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Embryonic origins of a motor system: motor dendrites form a myotopic map in Drosophila.

Landgraf M, Jeffrey V, Fujioka M, Jaynes JB, Bate M - PLoS Biol. (2003)

Bottom Line: This is likely to be mirrored, at least in part, by endings of higher-order neurons from central pattern-generating circuits, which converge onto the motor neuron dendrites.These findings will greatly simplify the task of understanding how a locomotor system is assembled.Our results suggest that the cues that organise the myotopic map may be laid down early in development as the embryo subdivides into parasegmental units.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Cambridge, Cambridge, United Kingdom. ml10006@cus.cam.ac.uk

ABSTRACT
The organisational principles of locomotor networks are less well understood than those of many sensory systems, where in-growing axon terminals form a central map of peripheral characteristics. Using the neuromuscular system of the Drosophila embryo as a model and retrograde tracing and genetic methods, we have uncovered principles underlying the organisation of the motor system. We find that dendritic arbors of motor neurons, rather than their cell bodies, are partitioned into domains to form a myotopic map, which represents centrally the distribution of body wall muscles peripherally. While muscles are segmental, the myotopic map is parasegmental in organisation. It forms by an active process of dendritic growth independent of the presence of target muscles, proper differentiation of glial cells, or (in its initial partitioning) competitive interactions between adjacent dendritic domains. The arrangement of motor neuron dendrites into a myotopic map represents a first layer of organisation in the motor system. This is likely to be mirrored, at least in part, by endings of higher-order neurons from central pattern-generating circuits, which converge onto the motor neuron dendrites. These findings will greatly simplify the task of understanding how a locomotor system is assembled. Our results suggest that the cues that organise the myotopic map may be laid down early in development as the embryo subdivides into parasegmental units.

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The Myotopic Map Forms Independently of Target MusclesISN motor neurons (red) with internal and SN motor neurons (green) with external muscle targets in a 15-h-old wild-type (A) and in an embryo, in which muscle formation had been suppressed by targeted expression of an activated form (intracellular domain) of Notch (24B-GAL4; UAS-Notch*) (B). In such muscleless embryos, the main nerve trunks (ISN and SN) still form and project into the periphery along distinctive paths. Thus, motor neurons whose axons project through these nerves can be retrogradely labelled. The neuropile, visualised with anti-HRP, is shown in blue. ISN and SN motor neuron dendritic domains show a normal separation despite absence of target muscles. Note that the ISN (red) and SN (green) dendritic arbors in (B) appear to be in closer proximity than those shown in (A). This is because in (B) the RP2 neuron (indicated) is labelled, which is the most posterior of the ISN motor neurons and therefore closest to the SN dendritic domain. See also Figure 2G, where RP2 and its dendrites are shown relative to the most posterior of the SN motor neuron (SBM) dendritic fields.Anterior is left and dorsal is up. Symbols and abbreviations: triangles, ventral midline; AC, anterior commissure; PC, posterior commissure; asterisks, dorsoventral channels (landmarks for the segment borders). Scale bar (not applicable to diagrams of CNS and muscle field): 10 μm.
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pbio.0000041-g006: The Myotopic Map Forms Independently of Target MusclesISN motor neurons (red) with internal and SN motor neurons (green) with external muscle targets in a 15-h-old wild-type (A) and in an embryo, in which muscle formation had been suppressed by targeted expression of an activated form (intracellular domain) of Notch (24B-GAL4; UAS-Notch*) (B). In such muscleless embryos, the main nerve trunks (ISN and SN) still form and project into the periphery along distinctive paths. Thus, motor neurons whose axons project through these nerves can be retrogradely labelled. The neuropile, visualised with anti-HRP, is shown in blue. ISN and SN motor neuron dendritic domains show a normal separation despite absence of target muscles. Note that the ISN (red) and SN (green) dendritic arbors in (B) appear to be in closer proximity than those shown in (A). This is because in (B) the RP2 neuron (indicated) is labelled, which is the most posterior of the ISN motor neurons and therefore closest to the SN dendritic domain. See also Figure 2G, where RP2 and its dendrites are shown relative to the most posterior of the SN motor neuron (SBM) dendritic fields.Anterior is left and dorsal is up. Symbols and abbreviations: triangles, ventral midline; AC, anterior commissure; PC, posterior commissure; asterisks, dorsoventral channels (landmarks for the segment borders). Scale bar (not applicable to diagrams of CNS and muscle field): 10 μm.

Mentions: Since dendritic arbors form after motor axons have reached their targets, the muscles could be instrumental in dictating the organisation of the central map. To test this idea, we used the UAS/GAL4 system (Brand and Perrimon 1993) to misexpress an activated form of Notch (Kidd et al. 1998) in the developing mesoderm, so suppressing the formation of muscle founder cells while leaving other tissues intact (Landgraf et al. 1999). In such muscleless embryos, the main nerve trunks, SN and ISN, still form and project into the periphery (Landgraf et al. 1999). Retrograde labellings of these nerves show that SN and ISN motor neurons form relatively normal dendritic arbors that consistently conform to the characteristic separation of SN and ISN dendrites (Figure 6).


Embryonic origins of a motor system: motor dendrites form a myotopic map in Drosophila.

Landgraf M, Jeffrey V, Fujioka M, Jaynes JB, Bate M - PLoS Biol. (2003)

The Myotopic Map Forms Independently of Target MusclesISN motor neurons (red) with internal and SN motor neurons (green) with external muscle targets in a 15-h-old wild-type (A) and in an embryo, in which muscle formation had been suppressed by targeted expression of an activated form (intracellular domain) of Notch (24B-GAL4; UAS-Notch*) (B). In such muscleless embryos, the main nerve trunks (ISN and SN) still form and project into the periphery along distinctive paths. Thus, motor neurons whose axons project through these nerves can be retrogradely labelled. The neuropile, visualised with anti-HRP, is shown in blue. ISN and SN motor neuron dendritic domains show a normal separation despite absence of target muscles. Note that the ISN (red) and SN (green) dendritic arbors in (B) appear to be in closer proximity than those shown in (A). This is because in (B) the RP2 neuron (indicated) is labelled, which is the most posterior of the ISN motor neurons and therefore closest to the SN dendritic domain. See also Figure 2G, where RP2 and its dendrites are shown relative to the most posterior of the SN motor neuron (SBM) dendritic fields.Anterior is left and dorsal is up. Symbols and abbreviations: triangles, ventral midline; AC, anterior commissure; PC, posterior commissure; asterisks, dorsoventral channels (landmarks for the segment borders). Scale bar (not applicable to diagrams of CNS and muscle field): 10 μm.
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Related In: Results  -  Collection

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pbio.0000041-g006: The Myotopic Map Forms Independently of Target MusclesISN motor neurons (red) with internal and SN motor neurons (green) with external muscle targets in a 15-h-old wild-type (A) and in an embryo, in which muscle formation had been suppressed by targeted expression of an activated form (intracellular domain) of Notch (24B-GAL4; UAS-Notch*) (B). In such muscleless embryos, the main nerve trunks (ISN and SN) still form and project into the periphery along distinctive paths. Thus, motor neurons whose axons project through these nerves can be retrogradely labelled. The neuropile, visualised with anti-HRP, is shown in blue. ISN and SN motor neuron dendritic domains show a normal separation despite absence of target muscles. Note that the ISN (red) and SN (green) dendritic arbors in (B) appear to be in closer proximity than those shown in (A). This is because in (B) the RP2 neuron (indicated) is labelled, which is the most posterior of the ISN motor neurons and therefore closest to the SN dendritic domain. See also Figure 2G, where RP2 and its dendrites are shown relative to the most posterior of the SN motor neuron (SBM) dendritic fields.Anterior is left and dorsal is up. Symbols and abbreviations: triangles, ventral midline; AC, anterior commissure; PC, posterior commissure; asterisks, dorsoventral channels (landmarks for the segment borders). Scale bar (not applicable to diagrams of CNS and muscle field): 10 μm.
Mentions: Since dendritic arbors form after motor axons have reached their targets, the muscles could be instrumental in dictating the organisation of the central map. To test this idea, we used the UAS/GAL4 system (Brand and Perrimon 1993) to misexpress an activated form of Notch (Kidd et al. 1998) in the developing mesoderm, so suppressing the formation of muscle founder cells while leaving other tissues intact (Landgraf et al. 1999). In such muscleless embryos, the main nerve trunks, SN and ISN, still form and project into the periphery (Landgraf et al. 1999). Retrograde labellings of these nerves show that SN and ISN motor neurons form relatively normal dendritic arbors that consistently conform to the characteristic separation of SN and ISN dendrites (Figure 6).

Bottom Line: This is likely to be mirrored, at least in part, by endings of higher-order neurons from central pattern-generating circuits, which converge onto the motor neuron dendrites.These findings will greatly simplify the task of understanding how a locomotor system is assembled.Our results suggest that the cues that organise the myotopic map may be laid down early in development as the embryo subdivides into parasegmental units.

View Article: PubMed Central - PubMed

Affiliation: Department of Zoology, University of Cambridge, Cambridge, United Kingdom. ml10006@cus.cam.ac.uk

ABSTRACT
The organisational principles of locomotor networks are less well understood than those of many sensory systems, where in-growing axon terminals form a central map of peripheral characteristics. Using the neuromuscular system of the Drosophila embryo as a model and retrograde tracing and genetic methods, we have uncovered principles underlying the organisation of the motor system. We find that dendritic arbors of motor neurons, rather than their cell bodies, are partitioned into domains to form a myotopic map, which represents centrally the distribution of body wall muscles peripherally. While muscles are segmental, the myotopic map is parasegmental in organisation. It forms by an active process of dendritic growth independent of the presence of target muscles, proper differentiation of glial cells, or (in its initial partitioning) competitive interactions between adjacent dendritic domains. The arrangement of motor neuron dendrites into a myotopic map represents a first layer of organisation in the motor system. This is likely to be mirrored, at least in part, by endings of higher-order neurons from central pattern-generating circuits, which converge onto the motor neuron dendrites. These findings will greatly simplify the task of understanding how a locomotor system is assembled. Our results suggest that the cues that organise the myotopic map may be laid down early in development as the embryo subdivides into parasegmental units.

Show MeSH
Related in: MedlinePlus