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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 by an Active Process of Dendritic Growth and ArborisationISN motor neurons (indicated in muscle diagrams) were retrogradely labelled in 15-h-old wild-type embryos. The neuropile, visualised with anti-HRP, is shown in blue.(A) External transverse muscle DT1 is innervated by an ISN motor neuron (green) whose dendrites overlap with those of the SBM motor neuron (red).(B and C) Internal muscles DO3–DO5 are innervated by motor neurons derived from the same NB as the DT1 motor neuron, and all have common axonal trajectories. However, dendrites of the DO3–DO5 motor neurons (arrowheads) form anterior to those of the DT1 (arrow in [B]) and the SN motor neurons (arrow in [C]).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-g005: The Myotopic Map Forms by an Active Process of Dendritic Growth and ArborisationISN motor neurons (indicated in muscle diagrams) were retrogradely labelled in 15-h-old wild-type embryos. The neuropile, visualised with anti-HRP, is shown in blue.(A) External transverse muscle DT1 is innervated by an ISN motor neuron (green) whose dendrites overlap with those of the SBM motor neuron (red).(B and C) Internal muscles DO3–DO5 are innervated by motor neurons derived from the same NB as the DT1 motor neuron, and all have common axonal trajectories. However, dendrites of the DO3–DO5 motor neurons (arrowheads) form anterior to those of the DT1 (arrow in [B]) and the SN motor neurons (arrow in [C]).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 what mechanisms underlie the formation of the myotopic map. Because ISN and SN motor neurons lie at different positions in the CNS and their axons grow out into the muscle field through different nerves, it is reasonable to suppose that at least the major subdivision of dendritic arborisations into internal and external domains could be a byproduct of the locations at which the motor neurons are generated and the paths taken by their growing axons. We can exclude this ‘passive mapping' explanation by considering a single motor neuron–muscle pair, namely dorsal transverse 1 (DT1) and its innervating motor neuron. DT1 is an external muscle (by position, orientation, wg dependence, and Connectin expression), yet its motor neuron is clustered with the internal muscle innervating set and its axon (uniquely for the external muscles) grows out through the ISN. Despite its packing within the ‘internal motor neuron' set, the DT1 motor neuron makes a long posterior projection through the internal muscle domain of the myotopic map to reach the external domain, where it arborises appropriately, reflecting the orientation and external nature of its target muscle (Figure 5A). In contrast, motor neurons derived from the same NB as DT1 innervate neighbouring internal muscles DO3–DO5 and put their dendrites in a more anterior region characteristic of the dorsolateral muscles (Figure 5B and 5C) (Landgraf et al. 1997). These findings strongly suggest that the mapping of the muscle field within the CNS is an active process of growth and arborisation that partitions dendrites into subdomains of the neuropile that are appropriate to their function, rather than a passive subdivision of available space by position of origin or axon trajectory.


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 by an Active Process of Dendritic Growth and ArborisationISN motor neurons (indicated in muscle diagrams) were retrogradely labelled in 15-h-old wild-type embryos. The neuropile, visualised with anti-HRP, is shown in blue.(A) External transverse muscle DT1 is innervated by an ISN motor neuron (green) whose dendrites overlap with those of the SBM motor neuron (red).(B and C) Internal muscles DO3–DO5 are innervated by motor neurons derived from the same NB as the DT1 motor neuron, and all have common axonal trajectories. However, dendrites of the DO3–DO5 motor neurons (arrowheads) form anterior to those of the DT1 (arrow in [B]) and the SN motor neurons (arrow in [C]).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

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getmorefigures.php?uid=PMC261881&req=5

pbio.0000041-g005: The Myotopic Map Forms by an Active Process of Dendritic Growth and ArborisationISN motor neurons (indicated in muscle diagrams) were retrogradely labelled in 15-h-old wild-type embryos. The neuropile, visualised with anti-HRP, is shown in blue.(A) External transverse muscle DT1 is innervated by an ISN motor neuron (green) whose dendrites overlap with those of the SBM motor neuron (red).(B and C) Internal muscles DO3–DO5 are innervated by motor neurons derived from the same NB as the DT1 motor neuron, and all have common axonal trajectories. However, dendrites of the DO3–DO5 motor neurons (arrowheads) form anterior to those of the DT1 (arrow in [B]) and the SN motor neurons (arrow in [C]).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 what mechanisms underlie the formation of the myotopic map. Because ISN and SN motor neurons lie at different positions in the CNS and their axons grow out into the muscle field through different nerves, it is reasonable to suppose that at least the major subdivision of dendritic arborisations into internal and external domains could be a byproduct of the locations at which the motor neurons are generated and the paths taken by their growing axons. We can exclude this ‘passive mapping' explanation by considering a single motor neuron–muscle pair, namely dorsal transverse 1 (DT1) and its innervating motor neuron. DT1 is an external muscle (by position, orientation, wg dependence, and Connectin expression), yet its motor neuron is clustered with the internal muscle innervating set and its axon (uniquely for the external muscles) grows out through the ISN. Despite its packing within the ‘internal motor neuron' set, the DT1 motor neuron makes a long posterior projection through the internal muscle domain of the myotopic map to reach the external domain, where it arborises appropriately, reflecting the orientation and external nature of its target muscle (Figure 5A). In contrast, motor neurons derived from the same NB as DT1 innervate neighbouring internal muscles DO3–DO5 and put their dendrites in a more anterior region characteristic of the dorsolateral muscles (Figure 5B and 5C) (Landgraf et al. 1997). These findings strongly suggest that the mapping of the muscle field within the CNS is an active process of growth and arborisation that partitions dendrites into subdomains of the neuropile that are appropriate to their function, rather than a passive subdivision of available space by position of origin or axon trajectory.

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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