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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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Parasegmental Organisation of the Motor System(A) Distribution of motor neuron dendritic arbors relative to the domains of en expression. Neurons expressing the en gene were visualised (blue) using en-GAL4;UAS-CD8-GFP. ISN motor neuron dendrites (red) elaborate in the En domain (blue) of the neuromere, whereas SN motor neuron dendrites (green) form in the anterior half of the next posterior segment (asterisks indicate the segment borders). Thus, the motor system appears to be parasegmental in nature. The diagrams to the right indicate which motor neurons were labelled.(B–H) ISN motor neurons (red) with dorsal internal and SN motor neurons (green) with lateral external muscle targets were retrogradely labelled in 15-h-old wild-type embryos (B) and those mutant for different segment polarity genes (C–H). (C) to (H) should be compared with the wild-type control in (B). As far as could be ascertained, similar sets of motor neurons were labelled in the wild-type (B) and mutants (C–H). The neuropile, visualised with anti-HRP, is shown in blue (except for [F]). In all mutant embryos, with the exception of Df(gsb) (H), ISN and SN motor neurons have separate nerve roots and dendritic fields, as in the wild-type. As (H) shows, in Df(gsb) mutant embryos, ISN and SN nerve roots are frequently fused, yet the respective dendritic fields (arrows) do not appear to intermingle.Anterior is left and dorsal is up. Symbols and abbreviations: triangles, ventral midline; AC, anterior commissure; PC, posterior commissure (RP2 cell bodies, the most posterior of the ISN motor neurons, are indicated in [C] and [E]); 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-g004: Parasegmental Organisation of the Motor System(A) Distribution of motor neuron dendritic arbors relative to the domains of en expression. Neurons expressing the en gene were visualised (blue) using en-GAL4;UAS-CD8-GFP. ISN motor neuron dendrites (red) elaborate in the En domain (blue) of the neuromere, whereas SN motor neuron dendrites (green) form in the anterior half of the next posterior segment (asterisks indicate the segment borders). Thus, the motor system appears to be parasegmental in nature. The diagrams to the right indicate which motor neurons were labelled.(B–H) ISN motor neurons (red) with dorsal internal and SN motor neurons (green) with lateral external muscle targets were retrogradely labelled in 15-h-old wild-type embryos (B) and those mutant for different segment polarity genes (C–H). (C) to (H) should be compared with the wild-type control in (B). As far as could be ascertained, similar sets of motor neurons were labelled in the wild-type (B) and mutants (C–H). The neuropile, visualised with anti-HRP, is shown in blue (except for [F]). In all mutant embryos, with the exception of Df(gsb) (H), ISN and SN motor neurons have separate nerve roots and dendritic fields, as in the wild-type. As (H) shows, in Df(gsb) mutant embryos, ISN and SN nerve roots are frequently fused, yet the respective dendritic fields (arrows) do not appear to intermingle.Anterior is left and dorsal is up. Symbols and abbreviations: triangles, ventral midline; AC, anterior commissure; PC, posterior commissure (RP2 cell bodies, the most posterior of the ISN motor neurons, are indicated in [C] and [E]); asterisks, dorsoventral channels (landmarks for the segment borders). Scale bar (not applicable to diagrams of CNS and muscle field): 10 μm.

Mentions: Like the muscle field itself, the map of motor neuron dendrites is metamerically repeated. However, we find that the boundaries of these two units are out of register with one another, since the dendrites of the motor neurons innervating internal muscles lie in the next anterior neuromere. The anterior border of the dendritic map, as defined by the extent of these anterior dendrites, coincides with the anterior margin of engrailed (en) expression (Figure 4A). Thus, while the muscles are segmental in their organisation, the domains occupied by the dendrites of their innervating motor neurons are parasegmental.


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)

Parasegmental Organisation of the Motor System(A) Distribution of motor neuron dendritic arbors relative to the domains of en expression. Neurons expressing the en gene were visualised (blue) using en-GAL4;UAS-CD8-GFP. ISN motor neuron dendrites (red) elaborate in the En domain (blue) of the neuromere, whereas SN motor neuron dendrites (green) form in the anterior half of the next posterior segment (asterisks indicate the segment borders). Thus, the motor system appears to be parasegmental in nature. The diagrams to the right indicate which motor neurons were labelled.(B–H) ISN motor neurons (red) with dorsal internal and SN motor neurons (green) with lateral external muscle targets were retrogradely labelled in 15-h-old wild-type embryos (B) and those mutant for different segment polarity genes (C–H). (C) to (H) should be compared with the wild-type control in (B). As far as could be ascertained, similar sets of motor neurons were labelled in the wild-type (B) and mutants (C–H). The neuropile, visualised with anti-HRP, is shown in blue (except for [F]). In all mutant embryos, with the exception of Df(gsb) (H), ISN and SN motor neurons have separate nerve roots and dendritic fields, as in the wild-type. As (H) shows, in Df(gsb) mutant embryos, ISN and SN nerve roots are frequently fused, yet the respective dendritic fields (arrows) do not appear to intermingle.Anterior is left and dorsal is up. Symbols and abbreviations: triangles, ventral midline; AC, anterior commissure; PC, posterior commissure (RP2 cell bodies, the most posterior of the ISN motor neurons, are indicated in [C] and [E]); 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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getmorefigures.php?uid=PMC261881&req=5

pbio.0000041-g004: Parasegmental Organisation of the Motor System(A) Distribution of motor neuron dendritic arbors relative to the domains of en expression. Neurons expressing the en gene were visualised (blue) using en-GAL4;UAS-CD8-GFP. ISN motor neuron dendrites (red) elaborate in the En domain (blue) of the neuromere, whereas SN motor neuron dendrites (green) form in the anterior half of the next posterior segment (asterisks indicate the segment borders). Thus, the motor system appears to be parasegmental in nature. The diagrams to the right indicate which motor neurons were labelled.(B–H) ISN motor neurons (red) with dorsal internal and SN motor neurons (green) with lateral external muscle targets were retrogradely labelled in 15-h-old wild-type embryos (B) and those mutant for different segment polarity genes (C–H). (C) to (H) should be compared with the wild-type control in (B). As far as could be ascertained, similar sets of motor neurons were labelled in the wild-type (B) and mutants (C–H). The neuropile, visualised with anti-HRP, is shown in blue (except for [F]). In all mutant embryos, with the exception of Df(gsb) (H), ISN and SN motor neurons have separate nerve roots and dendritic fields, as in the wild-type. As (H) shows, in Df(gsb) mutant embryos, ISN and SN nerve roots are frequently fused, yet the respective dendritic fields (arrows) do not appear to intermingle.Anterior is left and dorsal is up. Symbols and abbreviations: triangles, ventral midline; AC, anterior commissure; PC, posterior commissure (RP2 cell bodies, the most posterior of the ISN motor neurons, are indicated in [C] and [E]); asterisks, dorsoventral channels (landmarks for the segment borders). Scale bar (not applicable to diagrams of CNS and muscle field): 10 μm.
Mentions: Like the muscle field itself, the map of motor neuron dendrites is metamerically repeated. However, we find that the boundaries of these two units are out of register with one another, since the dendrites of the motor neurons innervating internal muscles lie in the next anterior neuromere. The anterior border of the dendritic map, as defined by the extent of these anterior dendrites, coincides with the anterior margin of engrailed (en) expression (Figure 4A). Thus, while the muscles are segmental in their organisation, the domains occupied by the dendrites of their innervating motor neurons are parasegmental.

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