Skip to main content
Log in

Neurogenesis in the Insect Central Nervous System and Its Peculiarities in the Brain Mushroom Bodies

  • Published:
Entomological Review Aims and scope Submit manuscript

Abstract

Neurogenesis is divided into two main stages: proliferation and differentiation. Neural stem cells were discovered in insects almost a century and a half ago, in 1885, by A.A. Korotneff who called them ganglion cells, while the term neuroblast was introduced by W.M. Wheeler in 1891. Neurogenesis was initially considered a singlestage process, and the smaller daughter cells of the neuroblast were believed to differentiate directly into nerve cells. V. Bauer in 1904 described the ganglion mother cell as a distinct stage and thus established the two-stage nature of neurogenesis. More than a century later, it was found out that two-stage neurogenesis was not the only possible type, and one more, three-stage type was discovered. The latter includes an additional link between the neuroblast and the ganglion mother cell, termed the intermediate neural progenitor. Correspondingly, the traditional neuroblasts are currently termed type I neuroblasts, and those giving rise to intermediate neural progenitors are termed type II neuroblasts. The modern stage of neurogenesis research is characterized by the range of study objects narrowed down practically to a single species, Drosophila melanogaster, and also by application of a great variety of molecular genetic methods capable of revealing the finest mechanisms of neurogenesis. Four different patterns of solitary type I neuroblast activity during insect development have been revealed: (1) only during the embryonic stage; (2) continuously in embryos and larvae; (3) intermittent with a period of quiescence during the late embryonic and the early larval stage; (4) two independent generations of neuroblasts: embryonic and postembryonic. The initial stage of neurogenesis in the mushroom bodies is characterized by longer mitotic activity of neuroblasts and the presence of clusters of neuroblasts of different origins. Some neuroblasts of the mushroom bodies may be type II neuroblasts. A variety of Kenyon cells, the intrinsic cells of the mushroom bodies, is formed at the second stage of neurogenesis. Similar to the descendants of solitary neuroblasts in the cortex, the type of Kenyon cells depends on the time of their formation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

REFERENCES

  1. Alten, H., Zur Phylogenie des Hymenopterengehirns, Jena. Z. Naturwiss., 1910, vol. 46, no. 2, p. 511.

    Google Scholar 

  2. Armstrong, J.D., de Belle, J.S., Wang, Z., and Kaiser, K., Metamorphosis of the mushroom bodies: large-scale rearrangements of the neural substrates for associative learning and memory in Drosophila, Learn. Mem., 1998, vol. 5, p. 102.

  3. Aso, Y., Grübel, K., Busch, S., Friedrich, A.B., Siwanovicz, I., and Tanimoto, H., The mushroom body of adult Drosophila characterized by GAL4 drivers, J. Neurogenet., 2009, vol. 23, no. 1, p. 156.

  4. Aso, Y., Hatton, D., Yu, Y., Johnston, R., Alyer, N., et al., The neuronal architecture of the mushroom body provides a logic for associative learning, eLife, 2014, vol. 3: e04577.

  5. Baden, V., Embryology of the nervous system in the grasshopper, Melanoplus differentialis, J. Morphol., 1936, vol. 60, pp. 156−190.

  6. Barendrecht, G., Die Corpora pedunculata bei der Gattungen Bombus und Psythirus, Acta Zool., 1931, vol. 12, p. 153.

  7. Bate, C.M., Embryogenesis of an insect nervous system. I. A map of the thoracic and abdominal neuroblasts in Locusta migratoria, J. Embryol. Exp. Morphol., 1976, vol. 35, no. 1, p. 107.

  8. Bauer, V., Zur inneren Metamorphose des Zentralnervensystems der Insekten, Zool. Jahrb. Abt. Anat. Ontog. Tiere, 1904, vol. 20, p. 123.

    Google Scholar 

  9. Bayraktar, O.A., Boone, J.Q., Drummond, M.L., and Doe, C., Drosophila type II neuroblast lineages keep Prospero level low to generate large clones that contribute to the adult brain central complex, Neural Dev., 2010, vol. 5, no. 26, p. 3.

  10. Bello, B.C., Izergina, N., Caussinus, E., and Reichert, H., Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development, Neural Dev., 2008, vol. 3, no. 5, p. 1.

  11. Birkenholz, O., Rickert, C., Novak, J., Coban, I.C., and Technau, G.M., Bridging the gap between postembryonic cell lineages and identified embryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster, Biol. Open, 2015, vol. 4, p. 420.

  12. Booker, R. and Truman, J.W., Postembryonic neurogenesis in the CNS of the tobacco hornworm, Manduca sexta. I. Neuroblast arrays and the fate of their progeny during metamorphosis, J. Comp. Neurol., 1987, vol. 255, p. 548.

  13. Boone, J.Q. and Doe, C.Q., Identification of Drosophila type II neuroblast lineages containing transit amplifying ganglion mother cells, Dev. Neurobiol., 2008, vol. 68, no. 9, p. 1185.

  14. Butt, F.H., Embryology of the milkweed bug, Oncopeltus fasciatus (Heteroptera), Cornell Univ. Exp. St., 1949, no. 283, p. 1.

  15. Cayre, M., Strambi, C., and Strambi, A., Neurogenesis in an adult insect brain and its hormonal control, Nature, 1994, vol. 368, p. 57.

    Article  CAS  Google Scholar 

  16. Cayre, M., Strambi, C., Charpin, P., Augier, P., Meyer, M.R., et al., Neurogenesis in adult insect mushroom bodies, J. Comp. Neurol., 1996, vol. 371, p. 300.

    Article  CAS  PubMed  Google Scholar 

  17. Choksi, S.P., Southall, T.D., Bossing, T., Edoff, K., de Wit E., et al., Prospero acts as a binary switch between self-renewal and differentiation in Drosophila neural stem cells, Dev. Cell, 2006, vol. 11, p. 775.

  18. Crittenden, J.R., Skoulakis, E.M.C., Han, K.-A., Kaldron, D., and Davis, R.L., Tripartite mushroom body architecture revealed by antigenic markers, Learn. Mem., 1998, vol. 5, p. 38.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Dietl, M.J., Die Organisation des Arthropodengehirns, Z. Wiss. Zool., 1876, vol. 27, no. 4, p. 488.

    Google Scholar 

  20. Doe, C.Q., Molecular markers for identified neuroblasts and ganglion mother cells in the Drosophila central nervous system, Development, 1992, vol. 116, p. 855.

  21. Doe, C.Q., Neural stem cells: balancing self-renewal with differentiation, Development, 2008, vol. 135, p. 1575.

    Article  CAS  PubMed  Google Scholar 

  22. Doe, C.Q., Kuwada, Y., and Goodman, C.S., From epithelium to neuroblasts to neurons: the role of cell interactions and cell lineage during insect neurogenesis, Phil. Trans. R. Soc. London Biol. Sci., 1985, vol. 312, p. 67.

    Article  CAS  Google Scholar 

  23. Eastham, L.E.S., The embryology of Pieris rapae. Organo­geny, Phil. Trans. R. Soc. London Biol. Sci., 1930, vol. 219, p. 1.

  24. Escherich, K., Zur Entwicklung des Nervensystems der Musciden, mit besonderer Berücksichtigung des sog. Mittelstran­ges, Z. Wiss. Zool., 1902, vol. 71, p. 525.

    Google Scholar 

  25. Farris, S.M., Evolution of insect mushroom bodies: old clues, new insights, Arthropod Struct. Devel., 2005, vol. 34, no. 3, p. 211.

    Article  Google Scholar 

  26. Farris, S.M. and Strausfeld, N.J., Development of laminar organization in the mushroom bodies of the cockroach: Kenyon cell proliferation, outgrowth, and maturation, J. Comp. Neurol., 2001, vol. 439, no. 3, p. 331.

    Article  CAS  PubMed  Google Scholar 

  27. Farris, S.M. and Strausfeld, N.J., A unique mushroom body substructure common to basal cockroaches and termites, J. Comp. Neurol., 2003, vol. 456, no. 4, p. 305.

    Article  PubMed  Google Scholar 

  28. Farris, S.M., Robinson, G.E., Davis, R.L., and Fahrbach, S.E., Larval and pupal development of the mushroom bodies in the honeybee, Apis mellifera, J. Comp. Neurol., 1999, vol. 414, p. 97.

  29. Farris, S.M., Pettrey, C., and Daly, K.C., A subpopulation of mushroom body intrinsic neurons is generated by protocerebral neuroblasts in the tobacco hornworm moth, Manduca sexta (Sphingidae, Lepidoptera), Arthropod Struct. Devel., 2011, vol. 40, no. 5, p. 395.

  30. Fukushima, R. and Kanzaki, R., Modular subdivision of mush­room bodies by Kenyon cells in the silkmoth, J. Comp. Neurol., 2009, vol. 513, p. 315.

    Article  PubMed  Google Scholar 

  31. Hanström, B., Inkretorische Organe, Sinnesorgane und Nervensystem des Kopfes einiger niederer Insektenordnungen, Kungl. Svenska Vetenskapsakad. Handl. Ser. 3, 1940, vol. 18, no. 8, p. 1.

    Google Scholar 

  32. Harding, K. and White, K., Drosophila as a model for developmental biology: stem cell-decisions in the developing nervous system, J. Dev. Biol., 2018, vol. 6, no. 4, p. 1.

  33. Hartenstein, V. and Campos-Ortega, J.A., Early neurogenesis in wild-type of Drosophila melanogaster, Wilhelm Roux’ Arch. Entwicklungsmech. Org., 1984, vol. 193, p. 308.

  34. Hartenstein, V., Eberhardt, R., and Campos-Ortega, J.A., The pattern of proliferation of the neuroblasts in the wild-type embryo of Drosophila melanogaster, Wilhelm Roux’ Arch. Dev. Biol., 1987, vol. 196, no. 8, p. 473.

  35. Hatschek, B., Beiträge zur Entwicklungsgeschichte der Lepidopteren, Jena. Z. Naturwiss., 1877, vol. 11, no. 4, p. 115.

    Google Scholar 

  36. Heisenberg, M., Mutants of brain structure and function. What is the significance of the mushroom bodies for beha­viour? in Development and Biology of Drosophila, Siddiqi, O., Babu, P., Hall, L.M., and Hall, J.C., Ed., New York: Plenum Press, 1980, p. 337.

  37. Heymons, R., Die Embryonalentwicklung von Dermapteren und Orthopteren unter besonderer Berücksichtigung der Keim­blätterbildung, in Monographisch bearbeitet, Jena: Gustav Fischer, 1895.

  38. Hirschler, J., Die Embryonalentwicklung von Donacia crassipes L., Z. Wiss. Zool., 1909, vol. 92, no. 4, p. 627.

  39. Holguera, I. and Desplan, C., Neuronal specification in space and time, Science, 2018, vol. 326, no. 6411, p. 176.

    Article  CAS  Google Scholar 

  40. Homem, C.F. and Knoblich, J.A., Drosophila neuroblasts: a model for stem cell biology, Development, 2012, vol. 139, p. 4297.

  41. Ishii, Y., Kubota, K., and Hara, K., Postembryonic development of the mushroom bodies in the ant, Camponotus japonicus, Zool. Sci., 2005, vol. 22, p. 743.

  42. Jacobs, J.R., Hiromi, Y., Patel, N.H., and Goodman, C.S., Lineage, migration and morphogenesis of longitudinal glia in the Drosophila CNS as revealed by a molecular lineage marker, Neuron, 1989, vol. 2, no. 6, p. 1625.

  43. Johannsen, O.A. and Butt, F.H., Embryology of Insects and Myriapods, New York: McGraw-Hill, 1941.

  44. Johansson, A.S., The nervous system of the milkweed bug, Oncopeltus fasciatus (Dallas) (Heteroptera, Lygaeidae), Trans. Am. Entomol. Soc., 1957, vol. 83, no. 3, p. 119.

  45. Jonescu, C.N., Vergleichende Untersuchungen über das Gehirn der Honigbiene, Jena. Z. Naturwiss., 1909, vol. 45, p. 111.

    Google Scholar 

  46. Kaneko, K., Ikeda, T., Nagai, M., Hori, S., Umatani, C., et al., Novel middle-type Kenyon cells in the honeybee brain revealed by area-preferential gene expression analysis, PLoS ONE, 2013, vol. 8, no. 8: e71732. https://doi.org/10.1371/journal.pone.0071732

  47. Kaneko, K., Suenami, S., and Kubo, T., Gene expression profiles and neural activities of Kenyon cell subtypes in the honey­bee brain: identification of novel “middle-type” Kenyon cells, Zool. Lett., 2016, vol. 2, p. 1. https://doi.org/10.1186/s40851-016-0051-6

    Article  Google Scholar 

  48. Kenyon, F.C., The brain of the bee. A preliminary contribution to the morphology of the nervous system of the Arthropoda, J. Comp. Neurol., 1896, vol. 6, p. 133.

    Article  Google Scholar 

  49. Knoblich, J.A., Mechanisms of asymmetric stem cell division, Cell, 2008, vol. 132, p. 583.

    Article  CAS  PubMed  Google Scholar 

  50. Kohwi, M. and Doe, C.Q., Temporal fate specification and neural progenitor competence during development, Nat. Rev. Neurosci., 2013, vol. 14, no. 12, p. 823.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Korotneff, A., Die Embryologie der Gryllotalpa, Z. Wiss. Zool., 1885, vol. 41, no. 4, p. 570.

  52. Kowalevski, A.O., Embryologische Studien an Würmern und Arthropoden, Mém. Acad. Imp. Sci. St. Pétersbourg 7 Sér., 1871, vol. 16, no. 12, p. 1.

    Google Scholar 

  53. Köllisch, G.V., Hoffmann, K.H., Strambi, A., and Strambi, C., Postembryonic mushroom body development in a migrating butterfly, Vanessa cardui (Lepidoptera: Nymphalidae), Entomon, 2002, vol. 27, no. 2, p. 117.

  54. Kunz, T., Kraft, K.F., Technau, G.M., and Urbach, R., Origin of Drosophila mushroom body neuroblasts and generation of divergent embryonic lineages, Development, 2012, vol. 139, p. 2510.

  55. Larsson, M.C., Hansson, B.S., and Strausfeld, N.J., A simple mushroom body in an African scarabid beetle, J. Comp. Neurol., 2004, vol. 478, p. 219.

    Article  PubMed  Google Scholar 

  56. Lécaillon, A., Recherches sur le développement embryonnaire de quelques chrysomélides, Arch. Anat. Micr. Morphol. Exp., 1898, vol. 2, p. 118.

    Google Scholar 

  57. Lee, T., Lee, A., and Luo, L., Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast, Development, 1999, vol. 126, p. 4065.

  58. Lovick, J.K., Ngo, K.T., Omoto, J.J., Wong, D.C., Nguyen, J.D., and Hartenstein, V., Postembryonic lineages of the Droso­phila brain: I. Development of the lineage-associated fiber tracts, Dev. Biol., 2013, vol. 384, p. 228.

  59. Malaterre, J., Strambi, C., Chiang, A.-Sh., Aouane, A., Strambi, A., and Cayre, M., Development of cricket mushroom bodies, J. Comp. Neurol., 2002, vol. 452, p. 215.

    Article  PubMed  Google Scholar 

  60. Malun, D., Early development of mushroom bodies in the brain of the honeybee Apis mellifera as revealed by BrdU incorporation and ablation experiments, Learn. Mem., 1998, vol. 5, no. 1, p. 90.

  61. Malzacher, P., Die Embryogenese des Gehirns paurometaboler Insekten. Untersuchungen an Carausius morosus und Peri­planeta americana, Z. Morphol. Ökol. Tiere, 1968, vol. 62, no. 2, p. 103.

  62. Mashaly, A., Winkler, M., Frambach, I., Gras, H., and Schürmann, F.-W., Sprouting interneurons in mushroom bodies of adult cricket brain, J. Comp. Neurol., 2008, vol. 508, p. 153.

    Article  PubMed  Google Scholar 

  63. Mizunami, M., Iwasaki, M., Okada, R., and Nishikawa, M., Topography of four classes of Kenyon cells in the mushroom bodies of the cockroach, J. Comp. Neurol., 1998, vol. 399, p. 162.

    Article  CAS  PubMed  Google Scholar 

  64. Mobbs, P.G., The brain of the honeybee, Apis mellifera L. The connections and spatial organization of the mushroom bodies, Phil. Trans. R. Soc. London Biol. Sci., 1982, vol. 298, p. 309.

  65. Nelson, J.A., The Embryology of the Honey Bee, Princeton: Princeton Univ. Press, 1915.

  66. Neumüller, R.A. and Knoblich, J.A., Dividing cellular asymmetry: asymmetric cell division and its implication for stem cells and cancer, Genes Dev., 2009, vol. 23, no. 23, p. 2675.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  67. Nordlander, R.H. and Edwards, J.S., Postembryonic brain development in the monarch butterfly, Danaus plexippus plexippus L. I. Cellular events during brain morphogenesis, Wilhelm Roux’ Arch. Entwicklungsmech. Org., 1969, vol. 162, p. 197.

  68. Nordlander, R.H. and Edwards, J.S., Postembryonic brain development in the monarch butterfly, Danaus plexippus plexippus L. III. Morphogenesis of centers other than the optic lobes, Wilhelm Roux’ Arch. Entwicklungsmech. Org., 1970, vol. 164, p. 247.

  69. Oya, S., Kohno, H., Kainoh, Y., Ono, M., and Kubo, T., Increased complexity of mushroom body Kenyon cell subtypes in the brain is associated with behavioral evolution in hymeno­pteran insects, Sci. Rep., 2017, vol. 7: 13785. https://doi.org/10.1038/s41598-017-14174-6

  70. Panov, A.A., Structure of the insect brain at the successive stages of postembryonic development, Entomol. Obozr., 1957, vol. 36, no. 2, p. 269.

    Google Scholar 

  71. Panov, A.A., Proliferation patterns of neuroblasts and neurilemma and neuroglia cells in the brain of the Chinese tussar moth larva, Dokl. Akad. Nauk SSSR, 1960, vol. 132, no. 3, p. 689.

    Google Scholar 

  72. Panov, A.A., The origin and fate of neuroblasts, neurons, and neuroglia cells in the central nervous system of the Chinese tussar moth Antheraea pernyi Guér. (Lepidoptera, Attacidae), Entomol. Obozr., 1963, vol. 42, no. 2, p. 337.

  73. Panov, A.A., Comparison of the central nervous system ontogenesis in the house cricket Gryllus domesticus L. and the European mole cricket Gryllotalpa gryllotalpa L. (Ortho­ptera, Grylloidea), Entomol. Obozr., 1966, vol. 45, no. 2, p. 326.

  74. Panov, A.A., Morphology of the mushroom bodies in Sca­rabaeoidea (Coleoptera). II. Herbivorous lamellicorn beetles and general discussion, Izv. Ross. Akad. Nauk Ser. Biol., 2010, no. 6, p. 683.

    Google Scholar 

  75. Panov, A.A., Leaf beetles (Coleoptera: Chrysomelidae): simplification of mushroom bodies in the course of progressive evolution of the family, Izv. Ross. Akad. Nauk Ser. Biol., 2012, no. 1, p. 35.

    Google Scholar 

  76. Panov, A.A., Histological structure of the tripartite mushroom bodies in ground beetles (Insecta: Coleoptera: Carabidae), Izv. Ross. Akad. Nauk Ser. Biol., 2013, no. 5, p. 574.

    Google Scholar 

  77. Panov, A.A., A novel, unusual (at least for beetles) mode of Kenyon cell production in the diving beetle Cybister lateralimarginalis Deg. (Coleoptera: Dytiscidae), Izv. Ross. Akad. Nauk Ser. Biol., 2014, no. 2, p. 150.

  78. Panov, A.A., Neuroblasts forming mushroom bodies in Lepido­ptera (Insecta), Izv. Ross. Akad. Nauk Ser. Biol., 2018, no. 5, p. 519.

    Google Scholar 

  79. Panov, A.A., Proliferation and differentiation: two sequential stages of proliferative center activity in the embryonic mushroom bodies of the crickets Gryllus bimaculatus and Acheta domesticus and the desert locust Schistocerca gregaria (Insecta: Orthoptera), Izv. Ross. Akad. Nauk Ser. Biol., 2019, no. 3, p. 273.

  80. Panov, A.A., Tens versus four: two generations of neural progenitors in the developing mushroom bodies of Muscina prolapsa Harris (Diptera, Muscidae), Entomol. Rev., 2020, vol. 100, no. 6, p. 745.

  81. Panov, A.A., The mushroom bodies of phasmids (Phasmatodea, Insecta): structure and sources of development, Izv. Ross. Akad. Nauk Ser. Biol., 2021, no. 1, p. 83.

    Google Scholar 

  82. Pearson, L., The corpora pedunculata of Sphinx ligustri L. and other Lepidoptera: an anatomical study, Phil. Trans. R. Soc. London Biol. Sci., 1971, vol. 259, p. 477.

  83. Pereanu, W., Shy, D., and Hartenstein, V., Morphogenesis and proliferation of the larval brain glia in Drosophila, Dev. Biol., 2005, vol. 283, no. 1, p. 191.

  84. Prokop, A. and Technau, G.M., The origin of postembryonic neuroblasts in the ventral nerve cord of Drosophila melanogaster, Development, 1991, vol. 111, no. 1, p. 79.

  85. Pyle, R.W., Changes in the Nervous System of Lepidoptera during Metamorphosis, Theses, Harvard University. Department of Biology, Cambridge, Massachusetts, 1941.

  86. Risler, H., Die somatische Polyploidie in der Entwicklung der Honigbiene (Apis mellifica) und die Wiederherstellung der Diploidie bei den Drohnen, Z. Zellforsch. Mikr. Anat., 1954, vol. 41, no. 1, p. 1.

  87. Roberts, H.S., The mechanism of cytokinesis in neuroblasts of Chortophaga viridifasciata (DeGeer), J. Exp. Zool., 1955, vol. 130, no. 1, p. 83.

  88. Roonwal, M.L., Studies on the embryology of the African migratory locust, Locusta migratoria migratorioides. II. Organogeny, Phil. Trans. R. Soc. London Biol. Sci., 1937, vol. 227, p. 157.

  89. Schmidt, H., Rickert, C., Bossing, T., Vef, O., Urban, J., and Technau, G.M., The embryonic central nervous system lineages of Drosophila melanogaster. II. Neuroblast lineages derived from the dorsal part of the neuroectoderm, Dev. Biol., 1997, vol. 189, no. 2, p. 186.

  90. Schrader, K., Untersuchungen über die Normalentwicklung des Gehirns und Gehirntransplantationen bei der Mehlmotte Ephestia kühniella Zeller nebst einigen Bemerkungen über das Corpus allatum, Biol. Zentralbl., 1938, vol. 58, p. 52.

  91. Schürmann, F.-W., Über die Struktur der Pilzkörper des Insektengehirns. III. Die Anatomie der Nervenfasern in der Corpora pedunculata bei der Acheta domesticus L. (Orthoptera): Eine Golgi Studie, Z. Zellforsch. Mikr. Anat., 1973, vol. 145, p. 247.

  92. Sheperd, D. and Bate, C.M., Spatial and temporal patterns of neurogenesis in the embryo of the locust (Schistocerca gregaria), Development, 1990, vol. 108, p. 83.

  93. Sjöholm, M., Sinakevitch, I., Ingell, R., Strausfeld, N.J., and Hansson, B.S., Organization of Kenyon cells in subdivisions of the mushroom bodies of a lepidopteran insect, J. Comp. Neurol., 2005, vol. 491, p. 290.

    Article  PubMed  Google Scholar 

  94. Sjöholm, M., Sinakevitch, I., Strausfeld, N.J., Ignell, R., and Hansson, B.S., Functional divisions of intrinsic neurons in the mushroom bodies of male Spodoptera littoralis, revealed by antibodies against aspartate, taurine, FMRF-amide, Masallatotropin, and DC0, Arthropod Struct. Devel., 2006, vol. 35, p. 153.

  95. Skeath, J.B. and Carroll, S.B., Regulation of proneural gene expression and cell fate during neuroblast segregation in the Drosophila embryo, Development, 1992, vol. 114, p. 939.

  96. Strausfeld, N.J., Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes, J. Comp. Neurol., 2002, vol. 450, p. 4.

    Article  PubMed  Google Scholar 

  97. Strausfeld, N.J., Sinakewitch, I., and Vilinsky, I., The mushroom bodies of Drosophila melanogaster: an immuno­cytological and Golgi study of Kenyon cells organization in the calyces and lobes, Microsc. Res. Tech., 2003, vol. 62, p. 151.

  98. Strindberg, H., Embryologische Studien an Insekten, Z. Wiss. Zool., 1913, vol. 106, p. 1.

    Google Scholar 

  99. Tiegs, O.W. and Murray, F.V., The Embryonic Development of Calandra oryzae, Q. J. Microsc. Sci., 1938, vol. 80, p. 159.

  100. Trebels, B., Doppel, S., Schaaf, M., Balakrishnan, K., Wimmer, E.A., and Schachtner, J., Adult neurogenesis in the mushroom bodies of red flour beetles (Tribolium castaneum Herbst) is influenced by the olfactory environment, Sci. Rep., 2020, vol. 10, art. 1090. https://doi.org/10.1038/s41598-020-57639-x

  101. Urbach, R., Schnabel, R., and Tchnau, G.M., The pattern of neuroblast formation, mitotic domains and proneural gene expression during early brain development in Drosophila, Development, 2003, vol. 130, p. 3589.

  102. Viallanes, M.H., Etudes histologiques et organologiques sur les centres nerveux. V. Le cerveau du criquet (Oedipoda coerulescens et Calliptamus italicus), Ann. Sci. Nat. Zool. 7me Sér., 1887, vol. 4, p. 1.

  103. Viallanes, H., Sur quelques pointes de l’histoire du développement embryonnaires de la mante religieuse (Mantis religiosa). Communication préliminaire, Rev. Biol. Nord Fr., 1890, vol. 2, p. 479.

  104. Viallanes, H., Sur quelques pointes de l’histoire du développement embryonnaires de la mante religieuse (Mantis religiosa), Ann. Sci. Nat. Zool. 7me Sér., 1891, vol. 11, p. 283.

  105. Weiss, M.J., Neuronal connections and the function of the corpora pedunculata in the brain of the American cockroach, Periplaneta americana, J. Morphol., 1974, vol. 142, p. 21.

  106. Weiss, M.J., Structural patterns in the corpora pedunculata of Orthoptera: a reduced silver analysis, J. Comp. Neurol., 1981, vol. 203, p. 515.

    Article  CAS  PubMed  Google Scholar 

  107. Wheeler, W.M., The embryology of Blatta germanica and Doryphora decemlineata, J. Morphol., 1889, vol. 3, no. 2, p. 291.

  108. Wheeler, W.M., Neuroblasts in the arthropod embryo, J. Morphol., 1891, vol. 4, no. 3, p. 337.

    Article  Google Scholar 

  109. Wheeler, W.M., A contribution to insect embryology, J. Morphol., 1893, vol. 8, no. 1, p. 1.

    Article  Google Scholar 

  110. Wong, D.C., Lovick, J.K., Ngo, K.T., Borisuthirattana, W., Omoto, J.J., and Hartenstein, V., Postembryonic lineages of the Drosophila brain: II. Identification of the lineage pro­jection patterns based on MARCM clones, Dev. Biol., 2013, vol. 384, p. 258.

  111. Yang, M.Y., Armstrong, J.D., Vilinsky, I., Strausfeld, N.J., and Kaiser, K., Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns, Neuron, 1995, vol. 15, p. 45.

  112. Yasugi, T. and Nishimura, T., Temporal regulation of the generation of neuronal diversity in Drosophila, Dev. Growth Differ., 2016, vol. 58, p. 73.

  113. Zhang, H.-L., Huang, Y., Lin, L.-L., Wang, X.-Y., and Zheng, Z.-M., The phylogeny of the Orthoptera (Insecta) as deduced from mitogenomic gene sequences, Zool. Stud., 2013, vol. 52, no. 37, p. 1.

    Article  CAS  Google Scholar 

  114. Zhao, X., Coptis, V., and Farris, S.M., Metamorphosis and adult development of the mushroom bodies of the red flour beetle, Tribolium castaneum, Dev. Neurobiol., 2008, vol. 68, p. 1487.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. A. Panov.

Ethics declarations

Statement on the welfare of animals. All the applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All the procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Panov, A.A. Neurogenesis in the Insect Central Nervous System and Its Peculiarities in the Brain Mushroom Bodies. Entmol. Rev. 102, 141–160 (2022). https://doi.org/10.1134/S0013873822020014

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0013873822020014

Keywords: