Embryonic Origin of Olfactory Circuitry in Drosophila: Contact and Activity-Mediated Interactions Pattern Connectivity in the Antennal Lobe

PLoS Biology

Volumn 10, Issue 10, 2012, Pages

  Prieto Godino, Lucia L ^a,b   Diegelmann, Soeren ^a,c   Bate, Michael ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTENNA (ORGAN); ARTICLE; CHEMICAL LABELING; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; HATCHING; INNERVATION; INSECT DEVELOPMENT; INTERNEURON; LARVAL STAGE; NERVE CELL DIFFERENTIATION; NONHUMAN; OLFACTORY CORTEX; OLFACTORY NERVE; OLFACTORY RECEPTOR; OLFACTORY SYSTEM; PRESYNAPTIC POTENTIAL; SENSORY NERVE CELL; SURVIVAL RATE; VERTEBRATE;

ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; LARVA; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; SENSORY RECEPTOR CELLS;

VERTEBRATA;

EID: 84868145610     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001400     Document Type: Article

References (61)

1. Jefferis GS, Marin EC, Stocker RF, Luo L, (2001) Target neuron prespecification in the olfactory map of Drosophila. Nature 414: 204-208.
2. Jefferis GS, Vyas RM, Berdnik D, Ramaekers A, Stocker RF, et al. (2004) Developmental origin of wiring specificity in the olfactory system of Drosophila. Development 131: 117-130.
3. Hildebrand JG, Rössler W, Tolbert LP, (1997) Postembryonic development of the olfactory system in the moth Manduca sexta: primary-afferent control of glomerular development. Semin Cell Dev Biol 8: 163-170.
4. Zhu H, Hummel T, Clemens JC, Berdnik D, Zipursky SL, et al. (2006) Dendritic patterning by Dscam and synaptic partner matching in the Drosophila antennal lobe. Nat Neurosci 9: 349-355.
5. Komiyama T, Sweeney LB, Schuldiner O, Garcia KC, Luo L, (2007) Graded expression of semaphorin-1a cell-autonomously directs dendritic targeting of olfactory projection neurons. Cell 128: 399-410.
6. Belluscio L, Lodovichi C, Feinstein P, Mombaerts P, Katz LC, (2002) Odorant receptors instruct functional circuitry in the mouse olfactory bulb. Nature 419: 296-300.
7. Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R, (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96: 725-736.
8. Gao Q, Chess A, (1999) Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60: 31-39.
9. Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, et al. (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22: 327-338.
10. Vosshall LB, Wong AM, Axel R, (2000) An olfactory sensory map in the fly brain. Cell 102: 147-159.
11. Gao Q, Yuan B, Chess A, (2000) Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe. Nat Neurosci 3: 780-785.
12. Hildebrand JG, Shepherd GM, (1997) Mechanisms of olfactory discrimination: converging evidence for common principles across phyla. Annu Rev Neurosci 20: 595-631.
13. Blanchart A, De Carlos JA, López-Mascaraque L, (2006) Time frame of mitral cell development in the mice olfactory bulb. J Comp Neurol 496: 529-543.
14. Matsutani S, Yamamoto N, (2000) Differentiation of mitral cell dendrites in the developing main olfactory bulbs of normal and naris-occluded rats. J Comp Neurol 418: 402-410.
15. López-Mascaraque L, García C, Blanchart A, De Carlos JA, (2005) Olfactory epithelium influences the orientation of mitral cell dendrites during development. Dev Dyn 232: 325-335.
16. Lin DM, Wang F, Lowe G, Gold GH, Axel R, et al. (2000) Formation of precise connections in the olfactory bulb occurs in the absence of odorant-evoked neuronal activity. Neuron 26: 69-80.
17. Chou YH, Spletter ML, Yaksi E, Leong JC, Wilson RI, et al. (2010) Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci 13: 439-449.
18. Sweeney LB, Chou YH, Wu Z, Joo W, Komiyama T, et al. (2011) Secreted semaphorins from degenerating larval ORN axons direct adult projection neuron dendrite targeting. Neuron 72: 734-747.
19. Yu CR, Power J, Barnea G, O'Donnell S, Brown HE, et al. (2004) Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42: 553-566.
20. Yoshida T, Uchida S, Mishina M, (2009) Regulation of synaptic vesicle accumulation and axon terminal remodeling during synapse formation by distinct Ca(2+) signaling. J Neurochem.
21. Chiang A, Priya R, Ramaswami M, Vijayraghavan K, Rodrigues V, (2009) Neuronal activity and Wnt signaling act through Gsk3-{beta} to regulate axonal integrity in mature Drosophila olfactory sensory neurons. Development 136: 1273-1282.
22. 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.
23. Ramaekers A, Magnenat E, Marin EC, Gendre N, Jefferis GS, et al. (2005) Glomerular maps without cellular redundancy at successive levels of the Drosophila larval olfactory circuit. Curr Biol 15: 982-992.
24. Kreher S, Kwon J, Carlson J, (2005) The molecular basis of odor coding in the Drosophila larva. Neuron 46: 445-456.
25. Gomez-Marin A, Stephens GJ, Louis M, (2011) Active sampling and decision making in Drosophila chemotaxis. Nature Communications 2: 441-410.
26. Kreher SA, Mathew D, Kim J, Carlson JR, (2008) Translation of sensory input into behavioral output via an olfactory system. Neuron 59: 110-124.
27. Hoare DJ, Mccrohan CR, Cobb M, (2008) Precise and fuzzy coding by olfactory sensory neurons. J Neurosci 28: 9710-9722.
28. Grillenzoni N, De Vaux V, Meuwly J, Vuichard S, Jarman A, et al. (2007) Role of proneural genes in the formation of the larval olfactory organ of Drosophila. Dev Genes Evol 217: 209-219.
29. Brand A, Perrimon N, (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development (Cambridge, England) 118: 401-415.
30. Certel S, Clyne P, Carlson JR, Johnson WA, (2000) Regulation of central neuron synaptic targeting by the Drosophila POU protein, Acj6. Development 127: 2395-2405.
31. Campos-Ortega Hartenstein (1985) The embryonic development of Drosophila melanogaster. Springer.
32. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K, (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8: 1263-1268.
33. Blankenship AG, Feller MB, (2009) Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 11: 18-29.
34. Dayan P, Abbott LF (2001) Theoretical neuroscience: computational and mathematical modeling of neural systems. Cambridge, MA: The MIT Press.
35. Sadeghi SG, Chacron MJ, Taylor MC, Cullen KE, (2007) Neural variability, detection thresholds, and information transmission in the vestibular system. J Neurosci 27: 771-781.
36. Larsson MC, Domingos AI, Jones WD, Chiappe ME, Amrein H, et al. (2004) Or83b encodes a broadly expressed odorant receptor essential for Drosophila olfaction. Neuron 43: 703-714.
37. Hummel T, Krukkert K, Roos J, Davis G, Klambt C, (2000) Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26: 357-370.
38. Potter CJ, Tasic B, Russler EV, Liang L, Luo L, (2010) The Q system: a repressible binary system for transgene expression, lineage tracing, and mosaic analysis. Cell 141: 536-548.
39. Baines RA, Uhler JP, Thompson A, Sweeney ST, Bate M, (2001) Altered electrical properties in Drosophila neurons developing without synaptic transmission. J Neurosci 21: 1523-1531.
40. Kremer MC, Christiansen F, Leiss F, Paehler M, Knapek S, et al. (2010) Structural long-term changes at mushroom body input synapses. Curr Biol 20 (21) (): 1938-1944.
41. Mauss A, Tripodi M, Evers JF, Landgraf M, (2009) Midline signalling systems direct the formation of a neural map by dendritic targeting in the Drosophila motor system. PLoS Biol 7: e1000200 doi:10.1371/journal.pbio.1000200.
42. Nitabach MN, Blau J, Holmes TC, (2002) Electrical silencing of Drosophila pacemaker neurons stops the free-running circadian clock. Cell 109: 485-495.
43. Lai SL, Lee T, (2006) Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat Neurosci 9: 703-709.
44. Tripodi M, Evers JF, Mauss A, Bate M, Landgraf M, (2008) Structural homeostasis: compensatory adjustments of dendritic arbor geometry in response to variations of synaptic input. PLoS Biol 6: e260 doi:10.1371/journal.pbio.0060260.
45. Harzsch S, Rieger V, Krieger J, Seefluth F, Strausfeld N, et al. (2011) Transition from marine to terrestrial ecologies: changes in olfactory and tritocerebral neuropils in land-living isopods. Arthropod Structure and Development pp. 1-14.
46. Byrd C, Burd G, (1993) The quantitative relationship between olfactory axons and mitral/tufted cells in developing Xenopus with partially deafferented olfactory bulbs. J Neurobiol 24: 1229-1242.
47. Salecker I, Boeckh J, (1996) Influence of receptor axons on the formation of olfactory glomeruli in a hemimetabolous insect, the cockroach Periplaneta americana. J Comp Neurol 370: 262-279.
48. Oland LA, Orr G, Tolbert LP, (1990) Construction of a protoglomerular template by olfactory axons initiates the formation of olfactory glomeruli in the insect brain. J Neurosci 10: 2096-2112.
49. Oland L, Pott W, Bukhman G, Sun XJ, Tolbert L, (1996) Activity blockade does not prevent the construction of olfactory glomeruli in the moth Manduca sexta. Int J Dev Neurosci 14: 983-996.
50. Mercer AR, Hildebrand JG, (2002) Developmental changes in the electrophysiological properties and response characteristics of Manduca antennal-lobe neurons. J Neurophysiol 87: 2650-2663.
51. Moody WJ, (1998) Control of spontaneous activity during development. J Neurobiol 37: 97-109.
52. Tritsch NX, Yi E, Gale JE, Glowatzki E, Bergles DE, (2007) The origin of spontaneous activity in the developing auditory system. Nature 450: 50-55.
53. Firth SI, Wang CT, Feller MB, (2005) Retinal waves: mechanisms and function in visual system development. Cell Calcium 37: 425-432.
54. Myers CP, Lewcock JW, Hanson MG, Gosgnach S, Aimone JB, et al. (2005) Cholinergic input is required during embryonic development to mediate proper assembly of spinal locomotor circuits. Neuron 46: 37-49.
55. Gonzalez-Islas C, Wenner P, (2006) Spontaneous network activity in the embryonic spinal cord regulates AMPAergic and GABAergic synaptic strength. Neuron 49: 563-575.
56. Fuchs E, Ayali A, Robinson A, Hulata E, Ben-Jacob E, (2007) Coemergence of regularity and complexity during neural network development. Dev Neurobiol 67: 1802-1814.
57. Yoshida T, Mishina M, (2005) Distinct roles of calcineurin-nuclear factor of activated T-cells and protein kinase A-cAMP response element-binding protein signaling in presynaptic differentiation. J Neurosci 25: 3067-3079.
58. Heimbeck G, Bugnon V, Gendre N, Haberlin C, Stocker R, (1999) Smell and taste perception in Drosophila melanogaster larva: toxin expression studies in chemosensory neurons. J Neurosci 19: 6599-6609.
59. Ben Fredj N, Hammond S, Otsuna H, Chien CB, Burrone J, et al. (2010) Synaptic activity and activity-dependent competition regulates axon arbor maturation, growth arrest, and territory in the retinotectal projection. J Neurosci 30: 10939-10951.
60. Wagh DA, Rasse TM, Asan E, Hofbauer A, Schwenkert I, 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.
61. Diegelmann S, Bate M, Landgraf M, (2008) Gateway cloning vectors for the LexA-based binary expression system in Drosophila. Fly (Austin) 2: 236-239.