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Glutamate, GABA and acetylcholine signaling components in the lamina of the Drosophila visual system.

Kolodziejczyk A, Sun X, Meinertzhagen IA, Nässel DR - PLoS ONE (2008)

Bottom Line: These neurons also express glutamate-like immunoreactivity.However, antisera to ionotropic and metabotropic glutamate receptors did not produce distinct immunosignals in the lamina.In summary, this paper describes novel features of two distinct types of tangential neurons in the Drosophila lamina and assigns putative neurotransmitters and some receptors to a few identified neuron types.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, Stockholm University, Stockholm, Sweden.

ABSTRACT
Synaptic connections of neurons in the Drosophila lamina, the most peripheral synaptic region of the visual system, have been comprehensively described. Although the lamina has been used extensively as a model for the development and plasticity of synaptic connections, the neurotransmitters in these circuits are still poorly known. Thus, to unravel possible neurotransmitter circuits in the lamina of Drosophila we combined Gal4 driven green fluorescent protein in specific lamina neurons with antisera to gamma-aminobutyric acid (GABA), glutamic acid decarboxylase, a GABA(B) type of receptor, L-glutamate, a vesicular glutamate transporter (vGluT), ionotropic and metabotropic glutamate receptors, choline acetyltransferase and a vesicular acetylcholine transporter. We suggest that acetylcholine may be used as a neurotransmitter in both L4 monopolar neurons and a previously unreported type of wide-field tangential neuron (Cha-Tan). GABA is the likely transmitter of centrifugal neurons C2 and C3 and GABA(B) receptor immunoreactivity is seen on these neurons as well as the Cha-Tan neurons. Based on an rdl-Gal4 line, the ionotropic GABA(A) receptor subunit RDL may be expressed by L4 neurons and a type of tangential neuron (rdl-Tan). Strong vGluT immunoreactivity was detected in alpha-processes of amacrine neurons and possibly in the large monopolar neurons L1 and L2. These neurons also express glutamate-like immunoreactivity. However, antisera to ionotropic and metabotropic glutamate receptors did not produce distinct immunosignals in the lamina. In summary, this paper describes novel features of two distinct types of tangential neurons in the Drosophila lamina and assigns putative neurotransmitters and some receptors to a few identified neuron types.

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Comparison between rdl-Tan and Cha-Tan neurons in distal part of lamina.Arrows indicate differences in structures between the two types of tangential neurons. rdl-Tan have thin varicose processes hanging down into the lamina, whereas the Cha-Tan have enlarged boutons in the same layer. A (1–3) rdl-Tan neurons (A2, green), visualised by GFP expression driven by rdl-Gal4, contact GABABR-immunolabeled cells at arrows, but do not coexpress the receptor (A1, magenta). B (1–3) Cha-Tan cells visualised by GFP expression driven by Cha-Gal4 (B2, green) co-express GABABR immunoreactivity (B1, magenta) in their boutons (arrow). C (1–3) rdl-Tan neurons in cross-section are organized in widely branched network with arborizations in each cartridge (C2, green). Close contacts with GABABR-immunopositive cells (C1, magenta) are visible. D (1–3) Cha-Tan neurons also are organized in a network but they have more distinct aggregates of boutons in each cartridge and these boutons co-express GABABR-immunolabeling (schown in Fig. 8E) and co-localize anti-ChAT (D1, magenta, D3 – merged). Scale bar for images A to D = 10 µm. E (1–2) Higher magnification of the rdl-Tan processes distally in the lamina in cross section (E1) and contacts with GABABR-immunolabeled neurons (E2). Scale bar = 10 µm.
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pone-0002110-g009: Comparison between rdl-Tan and Cha-Tan neurons in distal part of lamina.Arrows indicate differences in structures between the two types of tangential neurons. rdl-Tan have thin varicose processes hanging down into the lamina, whereas the Cha-Tan have enlarged boutons in the same layer. A (1–3) rdl-Tan neurons (A2, green), visualised by GFP expression driven by rdl-Gal4, contact GABABR-immunolabeled cells at arrows, but do not coexpress the receptor (A1, magenta). B (1–3) Cha-Tan cells visualised by GFP expression driven by Cha-Gal4 (B2, green) co-express GABABR immunoreactivity (B1, magenta) in their boutons (arrow). C (1–3) rdl-Tan neurons in cross-section are organized in widely branched network with arborizations in each cartridge (C2, green). Close contacts with GABABR-immunopositive cells (C1, magenta) are visible. D (1–3) Cha-Tan neurons also are organized in a network but they have more distinct aggregates of boutons in each cartridge and these boutons co-express GABABR-immunolabeling (schown in Fig. 8E) and co-localize anti-ChAT (D1, magenta, D3 – merged). Scale bar for images A to D = 10 µm. E (1–2) Higher magnification of the rdl-Tan processes distally in the lamina in cross section (E1) and contacts with GABABR-immunolabeled neurons (E2). Scale bar = 10 µm.

Mentions: A ChAT immunoreactive lamina neurons. Asterisk: layer with large monopolar cells (L1–L3); triangle: layer with small monopolar cells (L4 and L5); square: layer with processes of Cha-Tan neurons (see Fig. 8 and 9). Arrow labels level of branching of L4 neurons in the proximal lamina. Scale bar = 10 µm (for all images, except panel B). B GFP expression in lamina driven by the rdl-Gal4 reveals L4 neurons. Triangle: L4 cell body; arrow: characteristic branching of L4 collaterals in the proximal lamina. GFP is also seen in branches of a wide-field tangential neuron, in the distal lamina. Scale bar = 10 µm. C Weak immunolabeling in cell bodies of large monopolar neurons with antiserum to vGluT. Strong immunolabeling in the lamina neuropil is seen in processes of amacrine neurons. D1–3 Distributions of vesicular acetylcholine transporter (vAChT) immunoreactivity and rdl-Gal4 driven GFP expression co-localize to arborizations of the L4 neurons (arrow) in the proximal lamina, but not in their cell bodies (cb) and not in processes of rdl-Tan neurons (asterisk in D1) in the distal lamina. However, vAChT immunoreactivity is seen in enlarged boutons of another tangential neuron in this dorsal layer (large arrow). Scale bar = 5 µm. E1–3 Cell bodies of L2 monopolar neurons are ChAT immunoreactive, revealed by 21D-Gal4 driven GFP (green) in L2 neurons labeled with anti-ChAT (α-Cha; magenta). Co-localization of label is seen in cell bodies, but not clearly in their neurites. Scale bar = 10 µm. F1–3 Anti-vAChT labeling (α-vAChT; magenta) is not co-localized in L2 monopolar cells displayed by GFP driven by 21D-Gal4. Scale bar = 10 µm.


Glutamate, GABA and acetylcholine signaling components in the lamina of the Drosophila visual system.

Kolodziejczyk A, Sun X, Meinertzhagen IA, Nässel DR - PLoS ONE (2008)

Comparison between rdl-Tan and Cha-Tan neurons in distal part of lamina.Arrows indicate differences in structures between the two types of tangential neurons. rdl-Tan have thin varicose processes hanging down into the lamina, whereas the Cha-Tan have enlarged boutons in the same layer. A (1–3) rdl-Tan neurons (A2, green), visualised by GFP expression driven by rdl-Gal4, contact GABABR-immunolabeled cells at arrows, but do not coexpress the receptor (A1, magenta). B (1–3) Cha-Tan cells visualised by GFP expression driven by Cha-Gal4 (B2, green) co-express GABABR immunoreactivity (B1, magenta) in their boutons (arrow). C (1–3) rdl-Tan neurons in cross-section are organized in widely branched network with arborizations in each cartridge (C2, green). Close contacts with GABABR-immunopositive cells (C1, magenta) are visible. D (1–3) Cha-Tan neurons also are organized in a network but they have more distinct aggregates of boutons in each cartridge and these boutons co-express GABABR-immunolabeling (schown in Fig. 8E) and co-localize anti-ChAT (D1, magenta, D3 – merged). Scale bar for images A to D = 10 µm. E (1–2) Higher magnification of the rdl-Tan processes distally in the lamina in cross section (E1) and contacts with GABABR-immunolabeled neurons (E2). Scale bar = 10 µm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2373871&req=5

pone-0002110-g009: Comparison between rdl-Tan and Cha-Tan neurons in distal part of lamina.Arrows indicate differences in structures between the two types of tangential neurons. rdl-Tan have thin varicose processes hanging down into the lamina, whereas the Cha-Tan have enlarged boutons in the same layer. A (1–3) rdl-Tan neurons (A2, green), visualised by GFP expression driven by rdl-Gal4, contact GABABR-immunolabeled cells at arrows, but do not coexpress the receptor (A1, magenta). B (1–3) Cha-Tan cells visualised by GFP expression driven by Cha-Gal4 (B2, green) co-express GABABR immunoreactivity (B1, magenta) in their boutons (arrow). C (1–3) rdl-Tan neurons in cross-section are organized in widely branched network with arborizations in each cartridge (C2, green). Close contacts with GABABR-immunopositive cells (C1, magenta) are visible. D (1–3) Cha-Tan neurons also are organized in a network but they have more distinct aggregates of boutons in each cartridge and these boutons co-express GABABR-immunolabeling (schown in Fig. 8E) and co-localize anti-ChAT (D1, magenta, D3 – merged). Scale bar for images A to D = 10 µm. E (1–2) Higher magnification of the rdl-Tan processes distally in the lamina in cross section (E1) and contacts with GABABR-immunolabeled neurons (E2). Scale bar = 10 µm.
Mentions: A ChAT immunoreactive lamina neurons. Asterisk: layer with large monopolar cells (L1–L3); triangle: layer with small monopolar cells (L4 and L5); square: layer with processes of Cha-Tan neurons (see Fig. 8 and 9). Arrow labels level of branching of L4 neurons in the proximal lamina. Scale bar = 10 µm (for all images, except panel B). B GFP expression in lamina driven by the rdl-Gal4 reveals L4 neurons. Triangle: L4 cell body; arrow: characteristic branching of L4 collaterals in the proximal lamina. GFP is also seen in branches of a wide-field tangential neuron, in the distal lamina. Scale bar = 10 µm. C Weak immunolabeling in cell bodies of large monopolar neurons with antiserum to vGluT. Strong immunolabeling in the lamina neuropil is seen in processes of amacrine neurons. D1–3 Distributions of vesicular acetylcholine transporter (vAChT) immunoreactivity and rdl-Gal4 driven GFP expression co-localize to arborizations of the L4 neurons (arrow) in the proximal lamina, but not in their cell bodies (cb) and not in processes of rdl-Tan neurons (asterisk in D1) in the distal lamina. However, vAChT immunoreactivity is seen in enlarged boutons of another tangential neuron in this dorsal layer (large arrow). Scale bar = 5 µm. E1–3 Cell bodies of L2 monopolar neurons are ChAT immunoreactive, revealed by 21D-Gal4 driven GFP (green) in L2 neurons labeled with anti-ChAT (α-Cha; magenta). Co-localization of label is seen in cell bodies, but not clearly in their neurites. Scale bar = 10 µm. F1–3 Anti-vAChT labeling (α-vAChT; magenta) is not co-localized in L2 monopolar cells displayed by GFP driven by 21D-Gal4. Scale bar = 10 µm.

Bottom Line: These neurons also express glutamate-like immunoreactivity.However, antisera to ionotropic and metabotropic glutamate receptors did not produce distinct immunosignals in the lamina.In summary, this paper describes novel features of two distinct types of tangential neurons in the Drosophila lamina and assigns putative neurotransmitters and some receptors to a few identified neuron types.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, Stockholm University, Stockholm, Sweden.

ABSTRACT
Synaptic connections of neurons in the Drosophila lamina, the most peripheral synaptic region of the visual system, have been comprehensively described. Although the lamina has been used extensively as a model for the development and plasticity of synaptic connections, the neurotransmitters in these circuits are still poorly known. Thus, to unravel possible neurotransmitter circuits in the lamina of Drosophila we combined Gal4 driven green fluorescent protein in specific lamina neurons with antisera to gamma-aminobutyric acid (GABA), glutamic acid decarboxylase, a GABA(B) type of receptor, L-glutamate, a vesicular glutamate transporter (vGluT), ionotropic and metabotropic glutamate receptors, choline acetyltransferase and a vesicular acetylcholine transporter. We suggest that acetylcholine may be used as a neurotransmitter in both L4 monopolar neurons and a previously unreported type of wide-field tangential neuron (Cha-Tan). GABA is the likely transmitter of centrifugal neurons C2 and C3 and GABA(B) receptor immunoreactivity is seen on these neurons as well as the Cha-Tan neurons. Based on an rdl-Gal4 line, the ionotropic GABA(A) receptor subunit RDL may be expressed by L4 neurons and a type of tangential neuron (rdl-Tan). Strong vGluT immunoreactivity was detected in alpha-processes of amacrine neurons and possibly in the large monopolar neurons L1 and L2. These neurons also express glutamate-like immunoreactivity. However, antisera to ionotropic and metabotropic glutamate receptors did not produce distinct immunosignals in the lamina. In summary, this paper describes novel features of two distinct types of tangential neurons in the Drosophila lamina and assigns putative neurotransmitters and some receptors to a few identified neuron types.

Show MeSH
Related in: MedlinePlus