Synaptic Connections of Cholinergic Antennal Lobe Relay Neurons Innervating the Lateral Horn Neuropile in the Brain of Drosophila melanogaster

Journal of Comparative Neurology

Volumn 466, Issue 3, 2003, Pages 299-315

  Yasuyama, Kouji ^a,b   Meinertzhagen, Ian A ^a   Schürmann, Friedrich Wilhelm ^a,c  

^a DALHOUSIE UNIVERSITY   (Canada)

^b KAWASAKI MEDICAL SCHOOL   (Japan)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Choline acetyltransferase; Cholinergic projection neurons; Fruit fly; GABA; Mushroom body; Olfactory system; Synapses; Synaptic bouton

Indexed keywords

CHOLINE ACETYLTRANSFERASE;

ANIMAL TISSUE; ANTENNA; ANTIBODY LABELING; ARTICLE; BRAIN MAPPING; BRAIN REGION; CHOLINERGIC NERVE CELL; DROSOPHILA MELANOGASTER; ELECTRON MICROSCOPY; IMMUNOCYTOCHEMISTRY; IMMUNOELECTRON MICROSCOPY; IMMUNOREACTIVITY; INFORMATION PROCESSING; INNERVATION; INTERNEURON; MUSHROOM BODY; NERVE ENDING; NERVE FIBER; NERVE PROJECTION; NERVE TRACT; NEUROPIL; NONHUMAN; OLFACTORY SYSTEM; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SENSORY STIMULATION; SPINAL CORD; SYNAPSE; ULTRASTRUCTURE;

ANIMALS; BRAIN; BRAIN CHEMISTRY; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC FIBERS; DROSOPHILA MELANOGASTER; MUSHROOM BODIES; NEURONS; NEUROPIL; SYNAPSES;

EID: 0142094643     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10867     Document Type: Article

References (64)

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. Altman JS, Kien J. 1979. Suboesophageal neurons involved in head movements and feeding in locusts. Proc R Soc Lond B 205:209-227.
3. Anton S, Homberg U. 1999. Antennal lobe structure. In: Hansson BS, editor. Insect olfaction. Berlin: Springer. p 97-124.
4. Anton S, Ignell R, Hansson BS. 2002. Developmental changes in the structure and function of the central olfactory system in gregarious and solitary desert locusts. Microsc Res Tech 56:281-291.
5. Atwood HL, Govind CK, Wu C-F. 1993. Differential ultrastructure of synaptic terminals on ventral longitudinal abdominal muscles in Drosophila larvae. J Neurobiol 24:1008-1024.
6. Boeckh J, Ernst KD, Sass H, Waldow U. 1984. Anatomical and physiological characteristics of individual neurons in the central antennal pathway of insects. J Insect Physiol 30:15-26.
7. Breer H. 1987. Neurochemical aspects of cholinergic synapses in the insect brain. In: Gupta AP, editor. Arthropod brain: its evolution, development, structure and functions. New York: John Wiley & Sons. p 415-437.
8. Bullock TH, Horridge GA. 1965. Structure and function in the nervous systems of invertebrates, vol. II. San Francisco: WH Freeman.
9. Burrows M. 1996. The neurobiology of an insect brain. Oxford: Oxford University Press.
10. Crittenden JR, Skoulakis EMC, Han K-A, Kalderon D, Davis RL. 1998. Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 5:38-51.
11. de Belle JS, Heisenberg M. 1994. Associative odor learning in Drosophila abolished by chemical ablation ofmushroom bodies. Science 263:692-695.
12. de Belle JS, Kanzaki R. 1999. Protocorebral olfactory processing. In: Hansson BS, editor. Insect olfaction. Berlin: Springer. p 242-281.
13. De Camilli P, Haucke V, Takei, Mugnaini E. 2001. The structure of synapses. In: Cowan WM, Südhof TC, Stevens CF, Davies K, editors. Synapses. Baltimore: Johns Hopkins University Press. p 89-133.
14. Erber J, Masuhr T, Menzel R. 1980. Localization of short-term memory in the brain of the bee. Physiol Entomol 5:343-358.
15. Fiala A, Spall T, Diegelmann S, Eisermann B, Sachse S, Devaud J-M, Buchner E, Galizia CG. 2002. Genetically expressed Cameleon in Drosophila melanogaster is used to visualize olfactory information in projection neurons. Curr Biol 12:1877-1884.
16. Fuchs E, Dustmann JH, Stadler H, Schürmann FW. 1989. Neuroactive compounds in the brain of the honeybee during imaginal life. Comp Biochem Physiol 92C:337-342.
17. Heimbeck G, Bugnon V, Gendre N, Keller A, Stocker RF. 2001. A central neural circuit for experience-independant olfactory and courtship behaviour in Drosophila melanogaster. Proc Natl Acad Sci U S A 98: 15336-16341.
18. Heisenberg M. 1980. Mutants of brain structure and function: what is the significance of the mushroom bodies in behavior. In: Siddiqui O, Babu P, Hall LM, Hall IC, editors. Development and neurobiology of Drosophila. New York: Plenum Press. p 373-390.
19. Heisenberg M. 1998. What do the mushroom bodies do for the insect brain? An introduction. Learn Mem 5:1-10.
20. Heisenberg M, Heusipp M, Wanke C. 1995. Structural plasticity in the Drosophila brain. J Neurosci 15:1951-1960.
21. Hill ES, Iwano M, Gatellier L, Kanzaki R. 2002. Morphology and physiology of the serotonin-immunoreactive putative antennal lobe feedback neuron in the male silkmoth Bombyx mori. Chem Senses 27:475-483.
22. Homberg U. 1994. Distribution of neurotransmitters in the insect brain. In: Rathmayer W, editor. Progress in zoology, vol. 40. Stuttgart: Gustav Fischer. p 1-88.
23. Homberg U. 2002. Neurotransmitters and neuropeptides in the brain of the locust. Microsc Res Tech 56:189-209.
24. Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto D. 1997. 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 124:761-771.
25. 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.
26. Kien J, Williams M. 1983. Morphology of neurons in locust brain and suboesophageal ganglion involved in initiation and maintenance of walking. Proc R Soc Lond B 219:175-192.
27. Killmann F, Schürmann F-W. 1985. Both electrical and chemical transmission between lobula giant movement detector and the descending contralateral movement detector neurons of locusts are supported by electron microscopy. J Neurocytol 14:637-652.
28. Killmann F, Gras H, Schürmann F-W. 1999. Types, numbers and distribution of synapses on the dendritic tree of an identified visual interneuron in the brain of the locust. Cell Tissue Res 296:645-665.
29. Leitinger G, Simmons PJ. 2000. Cytochemical evidence that acetylcholine is a neurotransmitter of neurons that make excitatory and inhibitory outputs in the locust ocellar visual system. J Comp Neurol 416:345-355
30. Marin EC, Jefferis GSXE, Komiyama T, Zhu H, Luo L. 2002. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109:243-255.
31. Meinertzhagen IA. 1996. Ultrastructure and quantification of synapses in the insect nervous system. J Neurosci Methods 69:59-73.
32. 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.
33. Meinertzhagen IA, Sorra KE. 2001. Synaptic organisation in the fly's optic lamina: few cells, many synapses and divergent microcircuits. In: Kolb H, Ripps H, Wu S, editors. Concepts and challenges in retinal biology: a tribute to John E. Dowling (Progress in Brain Research, Volume 131). Amsterdam: Elsevier. p 53-69.
34. Menzel R, Müller U. 1996. Learning and memory in honeybees: from behavior to neural substrates. Annu Rev Neurosci 19:379-404.
35. Müller D, Abel R, Brandt R, Zöckter Zbckler M, Menzel R. 2002. Differential parallel processing of olfactory information in the honeybee, Apis mellifera. J Comp Physiol A 188:359-370.
36. Nässel DR. 1993. Neuropeptides in the insect brain: a review. Cell Tissue Res 273:1-29
37. Nishino H, Yamashita S, Yamazaki Y, Nishikawa M, Yokohari F, Mizunami M. 2003. Projection neurons originating from thermo- and hygrosensory glomeruli in the antennal lobe of the cockroach. J Comp Neurol 455:40-55.
38. 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.
39. Python F, Stocker RF. 2002. Immunoreactivity against choline acetyltransferase, γ-aminobutyric acid, histamine, octopamine, and serotonin in the larval chemosensory system of Drosophila melanogaster. J Comp Neurol 453:157-167.
40. Rein K, Zöckler M, Mader MT, Grübel C, Heisenberg M. 2002. The Drosophila standard brain. Curr Biol 12:227-231.
41. Schildberger K. 1984. Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J Comp Physiol A 154:71-79.
42. Schürmann F-W. 1973. Ober die Struktur der Pilzkörper des Insektengehirns. III. Die Anatomie der Nervenfasern in den Corpora pedunculata bei Acheta domesticus L (Orthopt.). Z Zellforsch 145: 247-285.
43. Schürmann F-W. 1987. The architecture of the mushroom bodies and related neuropils in the insect brain. In: Gupta AP, editor. Arthropod brain: its evolution, development, structure and functions. New York: John Wiley & Sons. p 231-264.
44. Simmons PJ, Littlewood PMH. 1989. Structure of a tonically transmitting synapse between identified interneurons in the locust brain. J Comp Neurol 283:129-249.
45. Stocker RF, Leinhard MC, Borst A, Fischbach K-F. 1990. Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262:9-34.
46. 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.
47. Strausfeld NJ. 1976. Atlas of an insect brain. Berlin: Springer.
48. Strausfeld NJ, Bassemir UK. 1985a. The organization of giant horizontal-motion-sensitive neurons and their synaptic relationships in the lateral deutocerebrum of Calliphora eythrocephala and Musca domestica. Cell Tissue Res 242:531-550.
49. Strausfeld NJ, Bassemir UK. 1985b. Lobula plate and ocellar interneurons converge onto a cluster of descending neurons leading to neck and leg neuropil in Calliphora eythrocephala. Cell Tissue Res 240:617-640.
50. Strausfeld NJ, Meinertzhagen IA. 1998. The insect neuron: types morphologies fine structure and relationship to the architectonics of the insect nervous system. In: Harrison FW, Locke M, editors. Microscopic anatomy of invertebrates, vol. 11(B). Insecta. New York: John Wiley & Sons. p 487-538.
51. Strausfeld NJ, Hansen L, Li YS, Gomez RS, Ito K. 1998. Evolution discovery and interpretations of arthropod mushroom bodies. Learn Mem 5:11-37.
52. 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.
53. Takagawa K, Salvaterra PM. 1996. Analysis of choline acetyltransferase protein in temperature sensitive mutant flies using newly generated monoclonal antibody. Neurosci Res 24:237-243.
54. Tyrer NM, Gregory GE. 1982. A guide to the neuroanatomy of locust suboesophageal and thoracic ganglia. Philos Trans R Soc Lond B 297: 91-123.
55. Watson AHD, Pflüger H-J. 1989. Regional specialisation for synaptic input and output on a locust intersegmental interneurone with multiple spike-initiating zones. J Comp Neurol 279:515-527.
56. Watson AHD, Schürmann F-W. 2002. Synaptic structure distribution and circuitry in the central nervous system of the locust and related insects. Microsc Res Tech 56:210-226.
57. Witthöft W. 1967. Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. Z Morph Tiere 61:160-184.
58. Wong AM, Wang JW, Axel R. 2002. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109:229-241.
59. Yasuyama K, Salvaterra PM. 1999. Localization of choline acetyltransferase-expressing neurons in Drosophila nervous system. Microsc Res Tech 45:65-79.
60. Yasuyama K, Kitamoto T, Salvaterra PM. 1995. Immunocytochemical study ofcholine acetyltransferase in Drosophila melanogaster: an analysis of cis-regulatory regions controlling expression in the brain of cDNA-transformed flies. J Comp Neurol 361:25-37.
61. Yasuyama K, Kitamoto T, Salvaterra PM. 1996. Differential regulation of choline acetyltransferase expression in adult Drosophila melanogaster brain. J Neurobiol 30:205-218.
62. Yasuyama K, Meinertzhagen IA, Schürmann F-W. 2002. Synaptic organization of the mushroom body calyx in Drosophila melanogaster. J Comp Neurol 445:211-226.
63. Younossi-Hartenstein A, Salvaterra PM, Hartenstein V. 2003. Early development of the Drosophila brain. IV. Larval neuropile compartments defined by glial septa. J Comp Neurol 455:435-450.
64. Zars T. 2000. Behavioral functions of the insect mushroom bodies. Curr Opin Neurobiol 10:790-795.