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Dendritic targeting in the leg neuropil of Drosophila: the role of midline signalling molecules in generating a myotopic map.

Brierley DJ, Blanc E, Reddy OV, Vijayraghavan K, Williams DW - PLoS Biol. (2009)

Bottom Line: Thus the cellular distinctions in peripheral targets and central dendritic domains, which make up the myotopic map, are linked to the birth-order of these motoneurons.Our developmental analysis of dendrite growth reveals that this myotopic map is generated by targeting.We demonstrate that the medio-lateral positioning of motoneuron dendrites in the leg neuropil is controlled by the midline signalling systems Slit-Robo and Netrin-Fra.

View Article: PubMed Central - PubMed

Affiliation: Medical Research Council (MRC) Centre for Developmental Neurobiology, King's College London, London, United Kingdom.

ABSTRACT
Neural maps are emergent, highly ordered structures that are essential for organizing and presenting synaptic information. Within the embryonic nervous system of Drosophila motoneuron dendrites are organized topographically as a myotopic map that reflects their pattern of innervation in the muscle field. Here we reveal that this fundamental organizational principle exists in adult Drosophila, where the dendrites of leg motoneurons also generate a myotopic map. A single postembryonic neuroblast sequentially generates different leg motoneuron subtypes, starting with those innervating proximal targets and medial neuropil regions and producing progeny that innervate distal muscle targets and lateral neuropil later in the lineage. Thus the cellular distinctions in peripheral targets and central dendritic domains, which make up the myotopic map, are linked to the birth-order of these motoneurons. Our developmental analysis of dendrite growth reveals that this myotopic map is generated by targeting. We demonstrate that the medio-lateral positioning of motoneuron dendrites in the leg neuropil is controlled by the midline signalling systems Slit-Robo and Netrin-Fra. These results reveal that dendritic targeting plays a major role in the formation of myotopic maps and suggests that the coordinate spatial control of both pre- and postsynaptic elements by global neuropilar signals may be an important mechanism for establishing the specificity of synaptic connections.

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The positioning of leg motoneuron dendrites occurs independently of changes in dendritic mass.(A) Detail of the proximal dendrites of the sensory neuron ddaC. WT, wild-type. (B) Detail of the proximal dendrites of the sensory neuron ddaC expressing Dp110 reveals an increase in branch complexity. (C) Analysis of cell body size in wild-type (blue) and DP110 expressing (red) ddaC neurons. (D) Sholl analysis of wild-type (blue) and DP110 expressing (red) ddaC neurons. (E) Motoneurons born at 96 h AH generate dendrites that target lateral neuropil territories. (F) Robo  (RoboLOF) clones generated at 96 h AH show medial shifts in the distribution of their dendritic fields. (G) Ecotopic expression of UAS-DP110 in 96 h AH clones results in dendritic arborizations that elaborate mainly in lateral territories of the neuropil with a few ectopic medial branches present in anterior and posterior neuropil. (H) Analysis of cell body size in wild-type (WT), RoboLOF, and UAS-DP110 96 h AH clones. (I–J) Plot profile graphs to reveal the distribution of dendrites along the medio-lateral axis within the leg neuropil (n = 8 for each genotype). The mean centre of mass (circle) for the dendrites of each genotype. The standard error of each experimental condition and the statistical significance between groups can also be seen. Triangles denote the 33rd percentile for each group. (K) Dorsoventral projection of a wild-type dendritic arborization of a motoneuron born at 96 h AH. (L) Dorsoventral projection of a Robo LOF 96 h AH motoneuron. (M) Dorsoventral projection of a CommGOF 96 h AH motoneuron. (N) Dorsoventral projection of a DP110 GOF 96 h AH motoneuron. (K–N) Dorsal is up. Anterior to right. Scale bars = 20 µm.
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pbio-1000199-g007: The positioning of leg motoneuron dendrites occurs independently of changes in dendritic mass.(A) Detail of the proximal dendrites of the sensory neuron ddaC. WT, wild-type. (B) Detail of the proximal dendrites of the sensory neuron ddaC expressing Dp110 reveals an increase in branch complexity. (C) Analysis of cell body size in wild-type (blue) and DP110 expressing (red) ddaC neurons. (D) Sholl analysis of wild-type (blue) and DP110 expressing (red) ddaC neurons. (E) Motoneurons born at 96 h AH generate dendrites that target lateral neuropil territories. (F) Robo (RoboLOF) clones generated at 96 h AH show medial shifts in the distribution of their dendritic fields. (G) Ecotopic expression of UAS-DP110 in 96 h AH clones results in dendritic arborizations that elaborate mainly in lateral territories of the neuropil with a few ectopic medial branches present in anterior and posterior neuropil. (H) Analysis of cell body size in wild-type (WT), RoboLOF, and UAS-DP110 96 h AH clones. (I–J) Plot profile graphs to reveal the distribution of dendrites along the medio-lateral axis within the leg neuropil (n = 8 for each genotype). The mean centre of mass (circle) for the dendrites of each genotype. The standard error of each experimental condition and the statistical significance between groups can also be seen. Triangles denote the 33rd percentile for each group. (K) Dorsoventral projection of a wild-type dendritic arborization of a motoneuron born at 96 h AH. (L) Dorsoventral projection of a Robo LOF 96 h AH motoneuron. (M) Dorsoventral projection of a CommGOF 96 h AH motoneuron. (N) Dorsoventral projection of a DP110 GOF 96 h AH motoneuron. (K–N) Dorsal is up. Anterior to right. Scale bars = 20 µm.

Mentions: To test this idea we next set out to establish if an induced increase in dendrite mass alone would result in dendrites “spilling over” into medial territories. We predicted that the cell autonomous activation of the insulin signalling pathway would allow us to change the global size of the cell whilst leaving other features of the environment the same. To do this we expressed the active subunit of PI3-Kinase, Dp110, which is sufficient to enlarge many different cell types [37]. To first determine how Dp110 changes neuronal morphology, we expressed it in the class IV dendritic arborizing sensory neuron ddaC, as the dendrites of these cells have a nearly two-dimensional organization, making them very amenable to morphometric analysis [38]. Using Volocity Acquisition software (version 4.2, Improvision), we imported raw data stacks and reconstructed 3D projections of the cell bodies of ddaC neurons from both control and experimental groups (Figure 7A and 7B). We then used the lasso tool to capture the cell body and subsequently measure the volume and found that control ddaC neurons had a mean soma volume of 2760.9±149.9 µm3 whereas the mean soma volume in the Dp110 group was 5702.2±142.3 µm3 (Figure 7C). To establish how the dendrites of the two groups were different, we performed Sholl analysis [39] to give a quantitative measure of dendrite complexity throughout the tree. The number of intersections between dendritic processes and Sholl-rings were counted in Photoshop using a template of 12 concentric circles (each 22 µm apart) centred on the cell body. We found the Dp110 expressing neurons distributed their branches in much the same manner as wild-type neurons, but had a two-fold increase in branch number (Figure 7A, 7B, and 7D). Thus Dp110 overexpression results in a two-fold increase in soma size that was mirrored with a two-fold increase in dendritic branch number.


Dendritic targeting in the leg neuropil of Drosophila: the role of midline signalling molecules in generating a myotopic map.

Brierley DJ, Blanc E, Reddy OV, Vijayraghavan K, Williams DW - PLoS Biol. (2009)

The positioning of leg motoneuron dendrites occurs independently of changes in dendritic mass.(A) Detail of the proximal dendrites of the sensory neuron ddaC. WT, wild-type. (B) Detail of the proximal dendrites of the sensory neuron ddaC expressing Dp110 reveals an increase in branch complexity. (C) Analysis of cell body size in wild-type (blue) and DP110 expressing (red) ddaC neurons. (D) Sholl analysis of wild-type (blue) and DP110 expressing (red) ddaC neurons. (E) Motoneurons born at 96 h AH generate dendrites that target lateral neuropil territories. (F) Robo  (RoboLOF) clones generated at 96 h AH show medial shifts in the distribution of their dendritic fields. (G) Ecotopic expression of UAS-DP110 in 96 h AH clones results in dendritic arborizations that elaborate mainly in lateral territories of the neuropil with a few ectopic medial branches present in anterior and posterior neuropil. (H) Analysis of cell body size in wild-type (WT), RoboLOF, and UAS-DP110 96 h AH clones. (I–J) Plot profile graphs to reveal the distribution of dendrites along the medio-lateral axis within the leg neuropil (n = 8 for each genotype). The mean centre of mass (circle) for the dendrites of each genotype. The standard error of each experimental condition and the statistical significance between groups can also be seen. Triangles denote the 33rd percentile for each group. (K) Dorsoventral projection of a wild-type dendritic arborization of a motoneuron born at 96 h AH. (L) Dorsoventral projection of a Robo LOF 96 h AH motoneuron. (M) Dorsoventral projection of a CommGOF 96 h AH motoneuron. (N) Dorsoventral projection of a DP110 GOF 96 h AH motoneuron. (K–N) Dorsal is up. Anterior to right. Scale bars = 20 µm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2737123&req=5

pbio-1000199-g007: The positioning of leg motoneuron dendrites occurs independently of changes in dendritic mass.(A) Detail of the proximal dendrites of the sensory neuron ddaC. WT, wild-type. (B) Detail of the proximal dendrites of the sensory neuron ddaC expressing Dp110 reveals an increase in branch complexity. (C) Analysis of cell body size in wild-type (blue) and DP110 expressing (red) ddaC neurons. (D) Sholl analysis of wild-type (blue) and DP110 expressing (red) ddaC neurons. (E) Motoneurons born at 96 h AH generate dendrites that target lateral neuropil territories. (F) Robo (RoboLOF) clones generated at 96 h AH show medial shifts in the distribution of their dendritic fields. (G) Ecotopic expression of UAS-DP110 in 96 h AH clones results in dendritic arborizations that elaborate mainly in lateral territories of the neuropil with a few ectopic medial branches present in anterior and posterior neuropil. (H) Analysis of cell body size in wild-type (WT), RoboLOF, and UAS-DP110 96 h AH clones. (I–J) Plot profile graphs to reveal the distribution of dendrites along the medio-lateral axis within the leg neuropil (n = 8 for each genotype). The mean centre of mass (circle) for the dendrites of each genotype. The standard error of each experimental condition and the statistical significance between groups can also be seen. Triangles denote the 33rd percentile for each group. (K) Dorsoventral projection of a wild-type dendritic arborization of a motoneuron born at 96 h AH. (L) Dorsoventral projection of a Robo LOF 96 h AH motoneuron. (M) Dorsoventral projection of a CommGOF 96 h AH motoneuron. (N) Dorsoventral projection of a DP110 GOF 96 h AH motoneuron. (K–N) Dorsal is up. Anterior to right. Scale bars = 20 µm.
Mentions: To test this idea we next set out to establish if an induced increase in dendrite mass alone would result in dendrites “spilling over” into medial territories. We predicted that the cell autonomous activation of the insulin signalling pathway would allow us to change the global size of the cell whilst leaving other features of the environment the same. To do this we expressed the active subunit of PI3-Kinase, Dp110, which is sufficient to enlarge many different cell types [37]. To first determine how Dp110 changes neuronal morphology, we expressed it in the class IV dendritic arborizing sensory neuron ddaC, as the dendrites of these cells have a nearly two-dimensional organization, making them very amenable to morphometric analysis [38]. Using Volocity Acquisition software (version 4.2, Improvision), we imported raw data stacks and reconstructed 3D projections of the cell bodies of ddaC neurons from both control and experimental groups (Figure 7A and 7B). We then used the lasso tool to capture the cell body and subsequently measure the volume and found that control ddaC neurons had a mean soma volume of 2760.9±149.9 µm3 whereas the mean soma volume in the Dp110 group was 5702.2±142.3 µm3 (Figure 7C). To establish how the dendrites of the two groups were different, we performed Sholl analysis [39] to give a quantitative measure of dendrite complexity throughout the tree. The number of intersections between dendritic processes and Sholl-rings were counted in Photoshop using a template of 12 concentric circles (each 22 µm apart) centred on the cell body. We found the Dp110 expressing neurons distributed their branches in much the same manner as wild-type neurons, but had a two-fold increase in branch number (Figure 7A, 7B, and 7D). Thus Dp110 overexpression results in a two-fold increase in soma size that was mirrored with a two-fold increase in dendritic branch number.

Bottom Line: Thus the cellular distinctions in peripheral targets and central dendritic domains, which make up the myotopic map, are linked to the birth-order of these motoneurons.Our developmental analysis of dendrite growth reveals that this myotopic map is generated by targeting.We demonstrate that the medio-lateral positioning of motoneuron dendrites in the leg neuropil is controlled by the midline signalling systems Slit-Robo and Netrin-Fra.

View Article: PubMed Central - PubMed

Affiliation: Medical Research Council (MRC) Centre for Developmental Neurobiology, King's College London, London, United Kingdom.

ABSTRACT
Neural maps are emergent, highly ordered structures that are essential for organizing and presenting synaptic information. Within the embryonic nervous system of Drosophila motoneuron dendrites are organized topographically as a myotopic map that reflects their pattern of innervation in the muscle field. Here we reveal that this fundamental organizational principle exists in adult Drosophila, where the dendrites of leg motoneurons also generate a myotopic map. A single postembryonic neuroblast sequentially generates different leg motoneuron subtypes, starting with those innervating proximal targets and medial neuropil regions and producing progeny that innervate distal muscle targets and lateral neuropil later in the lineage. Thus the cellular distinctions in peripheral targets and central dendritic domains, which make up the myotopic map, are linked to the birth-order of these motoneurons. Our developmental analysis of dendrite growth reveals that this myotopic map is generated by targeting. We demonstrate that the medio-lateral positioning of motoneuron dendrites in the leg neuropil is controlled by the midline signalling systems Slit-Robo and Netrin-Fra. These results reveal that dendritic targeting plays a major role in the formation of myotopic maps and suggests that the coordinate spatial control of both pre- and postsynaptic elements by global neuropilar signals may be an important mechanism for establishing the specificity of synaptic connections.

Show MeSH
Related in: MedlinePlus