Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster

Technau, Gerhard M.; Heisenberg, Martin

doi:10.1038/295405a0

Cited by 263 publications

(176 citation statements)

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“…Overall MB morphology remains stable throughout metamorphosis. However, the number of axons, counted in crosssections through the peduncle, plummets dramatically at the onset of metamorphosis, without loss of cell bodies, and then increases as pupal development proceeds (Technau and Heisenberg, 1982). These ultrastructural data indicate that many Kenyon cell axons undergo retraction, followed by regeneration.…”

mentioning

confidence: 70%

“…␤Gal expression was examined in the late larval CNS of progeny of crosses between the reporter UAS GlacZ and each of six P[GAL4] lines (30Y, 72Y, 201Y, c35, c739, and c747). At this time, the MBs contain ϳ2200 Kenyon cells per side (Technau and Heisenberg, 1982;Technau, 1984). In all lines except 201Y, extensive reporter gene expression was seen outside the MB (data not shown).…”

Section: Y Shows Mb-selective Expression In the Brain During Metammentioning

confidence: 97%

“…Additional neurons are stained in the ventral ganglion (VG), but this region was excluded by dissection when establishing dissociated pupal cultures. Diagram, lower left corner, An oblique anterior view of an MB (adapted from Technau and Heisenberg, 1982;Yang et al, 1995). A single intrinsic neuron is depicted, showing the axonal projection into the lobes and the dendritic arbor within the calyx.…”

Section: Methodsmentioning

confidence: 99%

“…Our initial focus has been on Kenyon cells, the intrinsic neurons of the mushroom bodies (MBs), because they represent the single largest neuronal population whose metamorphic transition in vivo has been described in Drosophila (Technau and Heisenberg, 1982). The MBs command considerable interest because they are essential for higher order sensory integration as well as learning and memory (de Belle, 1995;Davis and Han, 1996).…”

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confidence: 99%

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The Steroid Hormone 20-Hydroxyecdysone Enhances Neurite Growth ofDrosophilaMushroom Body Neurons Isolated during Metamorphosis

1998

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Mushroom bodies (MBs) are symmetrically paired neuropils in the insect brain that are of critical importance for associative olfactory learning and memory. In Drosophila melanogaster, the MB intrinsic neurons (Kenyon cells) undergo extensive reorganization at the onset of metamorphosis. A phase of rapid axonal degeneration without cell death is followed by axonal regeneration. This re-elaboration occurs as levels of the steroid hormone 20-hydroxyecdysone (20E) are rising during the pupal stage. Based on the known role of 20E in directing many features of CNS remodeling during insect metamorphosis, we hypothesized that the outgrowth of MB axonal processes is promoted by 20E. Using a GAL4 enhancer trap line (201Y) that drives MB-restricted reporter gene expression, we identified Kenyon cells in primary cultures dissociated from early pupal CNS. Paired cultures derived from single brains isolated before the 20E pupal peak were incubated in medium with or without 20E for 2-4 d. Morphometric analysis demonstrated that MB neurons exposed to 20E had significantly greater total neurite length and branch number compared with that of MB neurons grown without hormone. The relationship between branch number and total neurite length remained constant regardless of hormone treatment in vitro, suggesting that 20E enhances the rate of outgrowth from pupal MB neurons in a proportionate manner and does not selectively increase neuritic branching. These results implicate 20E in enhancing axonal outgrowth of Kenyon cells to support MB remodeling during metamorphosis.

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mentioning

confidence: 70%

Section: Y Shows Mb-selective Expression In the Brain During Metammentioning

confidence: 97%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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The Steroid Hormone 20-Hydroxyecdysone Enhances Neurite Growth ofDrosophilaMushroom Body Neurons Isolated during Metamorphosis

1998

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“…Kenyon cells, which comprise at least half of the mushroom body neurons (Ito and Hotta, 1992) have been shown specifitally to survive the pupal stage (Tee :hnauandHeisenberg, 1982). During metamorphosis, most of their projections first degenerate to a core of about 500 fibers and then regrow to make new connections (Technau and Heisenberg, 1982). Interestingly, the flies are affected by environmental stimulation and by the dunce and rutabaga memory mutants (Technau, 1984;Balling et al, 1987).…”

Section: Discussionmentioning

confidence: 99%

Memory through metamorphosis in normal and mutant Drosophila

1994

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To establish that a stable, long-lasting form of memory exists in Drosophila, we trained third-instar larvae by electroshocking them in the presence of a specific odor using a Pavlovian conditioning procedure. We show that conditioned odor avoidance produced in larvae still was present in adults 8 d later. Such memory through metamorphosis was specific to the temporal pairing of odor and shock; presentations of odors alone or shock alone did not produce a change. Thus, the memory involved associative processes. We also show that similar training of the single-gene memory mutants dunce and amnesiac did not yield any detectable learning in larvae or memory retention in adults, suggesting that these mutations interfere with long-term memory (LTM) formation even if LTM is induced independently of earlier memory retention processes.

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Neurogenesis in adult insect mushroom bodies

et al. 1996

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The occurrence of neurogenesis in mushroom bodies of adult insects belonging to several orthopteroid and coleopteran families is described. Using injections of 5-bromo, T2'-deoxyuridine, we showed that neuroblasts, which are progenitors of Kenyon cells during preimaginal instars, continue to divide in adult Acheta domesticus. Their progeny constitute a central column in mushroom body cortices of 3-week-old females. Other Gryllidae, Gryllus bimaculatus and Gryllomorpha dalmatina, show the same pattern of neuroblast activity and migration of their progeny. Immunocytochemical staining of glial cells failed to reveal any immunoreactivity, either in proliferating regions or in the resulting cells. In another orthopteran, Locusta migratoria, discrete clusters of cells, located dorsolateral to the Kenyon cells, incorporated 5-bromo, 2'-deoxyuridine, but we could not detect any neuronal progeny migrating to the mushroom body cortices. These cells were strongly labeled with an antiglial antibody, indicating that the replicating cells are glioblasts rather than neuroblasts. In Periplaneta americana (Dictyoptera), cells replicating their DNA were similarly shown to immunoreact with glial antibodies. In contrast, three coleopterans (Tenebrio molitor, Zophobas species, Harmonia axyridis) have two large neuroblasts located in the middle of the mushroom body cortices. These produce cells which migrate within the group of Kenyon cells, their nuclei having the same shape and size as those of surrounding Kenyon cells. In adult insects, neurogenesis in mushroom bodies occurs in Gryllidae and several coleopteran families, but could not be demonstrated in Dictyoptera and Acrididae. Its occurrence and distribution raise the issue of unexpected plasticity in the adult insect brain.

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Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster

Cited by 263 publications

References 8 publications

The Steroid Hormone 20-Hydroxyecdysone Enhances Neurite Growth ofDrosophilaMushroom Body Neurons Isolated during Metamorphosis

The Steroid Hormone 20-Hydroxyecdysone Enhances Neurite Growth ofDrosophilaMushroom Body Neurons Isolated during Metamorphosis

Memory through metamorphosis in normal and mutant Drosophila

Neurogenesis in adult insect mushroom bodies

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