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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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Glial Cell Differentiation Is Not Required for Neuropile SubdivisionISN (red) and SN (green) motor neurons labelled in 15-h-old wild-type (A and C) and gcm mutant (B and D) embryos. The neuropile, visualised with anti-HRP, is shown in blue.(A and B) Motor neurons innervating ventral (VL3–VL4, RP3) internal (red) and external (green) muscles of a segment elaborate their dendrites in separate regions of the neuropile on either side of the segment border (asterisks). This is accentuated when neuromeres separate in gcm mutant embryos (B).(C and D) The DT1 motor neuron (red) is the only ISN motor neuron whose dendrites branch in the SN dendritic domain (green). This dendritic projection pattern is maintained in gcm mutant embryos (D). An SN VUM efferent neuron has also been labelled.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-g007: Glial Cell Differentiation Is Not Required for Neuropile SubdivisionISN (red) and SN (green) motor neurons labelled in 15-h-old wild-type (A and C) and gcm mutant (B and D) embryos. The neuropile, visualised with anti-HRP, is shown in blue.(A and B) Motor neurons innervating ventral (VL3–VL4, RP3) internal (red) and external (green) muscles of a segment elaborate their dendrites in separate regions of the neuropile on either side of the segment border (asterisks). This is accentuated when neuromeres separate in gcm mutant embryos (B).(C and D) The DT1 motor neuron (red) is the only ISN motor neuron whose dendrites branch in the SN dendritic domain (green). This dendritic projection pattern is maintained in gcm mutant embryos (D). An SN VUM efferent neuron has also been labelled.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: We next asked whether motor neuron dendritic fields could be patterned by the substrates on which they grow. In the Drosophila ventral nerve cord (VNC), motor neuron dendrites form in the dorsal-most region of the neuropile, sandwiched between longitudinal glia above and the underlying scaffold of axons. Glial cells can act as substrates for supporting and guiding axonal growth (Bastiani and Goodman 1986; Hidalgo et al. 1995; Booth et al. 2000). To test whether they might also be required for the growth and spatial patterning of dendritic fields, we analysed dendritic arbors in glial cells missing (gcm) mutant embryos, which are defective in glial cell differentiation (Hosoya et al. 1995; Jones et al. 1995). Although the structure of the nervous system is disrupted in gcm mutant embryos and the dendritic arbors are abnormal, they continue to form in their characteristic locations and the fundamental distinction between the ISN and SN motor neuron dendritic fields is maintained (Figure 7A and 7B). Remarkably, even the long posterior dendritic projection of the DT1 motor neuron forms and reaches its target region, the SN external muscle dendritic domain (Figure 7C and 7D).


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)

Glial Cell Differentiation Is Not Required for Neuropile SubdivisionISN (red) and SN (green) motor neurons labelled in 15-h-old wild-type (A and C) and gcm mutant (B and D) embryos. The neuropile, visualised with anti-HRP, is shown in blue.(A and B) Motor neurons innervating ventral (VL3–VL4, RP3) internal (red) and external (green) muscles of a segment elaborate their dendrites in separate regions of the neuropile on either side of the segment border (asterisks). This is accentuated when neuromeres separate in gcm mutant embryos (B).(C and D) The DT1 motor neuron (red) is the only ISN motor neuron whose dendrites branch in the SN dendritic domain (green). This dendritic projection pattern is maintained in gcm mutant embryos (D). An SN VUM efferent neuron has also been labelled.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.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC261881&req=5

pbio.0000041-g007: Glial Cell Differentiation Is Not Required for Neuropile SubdivisionISN (red) and SN (green) motor neurons labelled in 15-h-old wild-type (A and C) and gcm mutant (B and D) embryos. The neuropile, visualised with anti-HRP, is shown in blue.(A and B) Motor neurons innervating ventral (VL3–VL4, RP3) internal (red) and external (green) muscles of a segment elaborate their dendrites in separate regions of the neuropile on either side of the segment border (asterisks). This is accentuated when neuromeres separate in gcm mutant embryos (B).(C and D) The DT1 motor neuron (red) is the only ISN motor neuron whose dendrites branch in the SN dendritic domain (green). This dendritic projection pattern is maintained in gcm mutant embryos (D). An SN VUM efferent neuron has also been labelled.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: We next asked whether motor neuron dendritic fields could be patterned by the substrates on which they grow. In the Drosophila ventral nerve cord (VNC), motor neuron dendrites form in the dorsal-most region of the neuropile, sandwiched between longitudinal glia above and the underlying scaffold of axons. Glial cells can act as substrates for supporting and guiding axonal growth (Bastiani and Goodman 1986; Hidalgo et al. 1995; Booth et al. 2000). To test whether they might also be required for the growth and spatial patterning of dendritic fields, we analysed dendritic arbors in glial cells missing (gcm) mutant embryos, which are defective in glial cell differentiation (Hosoya et al. 1995; Jones et al. 1995). Although the structure of the nervous system is disrupted in gcm mutant embryos and the dendritic arbors are abnormal, they continue to form in their characteristic locations and the fundamental distinction between the ISN and SN motor neuron dendritic fields is maintained (Figure 7A and 7B). Remarkably, even the long posterior dendritic projection of the DT1 motor neuron forms and reaches its target region, the SN external muscle dendritic domain (Figure 7C and 7D).

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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