The refinement of invertebrate synapses during development

Lnenicka, Gregory A.; Murphey, R. K.

doi:10.1002/neu.480200507

Cited by 46 publications

(39 citation statements)

References 70 publications

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“…In several systems it has been proposed that one of these factors is electrical activity (reviewed in Lnenicka and Murphey, 1989;Schmidt and Tieman, 1989). In Drosophila the innervation of the larval body wall muscles appears to be affected by activity.…”

Section: Studies In Hyperexcitable Mutantsmentioning

confidence: 99%

“…One of the mechanisms that has been related to the regulation of synaptogenesis and synapse modification in many systems is electrical activity (reviewed in Lnenicka and Murphey, 1989;Schmidt and Tieman, 1989). In vertebrates activity is believed to control both motoneuron survival and neuromuscular junction size (Brown and Ironton, 1977;Oppenheim and Nuñez, 1982).…”

Section: Introductionmentioning

confidence: 99%

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Ultrastructure of neuromuscular junctions in Drosophilal: Comparison of wild type and mutants with increased excitability

Jia¹,

Gorczyca²,

Budnik³

1993

J. Neurobiol.

207

157

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SUMMARYThe ventral longitudinal muscles of the Drosophila larval body wall are innervated by at least four types of synaptic terminals that can be distinguished on morphological grounds at the light microscopical level. The innervation of these muscles has been previously shown to be regulated by neuronal activity. In this report we investigate the ultrastructural basis for synaptic bouton differences by using serial sections, and examine the structure of synaptic terminals in mutants with increased excitability. We report that individual identifiable muscle fibers are innervated by terminals containing two to three types of synaptic boutons that can be distinguished in terms of synaptic vesicle population, presynaptic and postsynaptic specialization, and general shape. We propose a model to account for the bouton types observed at the light microscopical level. We find that in the hyperexcitable mutant eag Sh, there are dramatic ultrastructural alterations at synaptic boutons. These alterations include a partial depletion of two types of synaptic vesicles and a change in appearance of a third type, changes in number and appearance of synaptic densities, and the presence of multivesicular bodies. Our results show that an increase in neuronal excitability produces profound effects in synaptic terminal structure.

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Section: Studies In Hyperexcitable Mutantsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Ultrastructure of neuromuscular junctions in Drosophilal: Comparison of wild type and mutants with increased excitability

Jia¹,

Gorczyca²,

Budnik³

1993

J. Neurobiol.

207

157

View full text Add to dashboard Cite

show abstract

“…Neurogenesis during larval development and particularly in the course of metamorphosis, which is commonly referred to as "neurometamorphosis" (Harris, 1990), is a topic that has not been addressed in crustaceans (Laverack,I988a,b). On the other hand, recent reviews outline the significance of hormonal actions (Levine & Weeks, 1990), persistent neural elements (Breidbach, 1990), programmed cell death, structural remodelling (Truman, 1990) and synaptic refinement (Lnenicka & Murphey, 1989) during neurometamorphosis of insects. However, metamorphosis is quite different in holometabolous insects and decapod crustaceans.…”

Section: Introductionmentioning

confidence: 99%

On the morphology of the central nervous system in larval stages ofCarcinus maenas L. (Decapoda, Brachyura)

Harzsch

Dawirs

1993

Helgolander Meeresunters

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We investigated the morphology of the central nervous system throughout the larval development of Carcinus maenas. For that purpose single larvae were reared in the laboratory from hatching through metamorphosis. Complete series of whole mount semithin sections were obtained from individuals of all successive larval stages and analysed with a light microscope. Morphological feature and spatial arrangement of discernable neural cell clusters, fibre tracts and neuropile are described and compared with the adult pattern. We found that most of the morphological features characterizing the adult nervous system are already present in the zoea-1. Nevertheless, there are marked differences with respect to the arrangement of nerve cell bodies, organization of cerebral neuropile, and disposition of ganglia in the ventral nerve cord. It appears that complexity of the central nervous neuropile is selectively altered during postmetamorphotic development, probably reflecting adaptive changes of.sensory-motor integration in response to behavioural maturation. In contrast, during larval development there was httle change in the overall structural organization of the central nervous system despite some considerable growth. However, the transition from zoea-4 to megalopa brings about multiple fundamental changes in larval morphology and behavioural pattern. Since central nervous integration should properly adapt to the altered behavioural repertoire of the megalopa, it seems necessary to ask in which respect synaptic rearrangement might characterize development of the central nervous system.

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“…Thus, although our data do not exclude the possibility that the morphological abnormalities are caused by loci different from those causing the behavioral and biochemical defects, we consider this unlikely. In many organisms, activity-dependent processes have been shown to affect the morphology of the nervous system (10,(38)(39)(40)(41). Since the cAMP cascade modulates neuronal excitability, it is possible that memory mutations exert their effect on axonal morphology by impairing electrical activity of the sensory neuron.…”

Section: Discussionmentioning

confidence: 99%

“…Structural alterations in connectivity also occur during ontogenesis (7)(8)(9)(10)(11)(12). This similarity has led to the suggestion that developmental and behavioral plasticity share molecular and cellular mechanisms (13,14).…”

mentioning

confidence: 99%

Morphology of a sensory neuron in Drosophila is abnormal in memory mutants and changes during aging.

Corfas

Dudai

1991

Proc. Natl. Acad. Sci. U.S.A.

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Several mutations in DrosophUa impair learning and the cAMP cascade. We report here that the fine morphology of an identified mechanosensory neuron is abnormal in two of these mutants, dunce (dnc) and rutabaga (rut). The neuron innervating the antero-notopleural bristle was filled with horseradish peroxidase and studied at the light-and electron-microscopy level. In the mutants dnc and rut, this neuron has an abnormally large number of side branches and varicosities in a defined segment of the axon. In wild-type flies, age tends to decrease the number of side branches and varicosities in the same axonal segment that is affected by the mutations. Ultrastructural studies are compatible with the interpretation that the varicosities are potential synaptic sites. The results suggest that the cAMP cascade plays a role in shaping neuronal connectivity.Long-term memory probably involves structural alterations in neuronal connectivity (1-6). Structural alterations in connectivity also occur during ontogenesis (7-12). This similarity has led to the suggestion that developmental and behavioral plasticity share molecular and cellular mechanisms (13,14). Whether this is indeed the case can be tested by neurogenetics-i.e., by examining the effect of mutations that impair behavioral plasticity on developmental plasticity, and vice versa. The fruit fly, Drosophila melanogaster, is especially suitable for this purpose, since relatively specific memory mutants have been isolated in this organism (for reviews, see refs. 15 and 16).We have investigated in Drosophila a "cleaning" reflex that is subserved inter alia by the sensory neuron innervating the antero-notopleural (ANP) thoracic bristle (17). The reflex can undergo habituation and dishabituation, two simple forms of nonassociative learning (17). Habituation is abnormally short-lived in the memory mutants dunce (dnc) and rutabaga (rut), two mutations that also impair the cAMP cascade (ref. 17 and unpublished observations). Moreover, these mutations modify the decrement of the physiological response of the ANP neuron to repetitive mechanical stimuli (18). The ANP sensory neuron has a characteristic axonal morphology that permits analysis of axonal branching and potential synaptic sites in the central nervous system. Thus, one can investigate the effect of memory mutations on the structure of a neuron that subserves a modifiable behavior. In addition, correlation of morphology with age can be investigated in this neuron. In the present paper we report that in dnc and rut mutants there are a larger number of side branches and varicosities in a defined segment of the sensory axon. Age tends to decrease the number of varicosities in wild-type flies, and old flies have a lower number of side branches in the same axonal segment that is affected by the mutations. Our data suggest: (i) memory mutations affect structural connectivity of neurons, (it) the cAMP cascade plays a role in shaping neuronal connectivity, (iii) the ANP neuron undergoes age-dependent elimination of putati...

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The refinement of invertebrate synapses during development

Cited by 46 publications

References 70 publications

Ultrastructure of neuromuscular junctions in Drosophilal: Comparison of wild type and mutants with increased excitability

Ultrastructure of neuromuscular junctions in Drosophilal: Comparison of wild type and mutants with increased excitability

On the morphology of the central nervous system in larval stages ofCarcinus maenas L. (Decapoda, Brachyura)

Morphology of a sensory neuron in Drosophila is abnormal in memory mutants and changes during aging.

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