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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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Motor Neuron Dendrites Form a Myotopic Map of the Muscle FieldCollage of superimposed representative motor neurons (of 15-h-old embryos) that innervate the muscles of an abdominal half-segment (shown right). Entire dendritic domains are indicated on the contralateral side. Colour code: blue, ventral internal; yellow, dorsolateral internal; red, dorsal internal; green, external; black, neuropile; grey, cortex. Anterior is left and (for the muscle diagram) dorsal is up.Symbols and abbreviations: triangles, ventral midline; asterisks, dorsoventral channels (landmarks for the segment borders); AC, anterior commissure; PC, posterior commissure.
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pbio.0000041-g003: Motor Neuron Dendrites Form a Myotopic Map of the Muscle FieldCollage of superimposed representative motor neurons (of 15-h-old embryos) that innervate the muscles of an abdominal half-segment (shown right). Entire dendritic domains are indicated on the contralateral side. Colour code: blue, ventral internal; yellow, dorsolateral internal; red, dorsal internal; green, external; black, neuropile; grey, cortex. Anterior is left and (for the muscle diagram) dorsal is up.Symbols and abbreviations: triangles, ventral midline; asterisks, dorsoventral channels (landmarks for the segment borders); AC, anterior commissure; PC, posterior commissure.

Mentions: To put the idea of a regular map to the test, we focused on an unusual external motor neuron–muscle pair. Muscle VT1 is innervated by a TN rather than an SN motor neuron (Gorczyca et al. 1994; Landgraf et al. 1997). However, VT1 lies at the same place in the anteroposterior axis as the SBM, although VT1 is ventral and the SBM more dorsal. We find that the VT1 motor neuron dendritic field overlaps with that of the SBM motor neuron (Figure 2C). For the external set, we conclude that differences in target muscle location in the anteroposterior axis are mapped centrally as regular differences in dendritic position, but dorsoventral distinctions are not (Figure 3).


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)

Motor Neuron Dendrites Form a Myotopic Map of the Muscle FieldCollage of superimposed representative motor neurons (of 15-h-old embryos) that innervate the muscles of an abdominal half-segment (shown right). Entire dendritic domains are indicated on the contralateral side. Colour code: blue, ventral internal; yellow, dorsolateral internal; red, dorsal internal; green, external; black, neuropile; grey, cortex. Anterior is left and (for the muscle diagram) dorsal is up.Symbols and abbreviations: triangles, ventral midline; asterisks, dorsoventral channels (landmarks for the segment borders); AC, anterior commissure; PC, posterior commissure.
© Copyright Policy
Related In: Results  -  Collection

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

pbio.0000041-g003: Motor Neuron Dendrites Form a Myotopic Map of the Muscle FieldCollage of superimposed representative motor neurons (of 15-h-old embryos) that innervate the muscles of an abdominal half-segment (shown right). Entire dendritic domains are indicated on the contralateral side. Colour code: blue, ventral internal; yellow, dorsolateral internal; red, dorsal internal; green, external; black, neuropile; grey, cortex. Anterior is left and (for the muscle diagram) dorsal is up.Symbols and abbreviations: triangles, ventral midline; asterisks, dorsoventral channels (landmarks for the segment borders); AC, anterior commissure; PC, posterior commissure.
Mentions: To put the idea of a regular map to the test, we focused on an unusual external motor neuron–muscle pair. Muscle VT1 is innervated by a TN rather than an SN motor neuron (Gorczyca et al. 1994; Landgraf et al. 1997). However, VT1 lies at the same place in the anteroposterior axis as the SBM, although VT1 is ventral and the SBM more dorsal. We find that the VT1 motor neuron dendritic field overlaps with that of the SBM motor neuron (Figure 2C). For the external set, we conclude that differences in target muscle location in the anteroposterior axis are mapped centrally as regular differences in dendritic position, but dorsoventral distinctions are not (Figure 3).

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