Synaptic circuitry of identified neurons in the antennal lobe of Drosophila melanogaster

Journal of Comparative Neurology

Volumn 524, Issue 9, 2016, Pages 1920-1956

  Rybak, Jürgen ^a,d   Talarico, Giovanni ^a,d   Ruiz, Santiago ^b   Arnold, Christopher ^a   Cantera, Rafael ^b,c   Hansson, Bill S ^a  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b Microbial Biochemistry and Genomics Department   (Uruguay)

^c STOCKHOLM UNIVERSITY   (Sweden)

^d UNIVERSITY MEDICINE GREIFSWALD   (Germany)

Author keywords

Drosophila melanogaster; Glomerulus; Olfactory system; Projection neuron; Synaptic microcircuits; Ultrastructure

Indexed keywords

ADULT; ARTICLE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; FEMALE; MALE; NERVE CELL PLASTICITY; NERVE PROJECTION; NONHUMAN; OLFACTORY SYSTEM; POSTSYNAPTIC DENSITY; PRESYNAPTIC DENSITY; PRIORITY JOURNAL; SYNAPSE; SYNAPTIC TRANSMISSION; ANATOMIC MODEL; ANATOMY AND HISTOLOGY; ANIMAL; ANTENNA (ORGAN); CONFOCAL MICROSCOPY; CYTOLOGY; GENETICS; METABOLISM; NEUROPIL; PHYSIOLOGY; THREE DIMENSIONAL IMAGING; TRANSGENIC ANIMAL; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

DROSOPHILA PROTEIN; GREEN FLUORESCENT PROTEIN;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ARTHROPOD ANTENNAE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GREEN FLUORESCENT PROTEINS; IMAGING, THREE-DIMENSIONAL; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, ANATOMIC; NEUROPIL; SYNAPSES;

EID: 84960153344     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23966     Document Type: Article

References (170)

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. Acebes A, Martin-Pena A, Chevalier V, Ferrus A. 2011. Synapse loss in olfactory local interneurons modifies perception. J Neurosci 31:2734-2745.
3. Ache BW, Young JM. 2005. Olfaction: diverse species, conserved principles. Neuron 48:417-430.
4. Agarwal G, Isacoff E. 2011. Specializations of a pheromonal glomerulus in the Drosophila olfactory system. J Neurophysiol 105:1711-1721.
5. Ahrens MB, Li JM, Orger MB, Robson DN, Schier AF, Engert F, Portugues R. 2012. Brain-wide neuronal dynamics during motor adaptation in zebrafish. Nature 485:473-477.
6. Alonso-Nanclares L, Gonzalez-Soriano J, Rodriguez JR, DeFelipe J. 2008. Gender differences in human cortical synaptic density. Proc Natl Acad Sci U S A 105:14615-14619.
7. Armstrong JD, van Hemert JI. 2009. Towards a virtual fly brain. Philos Trans R Soc Lond B 367:2387-2397.
8. Berdnik D, Chihara T, Couto A, Luo L. 2006. Wiring stability of the adult Drosophila olfactory circuit after lesion. J Neurosci 26:3367-3376.
9. Beutel RG, Pohl H, Hünefeld F. 2005. Strepsipteran brains and effects of miniaturization (Insecta). Arthropod Struct Dev 34:301-313.
10. Bhandawat V, Olsen SR, Gouwens NW, Schlief ML, Wilson RI. 2007. Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nat Neurosci 10:1474-1482.
11. Boeckh J, Tolbert LP. 1993. Synaptic organization and development of the antennal lobe in insects. Microsc Res Tech 24:260-280.
12. Braitenberg V, Schüz A. 1991. Anatomy of the cortex. Berlin: Springer.
13. Brand A, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
14. Brochtrup A, Hummel T. 2011. Olfactory map formation in the Drosophila brain: genetic specificity and neuronal variability. Curr Opin Neurobiol 21:85-92.
15. Brown SM, Napper RM, Thompson CM, Mercer AR. 2002. Stereological analysis reveals striking differences in the structural plasticity of two readily identifiable glomeruli in the antennal lobes of the adult worker honeybee. J Neurosci 22:8514-8522.
16. Butcher NJ, Friedrich AB, Lu Z, Tanimoto H, Meinertzhagen IA. 2012. Different classes of input and output neurons reveal new features in microglomeruli of the adult Drosophila mushroom body calyx. J Comp Neurol 520:2185-2201.
17. Cachero S, Ostrovsky AD, Yu JY, Dickson BJ, Jefferis GSXE. 2010. Sexual dimorphism in the fly brain. Curr Biol 20:1589-1601.
18. Cardona A, Saalfeld S, Arganda I, Pereanu W, Schindelin J, Hartenstein V. 2010a. Identifying neuronal lineages of Drosophila by sequence analysis of axon tracts. J Neurosci 30:7538-7553.
19. Cardona A, Saalfeld S, Preibisch S, Schmid B, Cheng A, Pulokas J, Tomancak P, Hartenstein V. 2010b. An integrated micro- and macroarchitectural analysis of the Drosophila brain by computer-assisted serial section electron microscopy. PLoS Biol 8:1-17.
20. Cardona A, Saalfeld S, Schindelin J, Arganda-Carreras I, Preibisch S, Longair M, Tomancak P, Hartenstein V, Douglas RJ. 2012. TrakEM2 Software for neural circuit reconstruction. PLoS One 7:e38011.
21. Chen WR, Shepherd GM. 2005. The olfactory glomerulus: a cortical module with specific functions. J Neurocytol 34:353-360.
22. Chen Y, Akin O, Nern A, Tsui CYK, Pecot Matthew Y, Zipursky SL. 2014. Cell-type-specific labeling of synapses in vivo through synaptic tagging with recombination. Neuron 81:280-293.
23. 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 HH, 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.
24. Chou YH, Spletter ML, Yaksi E, Leong JC, Wilson RI, Luo L. 2010. Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci 13:439-449.
25. Christiansen F, Zube C, Andlauer TF, Wichmann C, Fouquet W, Owald D, Mertel S, Leiss F, Tavosanis G, Luna AJ, Fiala A, Sigrist SJ. 2011. Presynapses in Kenyon cell dendrites in the mushroom body calyx of Drosophila. J Neurosci 31:9696-9707.
26. Couto A, Alenius M, Dickson BJ. 2005. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535-1547.
27. Das S, Sadanandappa MK, Dervan A, Larkin A, Lee JA, Sudhakaran IP, Priya R, Heidari Rh, Holohan EE, Pimentel A, Gandhi A, Ito K, Sanyal S, Wang JW, Rodrigues V, Ramaswami M. 2011. Plasticity of local GABAergic interneurons drives olfactory habituation. Proc Natl Acad Sci U S A 108:E646-654.
28. de Bruyne M, Clyne PJ, Carlson JR. 1999. Odor coding in a model olfactory organ: the Drosophila maxillary palp. J Neurosci 19:4520-4532.
29. de Bruyne M, Foster K, Carlson JR. 2001. Odor coding in the Drosophila antenna. Neuron 30:537-552.
30. Denk W, Horstmann H. 2004. Scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol 2:10.
31. Didier A, Carleton A, Bjaalie JG, Vincent J-D, Ottersen OP, Storm-Mathisen J, Lledo P-M. 2001. A dendrodendritic reciprocal synapse provides a recurrent excitatory connection in the olfactory bulb. Proc Natl Acad Sci U S A 98:6441-6446.
32. Distler PG, Boeckh J. 1997. Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana: I. Uniglomerular projection neurons. J Comp Neurol 378:307-319.
33. Distler PG, Gruber C, Boeckh J. 1998. Synaptic connections between GABA-immunoreactive neurons and uniglomerular projection neurons within the antennal lobe of the cockroach, Periplaneta americana. Synapse 29:1-13.
34. El Jundi B, Huetteroth W, Kurylas AE, Schachtner J. 2009. Anisometric brain dimorphism revisited: implementation of a volumetric 3D standard brain in Manduca sexta. J Comp Neurol 517:210-225.
35. Esslen J, Kaissling K-E. 1976. Zahl und Verteilung antennaler Sensillen bei der Honigbiene (Apis mellifera L.). Zoomorphologie 83:227-251.
36. Evers JF, Schmitt S, Sibila M, Duch C. 2005. Progress in functional neuroanatomy: precise automatic geometric reconstruction of neuronal morphology from confocal image stacks. J Neurophysiol 93:2331-2342.
37. Faisal AA, White JA, Laughlin SB. 2005. Ion-channel noise places limits on the miniaturization of the brain's wiring. Curr Biol 15:1143-1149.
38. Feinberg EH, VanHoven MK, Bendesky A, Wang G, Fetter RD, Shen K, Bargmann CI. 2008. GFP reconstitution across synaptic partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 57:353-363.
39. Fishilevich E, Vosshall LB. 2005. Genetic and functional subdivision of the Drosophila antennal lobe. Curr Biol 15:1548-1553.
40. Flanagan D, Mercer AR. 1989a. An atlas and 3-D reconstruction of the antennal lobes in the worker honey bee, Apis mellifera L. (Hymenoptera: Apidae). Int J Insect Morphol Embryol 18:145-159.
41. Flanagan D, Mercer AR. 1989b. Morphology and response characteristics of neurons in the deutocerebrum of the brain in the honeybee Apis mellifera. J Comp Physiol A 164:483-494.
42. Fonta C, Sun XJ, Masson C. 1993. Morphology and spatial distribution of bee antennal lobe interneurones responsive to odours. Chem Senses 18:101-119.
43. Fouquet W, Owald D, Wichmann C, Mertel S, Depner H, Dyba M, Hallermann S, Kittel RJ, Eimer S, Sigrist SJ. 2009. Maturation of active zone assembly by Drosophila Bruchpilot. J Cell Biol 186:129-145.
44. Frank DD, Jouandet GC, Kearney PJ, Macpherson LJ, Gallio M. 2015. Temperature representation in the Drosophila brain. Nature 519:358-361.
45. Fröhlich. 1985. Freeze-Fracture Study of an Invertebrate Multiple-Contact Synapse: The Fly Photoreceptor Tetrad. J Comp Neurol 241:311-326.
46. Galizia CG. 2014. Olfactory coding in the insect brain: data and conjectures. Eur J Neurosci 39:1784-1795.
47. Galizia CG, Sachse S. 2010. Odor coding in insects. In: Menini A, editor. Neurobiology of olfaction. Boca Raton, FL: CRC Press. p 35-70.
48. Galizia CG, McIlwrath SL, Menzel R. 1999. A digital three-dimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res 295:383-394.
49. Gascuel J, Masson C. 1991. A quantitative ultrastructural-study of the honeybee antennal lobe. Tissue Cell 23:341-355.
50. Gordon MD, Scott K. 2009. Motor control in a Drosophila taste circuit. Neuron 61:373-384.
51. Grabe V, Strutz A, Baschwitz A, Hansson BS, Sachse S. 2015. Digital in vivo 3D atlas of the antennal lobe of Drosophila melanogaster. J Comp Neurol 523:530-544.
52. Grosjean Y, Rytz R, Farine J-P, Abuin L, Cortot J, Jefferis GSXE, Benton R. 2011. An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 478:236-240.
53. Grosse-Wilde E, Kuebler LS, Bucks S, Vogel H, Wicher D, Hansson BS. 2011. Antennal transcriptome of Manduca sexta. Proc Natl Acad Sci U S A 108:7449-7454.
54. Hansson BS, Stensmyr MC. 2011. Evolution of insect olfaction. Neuron 72:698-711.
55. Hansson BS, Christensen TA, Hildebrand JG. 1991. Functionally distinct subdivisions of the macroglomerular complex in the antennal lobe of the male sphinx moth Manduca sexta. J Comp Neurol 312:264-278.
56. Hansson BS, Ljungberg H, Hallberg E, Löfstedt C. 1992. Functional specialization of olfactory glomeruli in a moth. Science 256:1313-1315.
57. Heisenberg M. 1998. What do the mushroom bodies do for the insect brain? An introduction. Learn Mem 5:1-10.
58. Hildebrand JG, Shepherd GM. 1997. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20:595-631.
59. Hofbauer A, Ebel T, Waltenspiel B, Oswald P, Chen Y-C, Halder P, Biskup S, Lewandrowski U, Winkler C, Sickmann A, Buchner S, Buchner E. 2009. The Wuerzburg Hybridoma Library against Drosophila Brain. J Neurogenet 23:78-91.
60. Hong W, Luo L. 2014. Genetic control of wiring specificity in the fly olfactory system. Genetics 196:17-29.
61. Hong W, Mosca TJ, Luo L. 2012. Teneurins instruct synaptic partner matching in an olfactory map. Nature 484:201-207.
62. Hu A, Zhang W, Wang Z. 2010. Functional feedback from mushroom bodies to antennal lobes in the Drosophila olfactory pathway. Proc Natl Acad Sci U S A 107:10262-10267.
63. Hummel T, Zipursky SL. 2004. Afferent induction of olfactory glomeruli requires N-cadherin. Neuron 42:77-88.
64. Ibba I, Angioy A, Hansson BS, Dekker T. 2010. Macroglomeruli for fruit odors change blend preference in Drosophila. Naturwissenschaften 97:1059-1066.
65. Ignell R, Root CM, Birse RT, Wang JW, Nassel DR, Winther AM. 2009. Presynaptic peptidergic modulation of olfactory receptor neurons in Drosophila. Proc Natl Acad Sci U S A 106:13070-13075.
66. Ito K, Shinomiya K, Ito M, Armstrong JD, Boyan G, Hartenstein V, Harzsch S, Heisenberg M, Homberg U, Jenett A, Keshishian H, Restifo Linda L, Rössler W, Simpson Julie H, Strausfeld Nicholas J, Strauss R, Vosshall Leslie B. 2014. A systematic nomenclature for the insect brain. Neuron 81:755-765.
67. Jefferis GS, Marin EC, Stocker RF, Luo L. 2001. Target neuron prespecification in the olfactory map of Drosophila. Nature 414:204-208.
68. Jefferis G, Marin EC, Watts RJ, Luo LQ. 2002. Development of neuronal connectivity in Drosophila antennal lobes and mushroom bodies. Curr Opin Neurobiol 12:80-86.
69. Jefferis GS, 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.
70. Jenett A, Rubin GM, Ngo TT, Shepherd D, Murphy C, Dionne H, Pfeiffer BD, Cavallaro A, Hall D, Jeter J, Iyer N, Fetter D, Hausenfluck JH, Peng H, Trautman ET, Svirskas RR, Myers EW, Iwinski ZR, Aso Y, DePasquale GM, Enos A, Hulamm P, Lam SC, Li HH, Laverty TR, Long F, Qu L, Murphy SD, Rokicki K, Safford T, Shaw K, Simpson JH, Sowell A, Tae S, Yu Y, Zugates CT. 2012. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep 2:991-1001.
71. Jiang Y, Li YR, Tian H, Ma M, Matsunami H. 2015. Muscarinic acetylcholine receptor M3 modulates odorant receptor activity via inhibition of β-arrestin-2 recruitment. Nat Commun 6:6448.
72. Kasowski HJ, Kim H, Greer CA. 1999. Compartmental organization of the olfactory bulb glomerulus. J Comp Neurol 407:261-274.
73. Kazama H, Wilson RI. 2008. Homeostatic matching and nonlinear amplification at identified central synapses. Neuron 58:401-413.
74. Kelber C, Rossler W, Kleineidam CJ. 2006. Multiple olfactory receptor neurons and their axonal projections in the antennal lobe of the honeybee Apis mellifera. J Comp Neurol 496:395-405.
75. Kelber C, Rossler W, Kleineidam CJ. 2010. Phenotypic plasticity in number of glomeruli and sensory innervation of the antennal lobe in leaf-cutting ant workers (A. vollenweideri). Dev Neurobiol 70:222-234.
76. Knaden M, Strutz A, Ahsan J, Sachse S, Hansson BS. 2012. Spatial representation of odorant valence in an insect brain. Cell Rep 1:392-399.
77. Knott G, Marchman H, Lich B. 2008. Serial section scanning electron microscopy of adult brain tissue using focused ion beam milling. J Neurosci 28:2964-2959.
78. Kwon H-W, Lu T, Rützler M, Zwiebel LJ. 2006. Olfactory responses in a gustatory organ of the malaria vector mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 103:13526-13531.
79. Laissue PP, Vosshall LB. 2008. The olfactory sensory map in Drosophila. In: Technau GM, editor. Brain development in Drosophila melanogaster. New York: Springer. p 102-114
80. 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.
81. Lei H, Oland LA, Riffell JA, Beyerlein A, Hildebrand JG. 2010. Microcircuits for olfactory information processing in the antennal lobe of Manduca sexta. In: Shepherd GM, Grillner S, editors. Handbook of brain microcircuits. New York: Oxford University Press. p 417-426.
82. Leitch B, Laurent G. 1996. GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system. J Comp Neurol 372:487-514.
83. Li J, Wang Y, Chiu SL, Cline HT. 2010. Membrane targeted horseradish peroxidase as a marker for correlative fluorescence and electron microscopy studies. Front Neural Circuits 4:6.
84. Linster C, Cleland TA. 2009. Glomerular microcircuits in the olfactory bulb. Neural Netw 22:1169-1173.
85. Liu KSY, Siebert M, Mertel S, Knoche E, Wegener S, Wichmann C, Matkovic T, Muhammad K, Depner H, Mettke C, Bückers J, Hell SW, Müller M, Davis GW, Schmitz D, Sigrist SJ. 2011. RIM-binding protein, a central part of the active zone, is essential for neurotransmitter release. Science 334:1565-1569.
86. Liu Q, Chen B, Hall DH, Wang Z-W. 2007. A quantum of neurotransmitter causes minis in multiple postsynaptic cells at the Caenorhabditis elegans neuromuscular junction. Dev Neurobiol 67:123-128.
87. Liu WW, Wilson RI. 2013. Glutamate is an inhibitory neurotransmitter in the Drosophila olfactory system. Proc Natl Acad Sci U S A 110:10294-10299.
88. Lofaldli BB, Kvello P, Mustaparta H. 2010. Integration of the antennal lobe glomeruli and three projection neurons in the standard brain atlas of the moth Heliothis virescens. Front Syst Neurosci 4:5.
89. Malun D. 1991a. Inventory and distribution of synapses of identified uniglomerular projection neurons in the antennal lobe of Periplaneta americana. J Comp Neurol 305:348-360.
90. Malun D. 1991b. Synaptic relationships between GABA-immunoreactive neurons and an identified uniglomerular projection neuron in the antennal lobe of Periplaneta americana-a double-labeling electron-microscopic study. Histochemistry 96:197-207.
91. Marder E. 2015. Understanding brains: details, intuition, and big data. PLoS Biol 13:e1002147.
92. 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.
93. Martin JP, Beyerlein A, Dacks AM, Reisenman CE, Riffell JA, Lei H, Hildebrand JG. 2011. The neurobiology of insect olfaction: sensory processing in a comparative context. Prog Neurobiol 95:427-447.
94. Meinertzhagen IA. 1996. Ultrastructure and quantification of synapses in the insect nervous system. J Neurosci Meth 69:59-73.
95. Meinertzhagen IA. 2010. The organisation of invertebrate brains: cells, synapses and circuits. Acta Zool 91:64-71.
96. Meinertzhagen IA, Lee C-H. 2012. The genetic analysis of functional connectomics in Drosophila. Adv Genet 80:99-151.
97. 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.
98. Meyer A, Galizia CG, Nawrot MP. 2013. Local interneurons and projection neurons in the antennal lobe from a spiking point of view. J Neurophysiol 110:2465-2474.
99. Micheva KD, Smith SJ. 2007. Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 55:25-36.
100. Mishchenko Y. 2010. On optical detection of densely labeled synapses in neuropil and mapping connectivity with combinatorially multiplexed fluorescent synaptic markers. PLoS One 5:e8853.
101. Mosca TJ, Luo L. 2014. Synaptic organization of the Drosophila antennal lobe and its regulation by the Teneurins. eLife 3:e03726.
102. Mosca TJ, Hong W, Dani VS, Favaloro V, Luo L. 2012. Trans-synaptic Teneurin signalling in neuromuscular synapse organization and target choice. Nature 484:237-241.
103. Namiki S, Kanzaki R. 2008. Reconstructing the population activity of olfactory output neurons that innervate identifi able processing units. Front Neural Circuits 2:1.
104. Namiki S, Haupt SS, Kazawa T, Takashima A, Ikeno H, Kanzaki R. 2009. Reconstruction of virtual neural circuits in an insect brain. Front Neurosci 3:206-213.
105. Nässel D. 2009. Neuropeptide signaling near and far: how localized and timed is the action of neuropeptides in brain circuits? Invertebr Neurosci 9:57-75.
106. Nässel D. 2014. Neuropeptides regulating Drosophila behavior. In: Dubnau J, editor. Behavioral genetics of the fly (Drosophila melanogaster). Cambridge: Cambridge University Press. p 20-36.
107. Nawroth JC, Greer CA, Chen WR, Laughlin SB, Shepherd GM. 2007. An energy budget for the olfactory glomerulus. J Neurosci 27:9790-9800.
108. 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.
109. Nicolaï LJJ, Ramaekers A, Raemaekers T, Drozdzecki A, Mauss AS, Yan J, Landgraf M, Annaert W, Hassan BA. 2010. Genetically encoded dendritic marker sheds light on neuronal connectivity in Drosophila. Proc Natl Acad Sci U S A 107:20553-20558.
110. Nishino H, Nishikawa M, Mizunami M, Yokohari F. 2009. Functional and topographic segregation of glomeruli revealed by local staining of antennal sensory neurons in the honeybee Apis mellifera. J Comp Neurol 515:161-180.
111. Niven JE, Farris SM. 2012. Miniaturization of nervous systems and neurons. Curr Biol 22:R323-R329.
112. 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.
113. Oland LA, Tolbert LP. 2003. Key interactions between neurons and glial cells during neuronal development in insects. Annu Rev Entomol 48:89-110.
114. Olsen SR, Wilson RI. 2008. Lateral presynaptic inhibition mediates gain control in an olfactory circuit. Nature 452:956-960.
115. Pech U, Revelo Natalia H, Seitz Katharina J, Rizzoli Silvio O, Fiala A. 2015. Optical dissection of experience-dependent pre- and postsynaptic plasticity in the Drosophila brain. Cell Rep 10:2083-2095.
116. Pelz D, Roeske T, Syed Z, Bruyne Md, Galizia CG. 2006. The molecular receptive range of an olfactory receptor in vivo (Drosophila melanogaster Or22a). J Neurobiol 66:1544-1563.
117. Rein K, Zockler M, Mader MT, Grübel C, Heisenberg M. 2002. The Drosophila standard brain. Curr Biol 12:227-231.
118. Root CM, Masuyama K, Green DS, Enell LE, Nassel DR, Lee CH, Wang JW. 2008. A presynaptic gain control mechanism fine-tunes olfactory behavior. Neuron 59:311-321.
119. Rospars JP. 1988. Structure and development of the insect antennodeutocerebral system. Int J Insect Morphol Embryol 17:243-294.
120. Ruthensteiner B, Hess M. 2008. Embedding 3D models of biological specimens in PDF publications. Microsc Res Tech 71:778-786.
121. Rybak J. 2013. Exploring brain connectivity in insect model systems of learning and memory. In: Menzel R, Benjamin P, editors. Invertebrate learning and memory. San Diego, CA: Academic Press. p 26-40.
122. Rybak J, Meinertzhagen IA. 1997. The effects of light reversals on photoreceptor synaptogenesis in the fly Musca domestica. Eur J Neurosci 9:319-333.
123. Rybak J, Kuss A, Lamecker H, Zachow S, Hege HC, Lienhard M, Singer J, Neubert K, Menzel R. 2010. The digital bee brain: integrating and managing neurons in a common 3D reference system. Front Syst Neurosci 4:30.
124. Sachse S, Galizia CG. 2002. Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106-1117.
125. Sachse S, Rueckert E, Keller A, Okada R, Tanaka NK, Ito K, Voshall LB. 2007. Activity-dependent plasticity in an olfactory circuit. Neuron 56:838-850.
126. Salecker I, Distler P. 1990. Serotonin-immunoreactive neurons in the antennal lobes of the american cockroach Periplaneta americana-light-microscopic and electron-microscopic observations. Histochemistry 94:463-473.
127. Salvaterra PM, Kitamoto T. 2001. Drosophila cholinergic neurons and processes visualized with Gal4/UAS-GFP?. Gene Expr Patterns 1:73-82.
128. Schikorski T, Young Jr SM, Hu Y. 2007. Horseradish peroxidase cDNA as a marker for electron microscopy in neurons. J Neurosci Methods 165:210-215.
129. Seki Y, Rybak J, Wicher D, Sachse S, Hansson BS. 2010. Physiological and morphological characterization of local interneurons in the Drosophila antennal lobe. J Neurophysiol 104:1007-1019.
130. 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.
131. Shao HC, Wu CC, Chen GY, Chang HM, Chiang AS, Chen YC. 2014. Developing a stereotypical Drosophila brain atlas. IEEE Trans Biomed Eng 61:2848-2858.
132. Shepherd GM. 2011. The olfactory bulb: a simple system in the mammalian brain. comprehensive physiology. Hoboken, NJ: John Wiley and Sons.
133. 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 519:807-833.
134. Silbering AF, Okada R, Ito K, Galizia CG. 2008. Olfactory information processing in the Drosophila antennal lobe: anything goes? J Neurosci 28:13075-13087.
135. 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.
136. Stensmyr MC, Giordano E, Balloi A, Angioy A-M, Hansson BS. 2003. Novel natural ligands for Drosophila olfactory receptor neurones. J Exp Biol 206:715-724.
137. Stensmyr MC, Dweck HK, Farhan A, Ibba I, Strutz A, Mukunda L, Linz J, Grabe V, Steck K, Lavista-Llanos S, Wicher D, Sachse S, Knaden M, Becher PG, Seki Y, Hansson BS. 2012. A conserved dedicated olfactory circuit for detecting harmful microbes in Drosophila. Cell 151:1345-1357.
138. Stieb SM, Kelber C, Wehner R, Rössler W. 2011. Antennal-lobe organization in desert ants of the genus Cataglyphis. Brain Behav Evol 77:136-146.
139. Stocker RF. 1994. The organization of the chemosensory system in Drosophila melanogaster: a review. Cell Tissue Res 275:3-26.
140. Stocker RF. 2001. Drosophila as a focus in olfactory research: mapping of olfactory sensilla by fine structure, odor specificity, odorant receptor expression, and central connectivity. Microsc Res Tech 55:284-296.
141. Stocker RF, Lienhard MC, Borst A, Fischbach KF. 1990. Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262:9-34.
142. 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.
143. Stockinger P, Kvitsiani D, Rotkopf S, Tirian L, Dickson BJ. 2005. Neural circuitry that governs Drosophila male courtship behavior. Cell 121:795-807.
144. Stopfer M, Bhagavan S, Smith BH, Laurent G. 1997. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390:70-74.
145. Stork T, Engelen D, Krudewig A, Silies M, Bainton RJ, Klämbt C. 2008. Organization and function of the blood-brain barrier in Drosophila. J Neurosci 28:587-597.
146. Strutz A, Soelter J, Baschwitz A, Farhan A, Grabe V, Rybak J, Knaden M, Schmuker M, Hansson BS, Sachse S. 2014. Decoding odor quality and intensity in the Drosophila brain. eLife 3:e04147.
147. Su C-Y, Menuz K, Reisert J, Carlson JR. 2012. Non-synaptic inhibition between grouped neurons in an olfactory circuit. Nature 492:66-71.
148. Sudhakaran IP, Holohan EE, Osman S, Rodrigues V, Vijayraghavan K, Ramaswami M. 2012. Plasticity of recurrent inhibition in the Drosophila antennal lobe. J Neurosci 32:7225-7231.
149. Suh GSB, 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.
150. 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.
151. Takemura S-Y, Lu Z, Meinertzhagen IA. 2008. Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. J Comp Neurol 509:493-513.
152. Takemura S-Y, Karuppudurai T, Ting C-Y, Lu Z, Lee C-H, Meinertzhagen Ian A. 2011. Cholinergic circuits integrate neighboring visual signals in a Drosophila motion detection pathway. Curr Biol 21:2077-2084.
153. Takemura S-Y, Bharioke A, Lu Z, Nern A, Vitaladevuni S, Rivlin PK, Katz WT, Olbris DJ, Plaza SM, Winston P, Zhao T, Horne JA, Fetter RD, Takemura S, Blazek K, Chang L-A, Ogundeyi O, Saunders MA, Shapiro V, Sigmund C, Rubin GM, Scheffer LK, Meinertzhagen IA, Chklovskii DB. 2013. A visual motion detection circuit suggested by Drosophila connectomics. Nature 500:175-181.
154. Tanaka NK, Tanimoto H, Ito K. 2008. Neuronal assemblies of the Drosophila mushroom body. J Comp Neurol 508:711-755.
155. Tanaka NK, Ito K, Stopfer M. 2009. Odor-evoked neural oscillations in Drosophila are mediated by widely branching interneurons. J Neurosci 29:8595-8603.
156. 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.
157. Tanaka NK, Endo K, Ito K. 2012. The organization of antennal lobe-associated neurons in the adult Drosophila melanogaster brain. J Comp Neurol 520:4067-4130.
158. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL. 2009. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6:875-881.
159. Trujillo-Cenoz O. 1969. Some Aspects of the Structural Organization of the Medulla in Muscoid Flies l. J Ultrastruc Res 27:533-553.
160. van der Woude E, Smid HM, Chittka L, Huigens ME. 2013. Breaking Haller's rule: brain-body size isometry in a minute parasitic wasp. Brain Behav Evol 81:86-92.
161. Vosshall LB, Stocker RF. 2007. Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505-533.
162. Vosshall LB, Wong AM, Axel R. 2000. An olfactory sensory map in the fly brain. Cell 102:147-159.
163. Wagh D, Rasse T, Asan E, Hofbauer A, Schwenkert I, Durrbeck H, Buchner S, Dabauvalle M, Schmidt M, Qin G, Wichmann C, Kittel R, Sigrist S, 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.
164. Wang K, Gong J, Wang Q, Li H, Cheng Q, Liu Y, Zeng S, Wang Z. 2014. Parallel pathways convey olfactory information with opposite polarities in Drosophila. Proc Natl Acad Sci U S A 111:3164-3169.
165. Watts RJ, Schuldiner O, Perrino J, Larsen C, Luo L. 2004. Glia engulf degenerating axons during developmental axon pruning. Curr Biol 14:678-684.
166. Wilson RI. 2011. Understanding the functional consequences of synaptic specialization: insight from the Drosophila antennal lobe. Curr Opin Neurobiol 21:254-260.
167. 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.
168. Winther ÅME, Ignell R. 2010. Local peptidergic signaling in the antennal lobe shapes olfactory behavior. Fly 4:167-171.
169. Yaksi E, Wilson RI. 2010. Electrical coupling between olfactory glomeruli. Neuron 67:1034-1047.
170. Yuste R, Tank DW. 1996. Dendritic integration in mammalian neurons, a century after Cajal. Neuron 16:701-716.