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Diversity and wiring variability of visual local neurons in the Drosophila medulla M6 stratum.

Chin AL, Lin CY, Fu TF, Dickson BJ, Chiang AS - J. Comp. Neurol. (2014)

Bottom Line: Based on the segregation of putative dendrites and axons, these local neurons were classified into two families, directional and nondirectional.Neurotransmitter immunostaining suggested a signal routing model in which some visual information is relayed by directional M6-LNs from the anterior to the posterior M6 and all visual information is inhibited by a diverse population of nondirectional M6-LNs covering the entire M6 stratum.Our findings suggest that the Drosophila medulla M6 stratum contains diverse LNs that form repeating functional modules similar to those found in the vertebrate inner plexiform layer.

View Article: PubMed Central - PubMed

Affiliation: Institute of Biotechnology and Department of Life Science, National Tsing Hua University, Hsinchu, 30013, Taiwan.

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A specific driver of M6-LNs. A: Expression pattern of 30A-GAL4 (magenta). The brain is immunostained with anti-DLG (gray). Locations of M6-LN cell bodies at the ventral (V), medial (M), and dorsal (D) LCBR are marked. B: Presynaptic marker Syt::HA (magenta) and postsynaptic marker Dscam-GFP (green) in the 30A-GAL4 neurons labeled by MKO (gray). C: Expression pattern of 30A-GAL4;Cha-GAL80. The brain is immunostained with anti-DLG (gray). D: Presynaptic marker Syt::HA (magenta) and postsynaptic marker Dscam-GFP (green) in the 30A-GAL4;Cha-GAL80 neurons labeled by MKO (gray). The intense Dscam-GFP signal at the anterior M6 (asterisk), and the overlapping Dscam-GFP/Syt::HA signal at the posterior M6 (arrowhead) in B is absent in D. LCBR, lateral cell body rind; Med, medulla; Lob, lobula. E,F: Dual expression of 30A-GAL4 (green) and Rh3-LexA (magenta) in anti-DLG immunostained medulla (gray). At the medial M6 (E), only long-form R7 (arrowhead) intersects with M6-LNs (green). At the dorsal-posterior M6 (F), all R7s intersect with M6-LNs. G: A merged illustration of Mt11 (green) and two forms of R7 in medulla from Fischbach and Dittrich (1989). The restriction of the terminals of Mt11 to the proximal half of layer M6 is similar to that of the M6-LNs expressed by 30A-GAL4. Scale bars = 50 μm in A–D; 10 μm in E,F.
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fig03: A specific driver of M6-LNs. A: Expression pattern of 30A-GAL4 (magenta). The brain is immunostained with anti-DLG (gray). Locations of M6-LN cell bodies at the ventral (V), medial (M), and dorsal (D) LCBR are marked. B: Presynaptic marker Syt::HA (magenta) and postsynaptic marker Dscam-GFP (green) in the 30A-GAL4 neurons labeled by MKO (gray). C: Expression pattern of 30A-GAL4;Cha-GAL80. The brain is immunostained with anti-DLG (gray). D: Presynaptic marker Syt::HA (magenta) and postsynaptic marker Dscam-GFP (green) in the 30A-GAL4;Cha-GAL80 neurons labeled by MKO (gray). The intense Dscam-GFP signal at the anterior M6 (asterisk), and the overlapping Dscam-GFP/Syt::HA signal at the posterior M6 (arrowhead) in B is absent in D. LCBR, lateral cell body rind; Med, medulla; Lob, lobula. E,F: Dual expression of 30A-GAL4 (green) and Rh3-LexA (magenta) in anti-DLG immunostained medulla (gray). At the medial M6 (E), only long-form R7 (arrowhead) intersects with M6-LNs (green). At the dorsal-posterior M6 (F), all R7s intersect with M6-LNs. G: A merged illustration of Mt11 (green) and two forms of R7 in medulla from Fischbach and Dittrich (1989). The restriction of the terminals of Mt11 to the proximal half of layer M6 is similar to that of the M6-LNs expressed by 30A-GAL4. Scale bars = 50 μm in A–D; 10 μm in E,F.

Mentions: High-resolution imaging indicated that each M6 column contained one swollen terminal derived from an R7 neuron (Fig. 2G), except at the dorsal-posterior M6, where terminals were significantly larger (Fig. 2F). A closer examination revealed that dual terminals from ∼30 paired photoreceptor neurons contributed to the larger terminals in the dorsal-posterior M6 (Fig. 2H). The dual terminals along the M6 dorsal-posterior edge were also observed in PanR7-GAL4 (Fig. 2J), which was preferentially expressed in R7 and DRA R8 neurons (Lee et al., 2001; Wernet et al., 2006). Surprisingly, we found that neurons in Pan R8-GAL4 (Mikeladze-Dvali et al., 2005; Fig. 2J), Rh6-GAL4 (Fig. 2K), and Rh3-LexA (Fig. 3F) have a single terminal at the dorsal-posterior M6. Two-color labeling indicated that the proximal long-form terminals were from Rh3-LexA-positive neurons and that the distal short-form terminals were from Rh6-GAL4-positive neurons (Fig. 2L). The dual terminals could be induced by ectopically expressing DRA ommatidia-inducing homothorax (hth; Wernet et al., 2003; Fig. 2M) in all photoreceptors terminating at other M6 regions, which originally had only one terminal (Fig. 2K). Furthermore, terminals at the dorsal-posterior M6 could be altered to single terminals by overexpressing the dominant-negative form of Hth (hthHM; Ryoo et al., 1999; Fig. 2N), which leads to a loss of the DRA ommatidia (Wernet et al., 2003). Together, these results suggest that the dual terminals at dorsal-posterior M6 arise from DRA R7 and R8.


Diversity and wiring variability of visual local neurons in the Drosophila medulla M6 stratum.

Chin AL, Lin CY, Fu TF, Dickson BJ, Chiang AS - J. Comp. Neurol. (2014)

A specific driver of M6-LNs. A: Expression pattern of 30A-GAL4 (magenta). The brain is immunostained with anti-DLG (gray). Locations of M6-LN cell bodies at the ventral (V), medial (M), and dorsal (D) LCBR are marked. B: Presynaptic marker Syt::HA (magenta) and postsynaptic marker Dscam-GFP (green) in the 30A-GAL4 neurons labeled by MKO (gray). C: Expression pattern of 30A-GAL4;Cha-GAL80. The brain is immunostained with anti-DLG (gray). D: Presynaptic marker Syt::HA (magenta) and postsynaptic marker Dscam-GFP (green) in the 30A-GAL4;Cha-GAL80 neurons labeled by MKO (gray). The intense Dscam-GFP signal at the anterior M6 (asterisk), and the overlapping Dscam-GFP/Syt::HA signal at the posterior M6 (arrowhead) in B is absent in D. LCBR, lateral cell body rind; Med, medulla; Lob, lobula. E,F: Dual expression of 30A-GAL4 (green) and Rh3-LexA (magenta) in anti-DLG immunostained medulla (gray). At the medial M6 (E), only long-form R7 (arrowhead) intersects with M6-LNs (green). At the dorsal-posterior M6 (F), all R7s intersect with M6-LNs. G: A merged illustration of Mt11 (green) and two forms of R7 in medulla from Fischbach and Dittrich (1989). The restriction of the terminals of Mt11 to the proximal half of layer M6 is similar to that of the M6-LNs expressed by 30A-GAL4. Scale bars = 50 μm in A–D; 10 μm in E,F.
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fig03: A specific driver of M6-LNs. A: Expression pattern of 30A-GAL4 (magenta). The brain is immunostained with anti-DLG (gray). Locations of M6-LN cell bodies at the ventral (V), medial (M), and dorsal (D) LCBR are marked. B: Presynaptic marker Syt::HA (magenta) and postsynaptic marker Dscam-GFP (green) in the 30A-GAL4 neurons labeled by MKO (gray). C: Expression pattern of 30A-GAL4;Cha-GAL80. The brain is immunostained with anti-DLG (gray). D: Presynaptic marker Syt::HA (magenta) and postsynaptic marker Dscam-GFP (green) in the 30A-GAL4;Cha-GAL80 neurons labeled by MKO (gray). The intense Dscam-GFP signal at the anterior M6 (asterisk), and the overlapping Dscam-GFP/Syt::HA signal at the posterior M6 (arrowhead) in B is absent in D. LCBR, lateral cell body rind; Med, medulla; Lob, lobula. E,F: Dual expression of 30A-GAL4 (green) and Rh3-LexA (magenta) in anti-DLG immunostained medulla (gray). At the medial M6 (E), only long-form R7 (arrowhead) intersects with M6-LNs (green). At the dorsal-posterior M6 (F), all R7s intersect with M6-LNs. G: A merged illustration of Mt11 (green) and two forms of R7 in medulla from Fischbach and Dittrich (1989). The restriction of the terminals of Mt11 to the proximal half of layer M6 is similar to that of the M6-LNs expressed by 30A-GAL4. Scale bars = 50 μm in A–D; 10 μm in E,F.
Mentions: High-resolution imaging indicated that each M6 column contained one swollen terminal derived from an R7 neuron (Fig. 2G), except at the dorsal-posterior M6, where terminals were significantly larger (Fig. 2F). A closer examination revealed that dual terminals from ∼30 paired photoreceptor neurons contributed to the larger terminals in the dorsal-posterior M6 (Fig. 2H). The dual terminals along the M6 dorsal-posterior edge were also observed in PanR7-GAL4 (Fig. 2J), which was preferentially expressed in R7 and DRA R8 neurons (Lee et al., 2001; Wernet et al., 2006). Surprisingly, we found that neurons in Pan R8-GAL4 (Mikeladze-Dvali et al., 2005; Fig. 2J), Rh6-GAL4 (Fig. 2K), and Rh3-LexA (Fig. 3F) have a single terminal at the dorsal-posterior M6. Two-color labeling indicated that the proximal long-form terminals were from Rh3-LexA-positive neurons and that the distal short-form terminals were from Rh6-GAL4-positive neurons (Fig. 2L). The dual terminals could be induced by ectopically expressing DRA ommatidia-inducing homothorax (hth; Wernet et al., 2003; Fig. 2M) in all photoreceptors terminating at other M6 regions, which originally had only one terminal (Fig. 2K). Furthermore, terminals at the dorsal-posterior M6 could be altered to single terminals by overexpressing the dominant-negative form of Hth (hthHM; Ryoo et al., 1999; Fig. 2N), which leads to a loss of the DRA ommatidia (Wernet et al., 2003). Together, these results suggest that the dual terminals at dorsal-posterior M6 arise from DRA R7 and R8.

Bottom Line: Based on the segregation of putative dendrites and axons, these local neurons were classified into two families, directional and nondirectional.Neurotransmitter immunostaining suggested a signal routing model in which some visual information is relayed by directional M6-LNs from the anterior to the posterior M6 and all visual information is inhibited by a diverse population of nondirectional M6-LNs covering the entire M6 stratum.Our findings suggest that the Drosophila medulla M6 stratum contains diverse LNs that form repeating functional modules similar to those found in the vertebrate inner plexiform layer.

View Article: PubMed Central - PubMed

Affiliation: Institute of Biotechnology and Department of Life Science, National Tsing Hua University, Hsinchu, 30013, Taiwan.

Show MeSH
Related in: MedlinePlus