A subpopulation of mushroom body intrinsic neurons is generated by protocerebral neuroblasts in the tobacco hornworm moth, Manduca sexta (Sphingidae, Lepidoptera)

Arthropod Structure and Development

Volumn 40, Issue 5, 2011, Pages 395-408

  Farris, Sarah M ^a   Pettrey, Colleen ^a   Daly, Kevin C ^a  

^a WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

Kenyon cell; Lepidoptera; Neuroblast; Neurogenesis

Indexed keywords

BROXURIDINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; IMMUNOHISTOCHEMISTRY; LARVAL STAGE; MANDUCA SEXTA; MUSHROOM BODY; NERVE FIBER; NERVOUS SYSTEM DEVELOPMENT; NEUROBLAST; NONHUMAN; PERIKARYON;

ANIMALS; CELL DIFFERENTIATION; LARVA; MANDUCA; MUSHROOM BODIES; NEUROGENESIS; NEURONS;

BASIDIOMYCOTA; HEXAPODA; LEPIDOPTERA; MANDUCA; MANDUCA SEXTA; SPHINGIDAE;

EID: 80052898559     PISSN: 14678039     EISSN: 18735495     Source Type: Journal    
DOI: 10.1016/j.asd.2010.10.004     Document Type: Article

References (61)

1. Armstrong J.D., deBelle J.S., Wang Z., Kaiser K. Metamorphosis of the mushroom bodies; large-scale rearrangements of the neural substrates for associative learning and memory in Drosophila. Learning and Memory 1998, 5:102-114.
2. Bell R.A., Joachim F.G. Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms. Annals of the Entomologial Society of America 1976, 69:365-372.
3. Blum A.L., Li W., Cressy M., Dubnau J. Short- and long-term memory in Drosophila require cAMP signaling in distinct neuron types. Current Biology 2009, 19:1341-1350.
4. Cayre M., Scotto-Lomassese S., Malaterre J., Strambi C., Strambi A. Understanding the regulation and function of adult neurogenesis: contribution from an insect model, the house cricket. Chemical Senses 2007, 32:385-395.
5. Cayre M., Strambi C., Charpin P., Augier R., Meyer M.R., Edwards J.S., Strambi A. Neurogenesis in adult insect mushroom bodies. Journal of Comparative Neurology 1996, 371:300-310.
6. Crittenden J.R., Skoulakis E.M.C., Han K.-A., Kalderon D., Davis R.L. Tripartite mushroom body architecture revealed by antigenic markers. Learning and Memory 1998, 5:38-51.
7. Daly K.C., Christensen T.A., Lei H., Smith B.H., Hildebrand J.G. Learning modulates the ensemble representations for odors in primary olfactory networks. Proceedings of the National Academy of Sciences USA 2004, 101:10476-10481.
8. Dufour M.C., Gadenne C. Adult neurogenesis in a moth brain. Journal of Comparative Neurology 2006, 495:635-643.
9. Ehmer B., Hoy R.R. Mushroom bodies of vespid wasps. Journal of Comparative Neurology 2000, 416:93-100.
10. Farris S.M. Developmental organization of the mushroom bodies of Thermobia domestica (Zygentoma, Lepismatidae): insights into mushroom body evolution from a basal insect. Evolution of Development 2005, 7:150-159.
11. Farris S.M. Evolution of insect mushroom bodies: old clues, new insights. Arthropod Structure and Development 2005, 34:211-234.
12. Farris S.M. Evolutionary convergence of higher brain centers spanning the protostome-deuterostome boundary. Brain Behavior and Evolution 2008, 72:106-122.
13. Farris S.M. Structural, functional and developmental convergence of the insect mushroom bodies with higher brain centers of vertebrates. Brain Behavior and Evolution 2008, 72:1-15.
14. Farris S.M. Tritocerebral tract input to the insect mushroom bodies. Arthropod Structure and Development 2008, 37:492-503.
15. Farris S.M., Abrams A.I., Strausfeld N.J. Development and morphology of Class II Kenyon cells in the mushroom bodies of the honey bee, Apis mellifera. Journal of Comparative Neurology 2004, 474:325-339.
16. Farris S.M., Robinson G.E., Davis R.L., Fahrbach S.E. Larval and pupal development of the mushroom bodies in the honey bee, Apis mellifera. Journal of Comparative Neurology 1999, 414:97-113.
17. Farris S.M., Sinakevitch I. Development and evolution of the insect mushroom bodies: towards the understanding of conserved developmental mechanisms in a higher brain center. Arthropod Structure and Development 2003, 32:79-101.
18. Farris S.M., Strausfeld N.J. Development of laminar organization in the mushroom bodies of the cockroach: Kenyon cell proliferation, outgrowth, and maturation. Journal of Comparative Neurology 2001, 439:331-351.
19. Farris S.M., Strausfeld N.J. A unique mushroom body substructure common to both basal cockroaches and to termites. Journal of Comparative Neurology 2003, 456:305-320.
20. Frambach I., Schürmann F. Separate distribution of deutocerebral projection neurons in the mushroom bodies of the cricket brain. Acta Biologica Hungarica 2004, 55:21-29.
21. Fukushima R., Kanzaki R. Modular subdivision of mushroom bodies by Kenyon cells in the silkmoth. Journal of Comparative Neurology 2009, 513:315-330.
22. Ganeshina O., Vorobyev M., Menzel R. Synaptogenesis in the mushroom body calyx during metamorphosis in the honeybee Apis mellifera: an electron microscopic study. Journal of Comparative Neurology 2006, 497:876-897.
23. Groh C., Rössler W. Caste-specific postembryonic development of primary and secondary olfactory centers in the female honeybee brain. Arthropod Structure and Development 2008, 37:459-468.
24. Gundersen R.W., Larsen J.R. Postembryonic development of the lateral protocerebral lobes, corpora pedunculata, deutocerebrum and tritocerebrum of Phormia regina Meigen (Diptera: Calliphoridae). Journal of Insect Morphology and Embryology 1978, 7:467-477.
25. Huetteroth W., el Jundi B., el Jundi S., Schachtner J. 3D-reconstructions and virtual 4D-visualization to study metamorphic brain development in the sphinx moth Manduca sexta. Frontiers in Systems Neuroscience 2010, 4:7.
26. Ito I., Bazhenov M., Ong R.C.-Y., Raman B., Stopfer M. Frequency transitions in odor-evoked neural oscillations. Neuron 2009, 64:692-706.
27. Ito K., Awano W., Suzuki K., Hiromi Y., Yamamoto D. 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 1997, 124:761-771.
28. Ito K., Hotta Y. Proliferation pattern of postembryonic neuroblasts in the brain of Drosophila melanogaster. Developmental Biology 1992, 149:134-148.
29. Jørgensen K., Kvello P., Almaas T.J., Mustaparta H. Two closely located areas in the suboesophageal ganglion and the tritocerebrum receive projections of gustatory receptor neurons lovated on the antennae and the proboscis in the moth Heliothis virescens. Journal of Comparative Neurology 2006, 496:121-134.
30. Kent K.S., Hildebrand J.G. Cephalic sensory pathways in the central nervous system of larval Manduca sexta (Lepidoptera: Sphingidae). Philosophical Transactions of the Royal Society of London B 1987, 315:1-36.
31. Kurusu M., Awasaki T., Masuda-Nakagawa L.M., Kawauchi H., Ito K., Furukubo-Tokunaga K. Embryonic and larval development of the Drosophila mushroom bodies: concentric layer subdivisions and the role of fasciclin II. Development 2002, 129:409-419.
32. Kurusu M., Nagao T., Walldorf U., Flister S., Gehring W.J., Furukuo-Tokunaga K. Genetic control of development of the mushroom bodies, the associative learning centers in the Drosophila brain, by the eyeless, twin of eyeless, and dachshund genes. Proceedings of the National Academy of Sciences USA 2000, 97:2140-2144.
33. Kvello P., Almaas T.J., Mustaparta H. A confined taste area in a lepidopteran brain. Arthropod Structure and Development 2006, 35:35-45.
34. Larsson M.C., Hansson B.S., Strausfeld N.J. A simple mushroom body in an African scarabid beetle. Journal of Comparative Neurology 2004, 478:219-232.
35. Lee T., Lee A., Luo L. Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 1999, 126:4065-4076.
36. Lei H., Riffel J.A., Gage S.L., Hildebrand J.G. Contrast enhancement of stimulus intermittency in a primary olfactory network and its behavioral significance. Journal of Biology 2009, 8:21.
37. Li Y.-S., Strausfeld N.J. Multimodal efferent and recurrent neurons in the medial lobes of cockroach mushroom bodies. Journal of Comparative Neurology 1999, 409:647-663.
38. Malaterre J., Strambi C., Chiang A.-S., Aouane A., Strambi A., Cayre M. Development of cricket mushroom bodies. Journal of Comparative Neurology 2002, 452:215-227.
39. Marin E.C., Watts R.J., Tanaka N.K., Ito K., Luo L. Developmentally programmed remodeling of the Drosophila olfactory circuit. Development 2005, 132:725-737.
40. O'Shea M., Adams M. Pentapeptide (proctolin) associated with an identified neuron. Science 1981, 213:567-569.
41. Panov A.A. General structure of the mushroom body calyx in Brachycera Orthorrhapha flies (Diptera). Biological Bulletin 2009, 36:267-276.
42. Panov A.A. How many neuroblasts build mushroom bodies in Lucilia caesar L. and Musca domestica L. (Diptera, Brachycera Cyclorrhapha)?. Biological Bulletin 2009, 36:598-606.
43. Pearson L. The corpora pedunculata of Sphinx ligustri L. and other Lepidoptera: an anatomical study. Philosophical Transactions of the Royal Society of London B 1971, 259:477-516.
44. Perez-Orive J., Mazor O., Turner G.C., Cassenaer S., Wilson R.I., Laurent G. Oscillations and sparsening of odor representation in the mushroom body. Science 2002, 297:359-365.
45. Rössler W., Oland L.A., Higgins M.R., Hildebrand J.G., Tolbert L.P. Development of a glia-rich axon-sorting zone in the olfactory pathway of the moth Manduca sexta. Journal of Neuroscience 1999, 19:9865-9877.
46. Sánchez-Villagra M.R., Sultan F. The cerebellum at birth in therian mammals, with special reference to rodents. Brain Behavior and Evolution 2002, 59:101-113.
47. Sjöholm M., Sinakevitch I., Ignell R., Strausfeld N.J., Hansson B.S. Organization of Kenyon cells in subdivisions of the mushroom bodies of a lepidopteran insect. Journal of Comparative Neurology 2005, 491:290-304.
48. Sjöholm M., Sinakevitch I., Strausfeld N.J., Ignell R., Hansson B.S. Functional division of intrinsic neurons in the mushroom bodies of male Spodoptera littoralis revealed by antibodies against aspartate, taurine, FMRF-amide, Mas-allatotropin and DC0. Arthropod Structure and Development 2006, 35:153-168.
49. Skoulakis E.M.C., Kalderon D., Davis R.L. Preferential expression in mushroom bodies of the catalytic subunit of protein kinase A and its role in learning and memory. Neuron 1993, 11:197-208.
50. Strausfeld N.J. Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes. Journal of Comparative Neurology 2002, 450:4-33.
51. Strausfeld N.J., Li Y.-S. Organization of olfactory and multimodal afferent neurons supplying the calyx and pedunculus of the cockroach mushroom bodies. Journal of Comparative Neurology 1999, 409:603-625.
52. Strausfeld N.J., Sinakevitch I., Vilinsky I. The mushroom bodies of Drosophila melanogaster: an immunocytological and Golgi study of Kenyon cell organization in the calyces and lobes. Microscopy Research and Technique 2003, 62:151-169.
53. Truman J.W. Metamorphosis of the central nervous system of Drosophila. Journal of Neurobiology 1990, 21:1072-1084.
54. Truman J.W., Ball E. Patterns of embryonic neurogenesis in a primitive wingless insect, the silverfish, Ctenolepisma longicaudata: comparison with those seen in flying insects. Development Genes and Evolution 1998, 208:357-368.
55. Truman J.W., Bate M. Spatial and temporal patterns of neurogenesis in the CNS of Drosophila melanogaster. Developmental Biology 1988, 125:146-157.
56. Urbach R., Technau G.M. Early steps in building the insect brain: neuroblast formation and segmental patterning in the developing brain of different insect species. Arthropod Structure and Development 2003, 32:103-123.
57. Urbach R., Technau G.M. Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 2003, 130:3621-3637.
58. van Swinderen B., Brembs B. Attention-like deficit and hyperactivity in a Drosophila memory mutant. Journal of Neuroscience 2010, 30:1003-1014.
59. Weiss M.J. Structural patterns in the corpora pedunculata of Orthoptera: a reduced silver analysis. Journal of Comparative Neurology 1981, 203:515-553.
60. Zhao X., Coptis V., Farris S.M. Metamorphosis and adult development of the mushroom bodies of the red flour beetle, Tribolium castaneum. Developmental Neurobiology 2008, 68:1487-1502.
61. Zhu S., Chiang A.-S., Lee T. Development of the Drosophila mushroom bodies: elaboration, remodeling and spatial organization of dendrites in the calyx. Development 2003, 130:2603-2610.