.
68. Patel N.H., Snow P.M., Goodman C.S. Characterization and cloning of fasciclin III: a glycoprotein expressed on a subset of neurons and axon pathways in Drosophila. Cell 1987, 48:975-988.
69. Pereanu W., Kumar A., Jennett A, Reichert H., Hartenstein V. Development-based compartmentalization of the Drosophila central brain. J. Comp. Neurol. 2010, 518:2996-3023.
70. Pereanu W., Hartenstein V. 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. 2006, 26:5534-5553.
71. Pfeiffer B.D., Jenett A., Hammonds A.S., Ngo T.T., Misra S., Murphy C., Scully A., Carlson J.W., Wan K.H., Laverty T.R., Mungall C., Svirskas R., Kadonaga J.T., Doe C.Q., Eisen M.B., Celniker S.E., Rubin G.M. Tools for neuroanatomy and neurogenetics in Drosophila. Proc Natl Acad Sci USA. 2008, 105:9715-9720.
72. Power M.E. The brain of Drosophila melanogaster. J. Morphol. 1943, 72:517-559.
73. Power M.E. A quantitative study of the growth of the central nervous system of a holometabolous insect, Drosophila melanogaster. J. Morphol. 1952, 91:389-411.
74. Prokop A., Meinertzhagen I.A. Development and structure of synaptic contacts in Drosophila. Semin. Cell Dev. Biol. 2006, 17:20-30.
75. Rybak J., Kuß A., Lamecker H., Zachow S., Hege H.C., Lienhard M., Singer J., Neubert K., Menzel R. The digital bee brain: integrating and managing neurons in a common 3D reference system. Front Syst. Neurosci. 2010, 4:1-15.
76. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., Tinevez J.Y., White D.J., Hartenstein V., Eliceiri K., Tomancak P., Cardona A. FIJI: an open-source platform for biological-image analysis. Nat. Methods 2012, 9:676-682.
77. Schmid A., Chiba A., Doe C.Q. Clonal analysis of Drosophila embryonic neuroblasts: neural cell types, axon projections and muscle targets. Development 1999, 126:4653-4689.
78. Schmidt H., Rickert C., Bossing T., Vef O., Urban J., Technau G.M. The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm. Dev. Biol. 1997, 189:186-204.
79. Seibert J., Urbach R. Role of en and novel interactions between msh, ind, and vnd in dorsoventral patterning of the Drosophila brain and ventral nerve cord. Dev. Biol. 2010, 346:332-345.
80. Shafer O.T., Helfrich-Förster C., Renn S.C., Taghert P.H. Reevaluation of Drosophila melanogaster's neuronal circadian pacemakers reveals new neuronal classes. J. Comp. Neurol. 2006, 498:180-193.
81. Singh K., Singh R.N. Metamorphosis of the central nervous system of Drosophila melanogaster Meigen (Diptera: Drosophilidae) during pupation. J. Biosci. 1999, 24:345-360.
82. Snow P.M., Patel N.H., Harrelson A.L., Goodman C.S. Neural-specific carbohydrate moiety shared by many surface glycoproteins in Drosophila and grasshopper embryos. J. Neurosci. 1987, 7:4137-4144.
83. Spindler S.R., Hartenstein V. The Drosophila neural lineages: a model system to study brain development and circuitry. Dev. Genes Evol. 2010, 220:1-10.
84. Spindler S.R., Hartenstein V. Bazooka mediates secondary axon morphology in Drosophila brain lineages. Neural Dev. 2011, 6:16.
85. Sprecher S.G., Cardona A., Hartenstein V. The Drosophila larval visual system: high-resolution analysis of a simple visual neuropil. Dev. Biol. 2011, 358:33-43.
86. Stocker R.F., Heimbeck G., Gendre N., de Belle J.S. Neuroblast ablation in Drosophila P[Gal4] lines reveals origins of olfactory interneurons. J. Neurobiol. 1997, 32:443-456.
87. Stocker R.F., Lienhard M.C., Borst A., Fischbach K.F. Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res. 1990, 262:9-34.
88. Strausfeld N.J. Atlas of an Insect Brain 1976, 1-214. Springer-Verlag, Berlin.
89. Strausfeld N.J., Li Y. Representation of the calyces in the medial and vertical lobes of cockroach mushroom bodies. J. Comp. Neurol. 1999, 409:626-646.
90. Strausfeld N.J., Sinakevitch I., Brown S.M., Farris S.M. Ground plan of the insect mushroom body: functional and evolutionary implications. J. Comp. Neurol. 2009, 513:265-291.
91. Taghert P.H., Bastiani M.J., Ho R.K, Goodman C.S. Guidance of pioneer growth cones: filopodial contacts and coupling revealed with an antibody to Lucifer Yellow. Dev. Biol. 1982, 94:391-399.
92. Tanaka N.K., Endo K., Ito K. Organization of antennal lobe-associated neurons in adult Drosophila melanogaster Brain. J. Comp. Neurol. 2012, 520:4067-4130.
93. Technau G., Heisenberg M. Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 1982, 295:405-407.
94. Thomas J.B., Bastiani M.J., Bate M., Goodman C.S. From grasshopper to Drosophila: a common plan for neuronal development. Nature 1984, 310:203-207.
95. Tissot M., Stocker R.F. Metamorphosis in Drosophila and other insects: the fate of neurons throughout the stages. Prog. Neurobiol. 2000, 62:89-111.
96. Truman J.W., Bate M. Spatial and temporal patterns of neurogenesis in the central nervous system of Drosophila melanogaster. Dev. Biol. 1988, 125:145-157.
97. Truman J.W., Booker R. Adult-specific neurons in the nervous system of the moth, Manduca sexta: selective chemical ablation using hydroxyurea. J. Neurobiol. 1986, 17:613-625.
98. Truman J.W., Moats W., Altman J., Marin E.C., Williams D.W. Role of Notch signaling in establishing the hemilineages of secondary neurons in Drosophila melanogaster. Development 2010, 137:53-61.
99. Truman J.W., Reiss S.E. Hormonal regulation of the shape of identified motoneurons in the moth Manduca sexta. J. Neurosci. 1988, 8:765-775.
100. Truman J.W., Schuppe H., Shepherd D., Williams D.W. Developmental architecture of adult-specific lineages in the ventral CNS of Drosophila. Development 2004, 131:5167-5184.
101. Udolph G., Prokop A., Bossing T., Technau G.M. A common precursor for glia and neurons in the embryonic CNS of Drosophila gives rise to segment-specific lineage variants. Development 1993, 118:765-775.
102. Urbach R., Schnabel R., Technau G.M. The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila. Development 2003, 130:3589-3606.
103. Urbach R., Technau G.M. Segment polarity and DV patterning gene expression reveals segmental organization of the Drosophila brain. Development 2003, 130:3607-3620.
104. Urbach R., Technau G.M. Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 2003, 130:3621-3637.
105. Wagh D.A., Rasse T.M., Asan E., Hofbauer A., Schwenkert I., Dürrbeck H., Buchner S., Dabauvalle M.C., Schmidt M., Qin G., Wichmann C., Kittel R., Sigrist S.J., Buchner E. Bruchpilot, a protein with homology to ELKS/CAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron 2006, 49:833-844.
106. Watson A.H., Schürmann F.W. Synaptic structure, distribution, and circuitry in the central nervous system of the locust and related insects. Microsc. Res. Tech. 2002, 56:210-226.
107. Weeks J.C. Thinking globally, acting locally: steroid hormone regulation of the dendritic architecture, synaptic connectivity and death of an individual neuron. Prog. Neurobiol. 2003, 70:421-442.
108. Williams J.L., Boyan G.S. Building the central complex of the grasshopper Schistocerca gregaria: temporal topology organizes the neuroarchitecture of the w, xy, y, z tracts. Arthropod Struct. Dev. 2005, 34:97-110.
109. Wong, D.C., Lovick, J.K., Ngo, K.T., Omoto, J.J., Borisuthirattana, W., Hartenstein, V., 2013. Postembryonic lineages of the Drosophila brain: II. Identification of lineage projection patterns based on MARCM clones, Dev. Biol. 2013, http://dx.doi.org/10.1016/j.ydbio.2013.07.009.
110. Younossi-Hartenstein A., Nassif C., Green P., Hartenstein V. Early neurogenesis of the Drosophila brain. J. Comp. Neurol. 1996, 370:313-329.
111. Yu H.H., Kao C.F., He Y., Ding P., Kao J.C., Lee T. A complete developmental sequence of a Drosophila neuronal lineage as revealed by twin-spot MARCM. PLoS Biol. 2010, 8:e1000461.
112. Yu H.H., Awasaki T., Schroeder M.D., Long F., Yang J.S., He Y., Ding P., Kao J.C., Wu G.Y., Peng H., Myers G., Lee T. Clonal development and organization of the adult Drosophila central brain. Curr. Biol. 2013, 23:633-643.
113. Zacharias D., Leslie J., Williams D., Meier T., Reichert H. Neurogenesis in the insect brain: cellular identification and molecular characterization of brain neuroblasts in the grasshopper embryo. Development 1993, 118:941-955.
114. Zecca M., Basler K., Struhl G. Direct and long-range action of a wingless morphogen gradient. Cell 1996, 87:833-844.