Organization of antennal lobe-associated neurons in adult Drosophila melanogaster brain

Journal of Comparative Neurology

Volumn 520, Issue 18, 2012, Pages 4067-4130

  Tanaka, Nobuaki K ^a,b,c,d,e   Endo, Keita ^a   Ito, Kei ^a,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^c NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e KYOTO UNIVERSITY   (Japan)

Author keywords

Antennal lobe; Brain; Lateral horn; Mushroom body; Neural circuit; Olfaction

Indexed keywords

ANTENNAL LOBE ASSOCIATED NEURON; ARTICLE; BRAIN CELL; CELL STRUCTURE; CELL TYPE; CYTOLOGY; DROSOPHILA MELANOGASTER; NERVE CELL; NEUROANATOMY; NONHUMAN; OLFACTORY SYSTEM; PRIORITY JOURNAL; PROJECTION NEURON; SENSORY NERVE CELL;

AFFERENT PATHWAYS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, CD8; ARTHROPOD ANTENNAE; BRAIN; BRAIN MAPPING; CHOLINE O-ACETYLTRANSFERASE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GREEN FLUORESCENT PROTEINS; NERVE NET; SENSORY RECEPTOR CELLS; SEROTONIN; TRANSCRIPTION FACTORS;

EID: 84867824144     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23142     Document Type: Article

References (121)

1. Abel R, Rybak J, Menzel R. 2001. Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J Comp Neurol 437: 363-383.
2. Anton S, Homberg U. 1999. Antennal lobe structure. In: Hansson B, editor. Insect olfaction. Berlin: Springer. pp 97-124.
3. Belluscio L, Katz LC 2001. Symmetry, stereotypy, and topography of odorant representations in mouse olfactory bulbs. J Neurosci 21: 2113-2122.
4. Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB. 2009. Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136: 149-162.
5. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
6. Busch S, Selcho M, Ito K, Tanimoto H. 2009. Map of octopaminergic neurons in the Drosophila brain. J Comp Neurol 513: 643-667.
7. Chiang AS, Lin CY, Chuang CC, Chang HM, Hsieh CH, Yeh CW, Shih CT, Wu JJ, Wang GT, Chen YC, Wu CC, Chen GY, Ching YT, Lee PC, Lin CY, Lin HH, Wu CC, Hsu HW, Huang YA, Chen JY, Chiang HJ, Lu CF, Ni RF, Yeh CY, Hwang JK. 2011. Three-dimensional reconstruction of brain-wide wiring networks in Drosophila at single-cell resolution. Curr Biol 21: 1-11.
8. Chou YH, Spletter ML, Yaksi E, Leong JCS, Wilson RI, Luo L. 2010. Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci 13: 439-451.
9. 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.
10. Couto A, Alenius M, Dickson BJ. 2005. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15: 1535-1547.
11. Datta SR, Vasconcelos ML, Ruta V, Luo S, Wong A, Demir E, Flores J, Balonze K, Dickson BJ, Axel R. 2008. The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. 452: 473-477.
12. Davis RL. 2004. Olfactory learning. Neuron 44: 31-48.
13. de Bruyne M, Foster K, Carlson JR. 2001. Odor coding in the Drosophila antenna. Neuron 30: 537-552.
14. Eberl DF, Duyk GM, Perrimon N. 1997. A genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster. Proc Natl Acad Sci U S A 94: 14837-14842.
15. 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: 153-160.
16. Fischbach KF, Dittrich APM. 1989. The optic lobe of Drosophila melanogaster. I. A golgi analysis of wild-type structure. Cell Tissue Res 258: 441-475.
17. Fishilevich E, Vosshall LB. 2005. Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15: 1548-1553.
18. Frambach I, Schürmann FW. 2004. Separate distribution of deutocerebral projection neurons in the mushroom bodies of the cricket brain. Acta Biol Hung 55: 21-29.
19. Galizia CG, Rössler W. 2010. Parallel olfactory systems in insects: anatomy and function. Annu Rev Entomol 55: 399-420.
20. Galizia CG, Sachse S, Rappert A, Menzel R. 1999. The glomerular code for odor representation is species specific in the honeybee Apis mellifera. Nat Neurosci 2: 473-478.
21. Gallio M, Ofstad TA, Macpherson LJ, Wang JW, Zuker CS. 2011. The coding of temperature in the Drosophila brain. Cell 144: 614-624.
22. Gao Q, Chess A. 1999. Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60: 31-39.
23. Greenspan RJ, Ferveur JF. 2000. Courtship in Drosophila. Annu Rev Genet 34: 205-232.
24. Gronenberg W. 2001. Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol 436: 474-489.
25. Hallem EA, Carlson JR. 2006. Coding of odors by a receptor repertoire. Cell 125: 143-160.
26. Hallem EA, Ho MG, Carlson JR. 2004. The molecular basis of odor coding in the Drosophila antenna. Cell 117: 965-979.
27. Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, Jegla TJ, Garrity PA. 2008. An internal thermal sensor controlling temperature preference in Drosophila. Nature 454: 217-220.
28. Hammer M, Menzel, R. 1998. Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn Mem 5: 146-156.
29. Hansson BS, Ljungberg H, Hällberg E, Löfstedt C. 1992. Functional specialization of olfactory glomeruli in a moth. Science 5061: 1313-1315.
30. Hayashi S, Ito K, Sado Y, Taniguchi M, Akimoto A, Takeuchi H, Aigaki T, Matsuzaki F, Nakagoshi H, Tanimura T, Ueda R, Uemura T, Yoshihara M, Goto S. 2002. GETDB, a database compiling expression patterns and molecular locations of a collection of Gal4 enhancer traps. Genesis 34: 58-61.
31. Heisenberg M. 2003. Mushroom body memoir: from maps to models. Nat Rev Neurosci. 4: 266-275.
32. Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20: 595-631.
33. Hofbauer A. 1991. Eine Bibliothek monoklonaler Antikörper gegen das Gehirn von Drosophila melanogaster. Habilitation thesis, University of Würzburg, Würzburg, Germany.
34. Homberg U, Montague RA, Hildebrand JG. 1988. Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res 254: 255-281.
35. Hummel T, Zipursky SL. 2004. Afferant induction of olfactory glomeruli requires N-Cadherin. Neuron 42: 77-88.
36. Ignell R. 2001. Monoamines and neuropeptides in antennal lobe interneurons of the desert locust, Schistocerca gregaria: an immunocytochemical study. Cell Tissue Res 306: 143-156.
37. Isaacson JS, Strowbridge BW. 1998. Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20: 749-761.
38. 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 Arch Dev Biol 204: 284-307.
39. Ito K, Suzuki K, Estes P, Ramaswami M, Yamamoto D, Strausfeld NJ. 1998. The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn Mem 5: 52-77.
40. Itoh T, Yokohari F, Tanimura T, Tominaga Y. 1991. External morphology of sensilla in the sacculus of an antennal flagellum of the fruit fly Drosophila melanogaster (Diptera: Drosophilidae). Int J Insect Morphol Embryol 20: 235-243.
41. Jefferis GS, Marin EC, Stocker RF, Luo L. 2001. Target neuron prespecification in the olfactory map of Drosophila. Nature 414: 204-208.
42. Jefferis GS, Potter CJ, Chan AM, Marin EC, Rohlfing T, Maurer CR, Luo L. 2007. Comprehensive maps of Drosophila higher olfactory centers: spatially segregated fruit and pheromone representation. Cell 128: 1187-1203.
43. Kamikouchi A, Shimada T, Ito K. 2006. Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster. J Comp Neurol 499: 317-356.
44. Kido A, Ito K. 2002. Mushroom bodies are not required for courtship behavior by normal and sexually mosaic Drosophila. J Neurobiol 52: 302-311.
45. Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grünewald B, Rössler W. 2006. Dual olfactory pathway in the honeybee, Apis mellifera. J Comp Neurol 499: 933-952.
46. Kloppenburg P, Mercer AR. 2008. Serotonin modulation of moth central olfactory neurons. Annu Rev Entomol 53: 179-190.
47. Kondoh Y, Kaneshiro KY, Kimura K, Yamamoto D. 2003. Evolution of sexual dimorphism in the olfactory brain of Hawaiian Drosophila. Proc R Soc Lond B 270: 1005-1013.
48. Lai SL, 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.
49. 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.
50. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, Vosshall LB. 2004. Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43: 703-714.
51. Laurent G. 1999. A systems perspective on early olfactory coding. Science 286: 723-728.
52. Lee T, Luo L. 1999. Mosaic analysis with a repressible neurotechnique cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451-461.
53. Li Y, Strausfeld NJ. 1999. Multimodal efferent and recurrent neurons in the medial lobes of cockroach mushroom bodies. J Comp Neurol 409: 647-663.
54. Malun D. 1991. Inventory and distribution of synapses of identified uniglomerular projection neurons in the antennal lobe of Periplaneta americana. J Comp Neurol 305: 348-360.
55. Malun D, Waldow U, Kraus D, Boeckh J. 1993. Connections between the deutocerebrum and the protocerebrum, and neuroanatomy of several classes of deutocerebral projection neurons in the brain of male Periplaneta americana. J Comp Neurol 329: 143-162.
56. 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.
57. Miyazaki T, Ito K. 2010. Neural architecture of the primary gustatory center of Drosophila melanogaster visualized with GAL4 and LexA enhancer-trap systems. J Comp Neurol 518: 4147-4181.
58. Mobbs PG. 1982. The brain of the honeybee Apis mellifera. 1. The connections and spatial organization of the mushroom bodies. Philos Trans R Soc Lond B 298: 309-345.
59. Mombaerts P, Wang F, Dulac C, Chao SK, Nemes A, Mendelsohn, M, Edmondson J, Axel R. 1996. Visualizing an olfactory sensory map. Cell 87: 675-686.
60. Müller D, Abel R, Brandt R, Zöckler M, Menzel R. 2002. Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J Comp Physiol A 188: 359-370.
61. Murphy GJ, Darcy DP, Isaacson JS. 2005. Intraglomerular inhibition: signaling mechanisms of an olfactory microcircuit. Nat Neurosci 8: 354-364.
62. Nässel DR, Shiga S, Wikstrand EM, Rao KR. 1991. Pigment-dispersing hormone-immunoreactive neurons and their relation to serotonergic neurons in the browfly and cockroach visual system. Cell Tissue Res 266: 511-523
63. Nayak SV, Singh RN. 1985. Primary sensory projections from the labella to the brain of Drosophila melanogaster Meigen (Diptera : Drosophilidae). Int J Insect Morphol Embryol 14: 115-129.
64. Ng M, Roorda RD, Lima SQ, Zemelman BV, Morcillo P, Miesenböck G. 2002. Transmission of olfactory information between three populations of neurons in the antennal lobe of the fly. Neuron 36: 463-474.
65. Okada R, Awasaki T, Ito K. 2009. Gamma-aminobuyric acid (GABA)-mediated neural connections in the Drosophila antennal lobe. J Comp Neurol 514: 74-91.
66. Otsuna H, Ito K. 2006. Systematic analysis of the visual projection neurons of Drosophila melanogaster. I. Lobula-specific pathways. J Comp Neurol 497: 928-958.
67. Perez-Orive J, Mazor O, Turner GC, Cassenaer S, Wilson RI, Laurent G. 2002. Oscillations and sparsening of odor representations in the mushroom body. Science 297: 359-365.
68. Power ME. 1946. The antennal centers and their connections within the brain of Drosophila melanogaster. J Comp Neurol 85: 485-517.
69. Ressler KJ, Sullivan SL, Buck LB. 1994. Information coding in the olfactory system: evidence for a stereotyped and highly organized epitope map in the olfactory bulb. Cell 79: 1245-1255.
70. Rø H, Müller D, Mustaparta H. 2007. Anatomical organization of antennal lobe projection neurons in the moth Heliothis virescens. J Comp Neurol 500: 658-675.
71. Rodrigues V. 1988. Spatial coding of olfactory information in the antennal lobe of Drosophila melanogaster. Brain Res 453: 299-307.
72. 3H]2-deoxyglucose mapping of odor-induced neuronal activity in the antennal lobes of Drosophila melanogaster. Brain Res 324: 374-378.
73. Roy B, Singh AP, Shetty C, Chaudhary V, North A, Landgraf M, Vijayraghavan K, Rodrigues V. 2007. Metamorphosis of an identified serotonergic neuron in the Drosophila olfactory system. Neural Dev 2: 20
74. Rubin BD, Katz LC. 1999. Optical imaging of odorant representations in the mammalian olfactory bulb. Neuron 23: 499-511.
75. Sachse S, Rappert A, Galizia CG. 1999. The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code. Eur J Neurosci 11: 3970-3982.
76. Sachse S, Rueckert E, Keller A, Okada R, Tanaka NK, Ito K, Vosshall LB. 2007. Activity-dependent plasticity in an olfactory circuit. Neuron 56: 838-850.
77. Sayeed O, Benzer S. 1996. Behavioral genetics of thermosensation and hygrosensation in Drosophila. Proc Natl Acad Sci U S A 93: 6079-6084.
78. Schoppa NE. 2006. Synchronization of olfactory bulb mitral cells by precisely timed inhibitory inputs. Neuron 49: 271-283.
79. Schwaerzel M, Monastirioti M, Scholz H, Friggi-Grelin F, Birman S, Heisenberg M. 2003. Dopamine and octopamine differentiate between aversive and appetitive olfactory memories in Drosophila. J Neurosci 23: 10495-10502.
80. Scott K, Brady R Jr, Cravchik A, Morozov P, Rzhetsky A, Zuker C, Axel R. 2001. A chemosensory gene family encoding candidate gustatory and olfactory receptors in Drosophila. Cell 104: 661-673.
81. Shanbhag SR, Singh K, Singh RN. 1995. Fine structure and primary sensory projections of sensilla located in the sacculus of the antenna of Drosophila melanogaster. Cell Tissue Res 282: 237-249.
82. 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.
83. Shepherd GM, Greer CA. 1998. Olfactory bulb. In: Shepherd GM editor. The synaptic organization of the brain. Oxford: Oxford University Press. pp 159-203.
84. Shinomiya K, Matsuda K, Oishi T, Otsuna H, Ito K. 2011. Flybrain Neuron Database, a comprehensive database system of the Drosophila brain neurons. J Comp Neurol 519: 807-33.
85. Silbering AF, Rytz R, Grosjean Y, Abuin L, Ramdya P, Jefferis GS, Benton R. 2011. Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. J Neurosci 31: 13357-13375.
86. Sinakevitch I, Strausfeld NJ. 2006. Comparison of octopamine-like immunoreactivity in the brains of the fruit fly and blow fly. J Comp Neurol 494: 460-475.
87. Stocker RF. 1994. The organization of the chemosensory system in Drosophila melanogaster. Cell Tissue Res 275: 3-26.
88. Stocker RF, Schorderet M. 1981. Cobalt filling of sensory projections from internal and external mouthparts in Drosophila. Cell Tissue Res 216: 513-523.
89. Stocker RF, Lienhard MC, Borst A, Fischbach KF. 1990. Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262: 9-34.
90. 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.
91. Stockinger P, Kvitsiani D, Rotkopf S, Tirian L, Dickson BJ. 2005. Neural circuitry that governs Drosophila male courtship behavior. Cell 121: 795-807.
92. Stopfer M, Jayaraman V, Laurent G. 2003. Intensity versus identity coding in an olfactory system. Neuron 39: 991-1004.
93. Stortkuhl KF, Kettler R. 2001. Functional analysis of an olfactory receptor in Drosophila melanogaster. Proc Natl Acad Sci U S A 98: 9381-9385.
94. Strausfeld NJ. 1976. Atlas of an insect brain. Berlin: Springer.
95. Strausfeld NJ, Li Y. 1999. Organization of olfactory and multimodal afferent neurons supplying the calyx and pedunculus of the cockroach mushroom bodies. J Comp Neurol 409: 603-625.
96. Suh GS, Wong AM, Hergarden AC, Wang JW, Simon AF, Benzer S, Axel R, Anderson DJ. 2004. A single population of olfactory sensory neurons mediates an innate avoidance behaviour in Drosophila. Nature 431: 854-859.
97. Sun XJ, Tolbert LP, Hildebrand JG. 1993. Ramification pattern and ultrastructural characteristics of the serotonin-immunoreactive neuron in the antennal lobe of the moth Manduca sexta: a laser scanning confocal and electron microscopic study. J Comp Neurol 338: 5-16.
98. Sun XJ, Tolbert LP, Hildebrand JG. 1997. Synaptic organization of the uniglomerular projection neurons of the antennal lobe of the moth Manduca sexta: a laser scanning confocal and electron microscopic study. J Comp Neurol 379: 2-20.
99. Takagawa K, Salvaterra P. 1996. Analysis of choline acetyltransferase protein in temperature sensitive mutant flies using newly generated monoclonal antibody. Neurosci Res 24: 237-243.
100. Tanaka NK, Awasaki T, Shimada T, Ito K. 2004. Integration of chemosensory pathways in the Drosophila second-order olfactory centers. Curr Biol 14: 449-457.
101. Tanaka NK, Tanimoto H, Ito K. 2008. Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508: 711-755.
102. Tanaka NK, Ito K, Stopfer M. 2009. Odor-evoked neural oscillations in Drosophila are mediated by widely branching interneurons. J Neurosci 29: 8595-8603.
103. Tanaka NK, Dye L, Stopfer M. 2011. Dual-labeling method for electron microscopy to characterize synaptic connectivity using genetically encoded fluorescent reporters in Drosophila. J Neurosci Methods 194: 312-315.
104. Tanaka NK, Suzuki E, Dye L, Ejima A, Stopfer M. 2012. Dye-fills reveal additional olfactory tracts in the protocerebrum of wild-type Drosophila. J Comp Neurol 520: 4131-4140.
105. Thorne N, Chromey C, Bray S, Amrein H. 2004. Taste perception and coding in Drosophila. Curr Biol 14: 1065-1079.
106. Tomonari K, Spencer S. 1990. Epitope-specific binding of CD8 regulates activation of T cells and induction of cytotoxicity. Int Immunol 2: 1189-1194.
107. Uchida N, Takahashi YK, Tanifuji M, Mori K. 2000. Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features. Nat Neurosci 3: 1035-1043.
108. van der Goes van Naters W, Carlson JR. 2007. Receptors and neurons for fly odors in Drosophila. Curr Biol 17: 606-612.
109. Vosshall LB, Wong AM, Axel R. 2000. An olfactory sensory map in the fly brain. Cell 102: 147-159.
110. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, Dürrbeck H, Buchner S, Dabauvalle MC, Schmidt M, Qin G, Wichmann C, Kittel R, Sigrist SJ, Buchner E. 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.
111. 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.
112. Wang Z, Singhvi A, Kong P, Scott K. 2004. Taste representations in the Drosophila brain. Cell 117: 981-991.
113. Wetzel CH, Behrendt HJ, Gisselmann G, Stortkuhl KF, Hovemann B, Hatt H. 2001. Functional expression and characterization of a Drosophila odorant receptor in a heterologous cell system. Proc Natl Acad Sci USA 98: 9377-9380.
114. 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.
115. Wilson RI, Turner GC, Laurent G. 2004. Transformation of olfactory representations in the Drosophila antennal lobe. Science 303: 366-370.
116. Wong AM, Wang JW, Axel R. 2002. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109: 229-241.
117. Yao CA, Ignell R, Carlson JR. 2005. Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J Neurosci 25: 8359-8367.
118. Yasuyama K, Kitamoto T, Salvaterra PM. 1995. Localization of choline acetyltransferase-expressing neurons in the larval visual system of Drosophila melanogaster. Cell Tissue Res 282: 193-202.
119. Yokoi M, Mori K, Nakanishi S. 1995. Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci U S A 92: 3371-3375.
120. Yoshihara M, Ito K. 2000. Improved Gal4 screening kit for large-scale generation of enhancer-trap strains. Dros Info Serv 83: 199-202.
121. Zube C, Kleineidam CJ, Kirschner S, Neef J, Rössler W. 2008. Organization of the olfactory pathway and odor processing in the antennal lobe of the ant Camponotus floridanus. J Comp Neurol 506: 425-441.