Synaptogenesis in the first optic neuropile of the fly's visual system

Fröhlich, A.; Meinertzhagen, Ian A.

doi:10.1007/bf01258010

Cited by 80 publications

(59 citation statements)

References 23 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…After identification to familial level, the head was removed and dissected to allow access to fixative, usually a modified Karnovsky glutaraldehyde/formaldehyde mixture in cacodylate buffer, followed by osmication (11,12). Material was embedded in epoxy, and ribbons of up to 100 consecutive sections were cut and mounted on carbon-coated Formvar films on slot grids for examination with a Philips 201C electron microscope.…”

Section: Methodsmentioning

confidence: 99%

“…The identity of the postsynaptic elements is known precisely (11,12,22). The two larger median processes at the center of the postsynaptic site ( Fig.…”

Section: Methodsmentioning

confidence: 99%

“…1) always come one each from two large monopolar cells, Li and L2, the trunks of which form the longitudinal axis of the cylindrical cartridge, in Musca. The two smaller, outlying ("polar") elements at the synapse usually belong to a processes of an amacrine cell (11,12,20,22). To examine the counterpart synaptic contacts in Diptera closer to the ancestral line, evidence for homology across families has first been sought among the participating neurones.…”

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

Evolutionary progression at synaptic connections made by identified homologous neurones.

Shaw¹,

Meinertzhagen²

1986

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

View full text Add to dashboard Cite

A comparative ultrastructural study of photoreceptor synapses formed upon homologous postsynaptic neurones in insects has been made by using serial-section electron microscopy in representative Diptera from a monophyletic series of 14 families. At all of the synaptic contacts there is a presynaptic dense bar, surmounted in phylogenetically more recent families by a presynaptic platform. Opposite the bar lies a pair of postsynaptic elements that invariably originate one each from two unique monopolar neurones Li and L2. Both elements contain increasingly elaborate cisternae in more recent flies. Within the phylogenetic series, the postsynaptic ensemble itself changes from the original dyad to a tetradic configuration in more recent Muscomorpha by the addition of two new postsynaptic elements from an amacrine cell. This transition occurs once only in the series, which, gauged by the fossil record, covers divergences from the stem line extending back >200 million years.During the course of evolution, adaptive modifications of the nervous system must have occurred frequently to account for the many corresponding innovations in the behavioral repertoires of animals. How these evolutionary differences between the brains of related species are expressed at the cellular level remains a mystery. Here we distinguish between two contrasting cellular strategies which could alter brain circuitry during the evolutionary divergence ofdifferent phyletic lines: (i) the emergence of new types of neurones, which then become connected so as to modify the circuitry in an existing neuropil, or (ii) alteration in synaptic connectivity among preexisting neurones inherited from a common ancestor. Our comparative study of evolutionary progression in the most peripheral visual neuropil of an insect order, Diptera, supports process (ii) over (i).Since it is difficult to see any obvious homologies between the neurones of different phyla, the generation of new neurone classes is most likely to have been important at the divergence of the major phyla. Within established phyletic lines, however, this mechanism is contraindicated by examples of conservation of neuronal types, particularly clearly in arthropods, in which many of the larger neurones can be recognized uniquely in both sensory and motor pathways.

show abstract

Section: Methodsmentioning

confidence: 99%

“…The identity of the postsynaptic elements is known precisely (11,12,22). The two larger median processes at the center of the postsynaptic site ( Fig.…”

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

See 1 more Smart Citation

Evolutionary progression at synaptic connections made by identified homologous neurones.

Shaw¹,

Meinertzhagen²

1986

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

View full text Add to dashboard Cite

show abstract

“…In Musca, synapses can be observed in the lamina after ϳP ϩ 55% with electron microscopy (Fröhlich and Meinertzhagen, 1982). Electrophysiological measurement reveals an onset of light-evoked photoreceptor activity in Drosophila at P ϩ 82% (Hardie et al, 1993).…”

mentioning

confidence: 99%

Neuropil Pattern Formation and Regulation of Cell Adhesion Molecules inDrosophilaOptic Lobe Development Depend on Synaptobrevin

et al. 1999

View full text Add to dashboard Cite

To investigate a possible involvement of synaptic machinery in Drosophila visual system development, we studied the effects of a loss of function of neuronal synaptobrevin, a protein required for synaptic vesicle release. Expression of tetanus toxin light chain (which cleaves neuronal synaptobrevin) and genetic mosaics were used to analyze neuropil pattern formation and levels of selected neural adhesion molecules in the optic lobe. We show that targeted toxin expression in the developing optic lobe results in disturbances of the columnar organization of visual neuropils and of photoreceptor terminal morphology. IrreC-rst immunoreactivity in neuropils is increased after widespread expression of toxin. In photoreceptors, targeted toxin expression results in increased Fasciclin II and chaoptin but not IrreC-rst immunoreactivity. Axonal pathfinding and programmed cell death are not affected. In genetic mosaics, patches of photoreceptors that lack neuronal synaptobrevin exhibit the same phenotypes observed after photoreceptorspecific toxin expression. Our results demonstrate the requirement of neuronal synaptobrevin for regulation of cell adhesion molecules and development of the fine structure of the optic lobe. A possible causal link to fine-tuning processes that may include synaptic plasticity in the development of the Drosophila CNS is discussed.

show abstract

“…The assembly sequence implies the action of a concatenated sequence of cell recognition steps, but molecular details for these are lacking. The presynaptic site is marked by the accumulation of synaptic vesicles and the appearance of a presynaptic density, the T-bar ribbon (23,24), first as a pedestal and then surmounted by a platform (25).…”

mentioning

confidence: 99%

Central projections of photoreceptor axons originating from ectopic eyes in Drosophila

Clements

Lǚ

Gehring

et al. 2008

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

View full text Add to dashboard Cite

Ectopic expression of the retinal determination gene eyeless (ey) induces the formation of supernumerary eyes on antennae, legs, wings, and halteres. These ectopic eyes form ommatidia that contain photoreceptors and accessory cells and respond to light. Here, we demonstrate that ectopic eyes on antennae and legs extend axonal projections to the central nervous system. Furthermore, electroretinograms and morphological evidence indicate that the photoreceptor axons of at least the antennal ectopic eyes can form completely constituted ectopic synapses with foreign postsynaptic elements and suggest that transmission at these sites may be functional. However, the ectopic axons do not connect to their correct optic lobe targets and do not project deeply into the neuropile, but rather form synapses at superficial positions in the neuropils. By means of confocal and electron microscopy we show that these ectopic synapses resemble normal synapses, albeit with some distinct morphological differences. Our data strongly suggest that the developmental programs controlling photoreceptor synaptogenesis and visual map formation depend to a considerable extent on presynaptic and thus photoreceptor-autonomous steps. Our data also suggest that photoreceptor axon projections and the establishment of the highly stereotypical neural circuitry in the optic lobe, the normal target neuropil, may depend on targetspecific cues that appear to be absent from the antennal lobe and thoracic ganglion.T he compound eyes of the Drosophila visual system relay visual information to the underlying optic lobes via four successive neuropils, the distalmost lamina, medulla, and proximal lobula and lobula plate (1). The compound eyes consist of Ϸ800 ommatidia, each of which contains eight photoreceptors and 11 accessory cells (2). Photoreceptors R1-R6 project to the lamina, whereas R7 and R8 axons terminate in the medulla (reviewed in refs. 1 and 3).In the past decade, considerable insight has been gained in the genetic basis of early eye development, photoreceptor determination and ommatidium formation, and circuit assembly in the optic lobe. Early eye development is controlled by a genetic cascade comprising the Pax6 genes eyeless (ey) and twin of eyeless (toy), considered master control genes acting as the first step in the hierarchy, the SIX family members sine oculis (so) and optix, eyes absent (eya), dachshund (dac), and the Pax6-related gene eyegone (eyg). These genes act in complex gene networks and are integrated with signaling pathways (reviewed in refs. 4-6). Some of these genes individually, or in combination with others, are capable of inducing the formation of ectopic eyes (7-12).Photoreceptor differentiation is initiated at the posterior margin of the eye imaginal disc with the formation of the morphogenetic furrow and involves the integration of the decapentaplegic, hedgehog, and wingless signaling pathways with the retinal determination gene network (reviewed in refs. 5 and 13). Signaling by the Notch and Epidermal Growth Factor Recept...

show abstract

Synaptogenesis in the first optic neuropile of the fly's visual system

Cited by 80 publications

References 23 publications

Evolutionary progression at synaptic connections made by identified homologous neurones.

Evolutionary progression at synaptic connections made by identified homologous neurones.

Neuropil Pattern Formation and Regulation of Cell Adhesion Molecules inDrosophilaOptic Lobe Development Depend on Synaptobrevin

Central projections of photoreceptor axons originating from ectopic eyes in Drosophila

Contact Info

Product

Resources

About