Systematic analysis of neural projections reveals clonal composition of the Drosophila brain

Current Biology

Volumn 23, Issue 8, 2013, Pages 644-655

  Ito, Masayoshi ^a   Masuda, Naoki ^a   Shinomiya, Kazunori ^a,b   Endo, Keita ^a,c   Ito, Kei ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b DALHOUSIE UNIVERSITY   (Canada)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ARTICLE; BRAIN; CELL CLONE; CELL LINEAGE; CONFOCAL MICROSCOPY; CYTOLOGY; DROSOPHILA MELANOGASTER; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; LARVA; METABOLISM; NEURAL STEM CELL; NEUROPIL;

ANIMALS; BRAIN; CELL LINEAGE; CLONE CELLS; DROSOPHILA MELANOGASTER; FEMALE; LARVA; MICROSCOPY, CONFOCAL; NEURAL STEM CELLS; NEUROPIL;

BASIDIOMYCOTA; DROSOPHILA MELANOGASTER; HEXAPODA;

EID: 84876751827     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2013.03.015     Document Type: Article

References (57)

1. S. Ramon y Cajal Histology of the Nervous System of Man and Vertebrates 1909 Oxford University Press New York
2. H. Sawa Specification of neurons through asymmetric cell divisions Curr. Opin. Neurobiol. 20 2010 44 49
3. B.J. Molyneaux, P. Arlotta, J.R. Menezes, and J.D. Macklis Neuronal subtype specification in the cerebral cortex Nat. Rev. Neurosci. 8 2007 427 437
4. M.R. Costa, and C. Hedin-Pereira Does cell lineage in the developing cerebral cortex contribute to its columnar organization? Front Neuroanat 4 2010 26
5. G. Ohtsuki, M. Nishiyama, T. Yoshida, T. Murakami, M. Histed, C. Lois, and K. Ohki Similarity of visual selectivity among clonally related neurons in visual cortex Neuron 75 2012 65 72
6. Y. Li, H. Lu, P.L. Cheng, S. Ge, H. Xu, S.H. Shi, and Y. Dan Clonally related visual cortical neurons show similar stimulus feature selectivity Nature 486 2012 118 121
7. K. Ito, W. Awano, K. Suzuki, Y. Hiromi, and D. Yamamoto 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 1997 761 771
8. G. Boyan, and L. Williams Embryonic development of the insect central complex: insights from lineages in the grasshopper and Drosophila Arthropod Struct. Dev. 40 2011 334 348
9. S.L. Lai, T. Awasaki, K. Ito, and T. Lee Clonal analysis of Drosophila antennal lobe neurons: diverse neuronal architectures in the lateral neuroblast lineage Development 135 2008 2883 2893
10. K. Ito, and T. Awasaki Clonal unit architecture of the adult fly brain Adv. Exp. Med. Biol. 628 2008 137 158
11. K. Ito, and Y. Hotta Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster Dev. Biol. 149 1992 134 148
12. R. Urbach, and G.M. Technau Molecular markers for identified neuroblasts in the developing brain of Drosophila Development 130 2003 3621 3637
13. A. Prokop, and G.M. Technau The origin of postembryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster Development 111 1991 79 88
14. B.C. Bello, N. Izergina, E. Caussinus, and H. Reichert Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development Neural Dev. 3 2008 5
15. J.Q. Boone, and C.Q. Doe Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells Dev. Neurobiol. 68 2008 1185 1195
16. S. Cachero, A.D. Ostrovsky, J.Y. Yu, B.J. Dickson, and G.S. Jefferis Sexual dimorphism in the fly brain Curr. Biol. 20 2010 1589 1601
17. J.Y. Yu, M.I. Kanai, E. Demir, G.S. Jefferis, and B.J. Dickson Cellular organization of the neural circuit that drives Drosophila courtship behavior Curr. Biol. 20 2010 1602 1614
18. A.S. Chiang, C.Y. Lin, C.C. Chuang, H.M. Chang, C.H. Hsieh, C.W. Yeh, C.T. Shih, J.J. Wu, G.T. Wang, and Y.C. Chen Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution Curr. Biol. 21 2011 1 11
19. S. Hampel, P. Chung, C.E. McKellar, D. Hall, L.L. Looger, and J.H. Simpson Drosophila Brainbow: a recombinase-based fluorescence labeling technique to subdivide neural expression patterns Nat. Methods 8 2011 253 259
20. T. Lee, and L. Luo Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis Neuron 22 1999 451 461
21. H.-H. Yu, T. Awasaki, M.D. Schroeder, F. Long, J.S. Yang, Y. He, P. Ding, J.-C. Kao, A. Jenett, and G.Y.-Y. Wu Clonal development and organization of the adult Drosophila central brain Curr.Biol. 2013 10.1016/j.cub.2013.02.057 Published online March 28, 2013
22. H. Peng, P. Chung, F. Long, L. Qu, A. Jenett, A.M. Seeds, E.W. Myers, and J.H. Simpson BrainAligner: 3D registration atlases of Drosophila brains Nat. Methods 8 2011 493 500
23. J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, and B. Schmid Fiji: an open-source platform for biological-image analysis Nat. Methods 9 2012 676 682
24. N. Izergina, J. Balmer, B. Bello, and H. Reichert Postembryonic development of transit amplifying neuroblast lineages in the Drosophila brain Neural Dev. 4 2009 44
25. N.K. Tanaka, H. Tanimoto, and K. Ito Neuronal assemblies of the Drosophila mushroom body J. Comp. Neurol. 508 2008 711 755
26. H. Otsuna, and K. Ito Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula-specific pathways J. Comp. Neurol. 497 2006 928 958
27. A. Kamikouchi, T. Shimada, and K. Ito Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster J. Comp. Neurol. 499 2006 317 356
28. T. Miyazaki, and K. Ito Neural architecture of the primary gustatory center of Drosophila melanogaster visualized with GAL4 and LexA enhancer-trap systems J. Comp. Neurol. 518 2010 4147 4181
29. U. Hanesch, K.-F. Fischbach, and M. Heisenberg Neuronal architecture of the central complex in Drosophila melanogaster Cell Tissue Res. 257 1989 343 366
30. G. Liu, H. Seiler, A. Wen, T. Zars, K. Ito, R. Wolf, M. Heisenberg, and L. Liu Distinct memory traces for two visual features in the Drosophila brain Nature 439 2006 551 556
31. L. Mu, K. Ito, J.P. Bacon, and N.J. Strausfeld Optic glomeruli and their inputs in Drosophila share an organizational ground pattern with the antennal lobes J. Neurosci. 32 2012 6061 6071
32. N.J. Strausfeld Arthropod Brains: Evolution, Functional Elegance, and Historical Significance 2012 Harvard University Press Cambridge, MA
33. R. McKay Stem cells in the central nervous system Science 276 1997 66 71
34. K.N. Brown, S. Chen, Z. Han, C.H. Lu, X. Tan, X.J. Zhang, L. Ding, A. Lopez-Cruz, D. Saur, and S.A. Anderson Clonal production and organization of inhibitory interneurons in the neocortex Science 334 2011 480 486
35. S. Bonilla, A.C. Hall, L. Pinto, A. Attardo, M. Götz, W.B. Huttner, and E. Arenas Identification of midbrain floor plate radial glia-like cells as dopaminergic progenitors Glia 56 2008 809 820
36. R. Okada, T. Awasaki, and K. Ito Gamma-aminobutyric acid (GABA)-mediated neural connections in the Drosophila antennal lobe J. Comp. Neurol. 514 2009 74 91
37. A. Das, A. Chiang, S. Davla, R. Priya, H. Reichert, K. Vijayraghavan, and V. Rodrigues Identification and analysis of a glutamatergic local interneuron lineage in the adult Drosophila olfactory system Neural Syst Circuits 1 2011 4
38. N. Kasthuri, and J.W. Lichtman The rise of the 'projectome' Nat. Methods 4 2007 307 308
39. D.J. Watts, and S.H. Strogatz Collective dynamics of 'small-world' networks Nature 393 1998 440 442
40. E. Bullmore, and O. Sporns Complex brain networks: graph theoretical analysis of structural and functional systems Nat. Rev. Neurosci. 10 2009 186 198
41. A. Barrat, M. Barthélemy, R. Pastor-Satorras, and A. Vespignani The architecture of complex weighted networks Proc. Natl. Acad. Sci. USA 101 2004 3747 3752
42. V.D. Blondel, J.-L. Guillaume, R. Lambiotte, and E. Lefebvre Fast unfolding of communities in large networks J. Stat. Mech. 2008 2008 P10008
43. T. Kunz, K.F. Kraft, G.M. Technau, and R. Urbach Origin of Drosophila mushroom body neuroblasts and generation of divergent embryonic lineages Development 139 2012 2510 2522
44. T. Lee, A. Lee, and L. Luo Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast Development 126 1999 4065 4076
45. T. Isshiki, B. Pearson, S. Holbrook, and C.Q. Doe Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny Cell 106 2001 511 521
46. C.Q. Doe Chinmo and neuroblast temporal identity Cell 127 2006 254 256
47. J.W. Truman, W. Moats, J. Altman, E.C. Marin, and D.W. Williams Role of Notch signaling in establishing the hemilineages of secondary neurons in Drosophila melanogaster Development 137 2010 53 61
48. K. Endo, M.R. Karim, H. Taniguchi, A. Krejci, E. Kinameri, M. Siebert, K. Ito, S.J. Bray, and A.W. Moore Chromatin modification of Notch targets in olfactory receptor neuron diversification Nat. Neurosci. 15 2012 224 233
49. Y. Sohn, M.-K. Choi, Y.-Y. Ahn, J. Lee, and J. Jeong Topological cluster analysis reveals the systemic organization of the Caenorhabditis elegans connectome PLoS Comput. Biol. 7 2011 e1001139
50. R.K. Pan, N. Chatterjee, and S. Sinha Mesoscopic organization reveals the constraints governing Caenorhabditis elegans nervous system PLoS ONE 5 2010 e9240
51. J. Broadus, and C.Q. Doe Evolution of neuroblast identity: seven-up and prospero expression reveal homologous and divergent neuroblast fates in Drosophila and Schistocerca Development 121 1995 3989 3996
52. K. Letinic, R. Zoncu, and P. Rakic Origin of GABAergic neurons in the human neocortex Nature 417 2002 645 649
53. A. Alvarez-Buylla, J.M. García-Verdugo, and A.D. Tramontin A unified hypothesis on the lineage of neural stem cells Nat. Rev. Neurosci. 2 2001 287 293
54. T. Bossing, G. Udolph, C.Q. Doe, and G.M. Technau The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm Dev. Biol. 179 1996 41 64
55. Y. Wan, H. Otsuna, C.-B. Chien, and C. Hansen An interactive visualization tool for multi-channel confocal microscopy data in neurobiology research IEEE Trans. Vis. Comput. Graph. 15 2009 1489 1496
56. S. Fortunato Community detection in graphs Phys. Rep. 486 2010 75 174
57. M.E.J. Newman, and M. Girvan Finding and evaluating community structure in networks Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 69 2004 026113