Limits...
Neuroarchitecture of aminergic systems in the larval ventral ganglion of Drosophila melanogaster.

Vömel M, Wegener C - PLoS ONE (2008)

Bottom Line: Previous descriptions, however, did not determine the exact spatial location of aminergic neurite arborizations within the neuropil.In contrast to 5-HT neurons, TH and TDC2 neurons each comprise morphologically different neuron subsets with separated in- and output compartments in specific neuropil regions.The three-dimensional mapping of aminergic neurons now facilitates the identification of neuronal network contacts and co-localized signaling molecules, as exemplified for DOPA decarboxylase-synthesizing neurons that co-express crustacean cardioactive peptide and myoinhibiting peptides.

View Article: PubMed Central - PubMed

Affiliation: Emmy Noether Neuropeptide Group, Animal Physiology, Department of Biology, Philipps-University Marburg, Marburg, Germany.

ABSTRACT
Biogenic amines are important signaling molecules in the central nervous system of both vertebrates and invertebrates. In the fruit fly Drosophila melanogaster, biogenic amines take part in the regulation of various vital physiological processes such as feeding, learning/memory, locomotion, sexual behavior, and sleep/arousal. Consequently, several morphological studies have analyzed the distribution of aminergic neurons in the CNS. Previous descriptions, however, did not determine the exact spatial location of aminergic neurite arborizations within the neuropil. The release sites and pre-/postsynaptic compartments of aminergic neurons also remained largely unidentified. We here used gal4-driven marker gene expression and immunocytochemistry to map presumed serotonergic (5-HT), dopaminergic, and tyraminergic/octopaminergic neurons in the thoracic and abdominal neuromeres of the Drosophila larval ventral ganglion relying on Fasciclin2-immunoreactive tracts as three-dimensional landmarks. With tyrosine hydroxylase- (TH) or tyrosine decarboxylase 2 (TDC2)-specific gal4-drivers, we also analyzed the distribution of ectopically expressed neuronal compartment markers in presumptive dopaminergic TH and tyraminergic/octopaminergic TDC2 neurons, respectively. Our results suggest that thoracic and abdominal 5-HT and TH neurons are exclusively interneurons whereas most TDC2 neurons are efferent. 5-HT and TH neurons are ideally positioned to integrate sensory information and to modulate neuronal transmission within the ventral ganglion, while most TDC2 neurons appear to act peripherally. In contrast to 5-HT neurons, TH and TDC2 neurons each comprise morphologically different neuron subsets with separated in- and output compartments in specific neuropil regions. The three-dimensional mapping of aminergic neurons now facilitates the identification of neuronal network contacts and co-localized signaling molecules, as exemplified for DOPA decarboxylase-synthesizing neurons that co-express crustacean cardioactive peptide and myoinhibiting peptides.

Show MeSH

Related in: MedlinePlus

Mapping of Ddc-gal4 x mCD8GFP expressing neurons.A1) Ventral view of 3D image stacks showing volume-rendered GFP-immunoreactive neurons (green) and A2) Fas2-positive tracts (magenta) in a larva expressing Ddc-gal4-driven mCD8GFP. The merged image (A3) served for an idealized schematic representation of Ddc-gal4 x mCD8GFP expressing neurons in the Fas2 landmark system (A4). B1-3) Corresponding transversal views of the neuromere a4 (* in A3), and B4) the deduced idealized scheme. Note that the Ddc-gal4 driver typically drives mCD8GFP expression in most, but not all presumed DDC neurons of the VG (see Fig. S3 and S4). Thus, some presumed DDC neurons are not included in the idealized schemes shown here. Green-shaded areas in the schemes contain a high concentration of GFP-immunoreactive arborizations. Scale bars: 50 µm in A), 25 µm in B) and C).
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC2268740&req=5

pone-0001848-g006: Mapping of Ddc-gal4 x mCD8GFP expressing neurons.A1) Ventral view of 3D image stacks showing volume-rendered GFP-immunoreactive neurons (green) and A2) Fas2-positive tracts (magenta) in a larva expressing Ddc-gal4-driven mCD8GFP. The merged image (A3) served for an idealized schematic representation of Ddc-gal4 x mCD8GFP expressing neurons in the Fas2 landmark system (A4). B1-3) Corresponding transversal views of the neuromere a4 (* in A3), and B4) the deduced idealized scheme. Note that the Ddc-gal4 driver typically drives mCD8GFP expression in most, but not all presumed DDC neurons of the VG (see Fig. S3 and S4). Thus, some presumed DDC neurons are not included in the idealized schemes shown here. Green-shaded areas in the schemes contain a high concentration of GFP-immunoreactive arborizations. Scale bars: 50 µm in A), 25 µm in B) and C).

Mentions: Morphology (Fig. 6, 7). Inferred from Ddc-gal4-driven marker gene expression (Fig. 6), DDC immunostainings (Fig. 7; Fig. S3), and double labeling experiments with antibodies against 5-HT and TH (Fig. S4), DDC neurons can be categorized into five distinct neuron groups: The first group consists of segmentally reiterated DDC neuron pairs with somata in the ventral cortex below the CI fascicles. These DDC neurons likely represent serotonergic neurons since they showed 5-HT immunoreactivity (Fig. S4; see above for a detailed morphological description). The Ddc-gal4 driver induced mCD8GFP expression in additional neuron pairs of a3-6 which reside adjacent to the 5-HT neurons in the cortex beneath the CI tracts. These neurons constitute a second distinct DDC neuron group since they obviously synthesize the peptide corazonin [19]. The corazonin-immunoreactive DDC neurons showed faint DDC immunoreactivity in a few preparations, but lacked 5-HT immunoreactivity (Fig. S3, and S4; for a detailed morphological description of corazonin-immunoreactive neurons within the Fas2 landmark system see [20]). The third group of DDC neurons consists of unpaired neurons in the ventral midline of t3 and a1-5, whose somata lay right beneath the DM/VM tracts. Although these neurons typically showed poor Ddc-gal4-driven mCD8-GFP expression, they always strongly stained with both DDC and TH antisera (Fig. S3, and S4). Thus, these DDC neurons correspond to the presumptive dopaminergic vmTH neurons (see above). The somata of the fourth and the fifth distinct DDC neuron groups reside dorso-laterally at the height of the DL tracts. The fourth group of DDC neurons showed strong DDC and TH immunolabeling. These DDC neurons, therefore, likely represent the presumptive dopaminergic dlTH neurons (Fig. S4; see above), but were usually missing in the Ddc-gal4 expression pattern. The remaining neurons constitute the fifth distinct DDC neuron group (VL1 neurons; [19]; see also below) since they neither seem to synthesize 5-HT nor DA (Fig. S4). VL1 neurons showed prominent Ddc-gal4-driven mCD8GFP expression, but comparably weak DDC immunoreactivity (Fig. S3). The VL1 neuron somata are typically arranged as segmentally reiterated pairs in t3, a1-4, and a6-7, and reside laterally between the height of the VL and the DL tracts. In t3 and a1-4, VL1 neurites initially run ventrally towards the VL tracts, then project beneath the TP 4 ventro-medially until they converge in proximity to the VM tracts. After forming extensive arborizations between the DM and VM tracts, the VL1 neurites proceed dorsally, diverge within the cortex, and project via the segmental nerves to the periphery.


Neuroarchitecture of aminergic systems in the larval ventral ganglion of Drosophila melanogaster.

Vömel M, Wegener C - PLoS ONE (2008)

Mapping of Ddc-gal4 x mCD8GFP expressing neurons.A1) Ventral view of 3D image stacks showing volume-rendered GFP-immunoreactive neurons (green) and A2) Fas2-positive tracts (magenta) in a larva expressing Ddc-gal4-driven mCD8GFP. The merged image (A3) served for an idealized schematic representation of Ddc-gal4 x mCD8GFP expressing neurons in the Fas2 landmark system (A4). B1-3) Corresponding transversal views of the neuromere a4 (* in A3), and B4) the deduced idealized scheme. Note that the Ddc-gal4 driver typically drives mCD8GFP expression in most, but not all presumed DDC neurons of the VG (see Fig. S3 and S4). Thus, some presumed DDC neurons are not included in the idealized schemes shown here. Green-shaded areas in the schemes contain a high concentration of GFP-immunoreactive arborizations. Scale bars: 50 µm in A), 25 µm in B) and C).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2268740&req=5

pone-0001848-g006: Mapping of Ddc-gal4 x mCD8GFP expressing neurons.A1) Ventral view of 3D image stacks showing volume-rendered GFP-immunoreactive neurons (green) and A2) Fas2-positive tracts (magenta) in a larva expressing Ddc-gal4-driven mCD8GFP. The merged image (A3) served for an idealized schematic representation of Ddc-gal4 x mCD8GFP expressing neurons in the Fas2 landmark system (A4). B1-3) Corresponding transversal views of the neuromere a4 (* in A3), and B4) the deduced idealized scheme. Note that the Ddc-gal4 driver typically drives mCD8GFP expression in most, but not all presumed DDC neurons of the VG (see Fig. S3 and S4). Thus, some presumed DDC neurons are not included in the idealized schemes shown here. Green-shaded areas in the schemes contain a high concentration of GFP-immunoreactive arborizations. Scale bars: 50 µm in A), 25 µm in B) and C).
Mentions: Morphology (Fig. 6, 7). Inferred from Ddc-gal4-driven marker gene expression (Fig. 6), DDC immunostainings (Fig. 7; Fig. S3), and double labeling experiments with antibodies against 5-HT and TH (Fig. S4), DDC neurons can be categorized into five distinct neuron groups: The first group consists of segmentally reiterated DDC neuron pairs with somata in the ventral cortex below the CI fascicles. These DDC neurons likely represent serotonergic neurons since they showed 5-HT immunoreactivity (Fig. S4; see above for a detailed morphological description). The Ddc-gal4 driver induced mCD8GFP expression in additional neuron pairs of a3-6 which reside adjacent to the 5-HT neurons in the cortex beneath the CI tracts. These neurons constitute a second distinct DDC neuron group since they obviously synthesize the peptide corazonin [19]. The corazonin-immunoreactive DDC neurons showed faint DDC immunoreactivity in a few preparations, but lacked 5-HT immunoreactivity (Fig. S3, and S4; for a detailed morphological description of corazonin-immunoreactive neurons within the Fas2 landmark system see [20]). The third group of DDC neurons consists of unpaired neurons in the ventral midline of t3 and a1-5, whose somata lay right beneath the DM/VM tracts. Although these neurons typically showed poor Ddc-gal4-driven mCD8-GFP expression, they always strongly stained with both DDC and TH antisera (Fig. S3, and S4). Thus, these DDC neurons correspond to the presumptive dopaminergic vmTH neurons (see above). The somata of the fourth and the fifth distinct DDC neuron groups reside dorso-laterally at the height of the DL tracts. The fourth group of DDC neurons showed strong DDC and TH immunolabeling. These DDC neurons, therefore, likely represent the presumptive dopaminergic dlTH neurons (Fig. S4; see above), but were usually missing in the Ddc-gal4 expression pattern. The remaining neurons constitute the fifth distinct DDC neuron group (VL1 neurons; [19]; see also below) since they neither seem to synthesize 5-HT nor DA (Fig. S4). VL1 neurons showed prominent Ddc-gal4-driven mCD8GFP expression, but comparably weak DDC immunoreactivity (Fig. S3). The VL1 neuron somata are typically arranged as segmentally reiterated pairs in t3, a1-4, and a6-7, and reside laterally between the height of the VL and the DL tracts. In t3 and a1-4, VL1 neurites initially run ventrally towards the VL tracts, then project beneath the TP 4 ventro-medially until they converge in proximity to the VM tracts. After forming extensive arborizations between the DM and VM tracts, the VL1 neurites proceed dorsally, diverge within the cortex, and project via the segmental nerves to the periphery.

Bottom Line: Previous descriptions, however, did not determine the exact spatial location of aminergic neurite arborizations within the neuropil.In contrast to 5-HT neurons, TH and TDC2 neurons each comprise morphologically different neuron subsets with separated in- and output compartments in specific neuropil regions.The three-dimensional mapping of aminergic neurons now facilitates the identification of neuronal network contacts and co-localized signaling molecules, as exemplified for DOPA decarboxylase-synthesizing neurons that co-express crustacean cardioactive peptide and myoinhibiting peptides.

View Article: PubMed Central - PubMed

Affiliation: Emmy Noether Neuropeptide Group, Animal Physiology, Department of Biology, Philipps-University Marburg, Marburg, Germany.

ABSTRACT
Biogenic amines are important signaling molecules in the central nervous system of both vertebrates and invertebrates. In the fruit fly Drosophila melanogaster, biogenic amines take part in the regulation of various vital physiological processes such as feeding, learning/memory, locomotion, sexual behavior, and sleep/arousal. Consequently, several morphological studies have analyzed the distribution of aminergic neurons in the CNS. Previous descriptions, however, did not determine the exact spatial location of aminergic neurite arborizations within the neuropil. The release sites and pre-/postsynaptic compartments of aminergic neurons also remained largely unidentified. We here used gal4-driven marker gene expression and immunocytochemistry to map presumed serotonergic (5-HT), dopaminergic, and tyraminergic/octopaminergic neurons in the thoracic and abdominal neuromeres of the Drosophila larval ventral ganglion relying on Fasciclin2-immunoreactive tracts as three-dimensional landmarks. With tyrosine hydroxylase- (TH) or tyrosine decarboxylase 2 (TDC2)-specific gal4-drivers, we also analyzed the distribution of ectopically expressed neuronal compartment markers in presumptive dopaminergic TH and tyraminergic/octopaminergic TDC2 neurons, respectively. Our results suggest that thoracic and abdominal 5-HT and TH neurons are exclusively interneurons whereas most TDC2 neurons are efferent. 5-HT and TH neurons are ideally positioned to integrate sensory information and to modulate neuronal transmission within the ventral ganglion, while most TDC2 neurons appear to act peripherally. In contrast to 5-HT neurons, TH and TDC2 neurons each comprise morphologically different neuron subsets with separated in- and output compartments in specific neuropil regions. The three-dimensional mapping of aminergic neurons now facilitates the identification of neuronal network contacts and co-localized signaling molecules, as exemplified for DOPA decarboxylase-synthesizing neurons that co-express crustacean cardioactive peptide and myoinhibiting peptides.

Show MeSH
Related in: MedlinePlus