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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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Organisation of the Larval Motor System(A) Diagrams of abdominal body wall muscles of one half segment (top) and of the VNC (bottom). These diagrams are included in most subsequent figures as reference for the relative positions of muscles and their innervating motor neurons. Internal muscles are red; external muscles, green. Muscle nomenclature is according to Bate (1993): muscle position (D, dorsal; L, lateral; V, ventral), followed by orientation (A, acute; L, longitudinal; O, oblique; T, transverse) and SBM. In the VNC, cell bodies of motor neurons innervating an abdominal half-segment are indicated: red shows ISN with internal muscle targets; green shows SN with external muscle targets. The TN (brown) coincides approximately with the segment boundary. TN exit glia (asterisk) located on the ventral midline are also shown. The neuropile is indicated in black.(B and C) Retrograde fills of ISN and SN motor neurons in 15-h-old wild-type embryos. The neuropile (blue) was visualised with anti-HRP. ISN and SN motor neurons innervating muscles in the same segment elaborate their dendrites (arrows) in distinct regions. In (B), groups of ISN and SN motor neurons are labelled in two consecutive segments. In (C), individual ISN and SN motor neurons of a segment are shown.(D) The separation between ISN and SN motor neuron dendrites appears to be maintained, at least until 19 h AEL, when the motor system is functional.Anterior is left and dorsal is up. Symbols and abbreviations: triangles, ventral midline; AC, anterior commissure; PC, posterior commissure; asterisks, TN exit glia in (A) and dorsoventral channels, which are landmarks for the segment borders, in (B)–(D). Scale bar (not applicable to diagrams of CNS and muscle field): (B) 18 μm; (C–D) 14 μm. n numbers refer to the number of segments in which the same types of motor neurons (e.g., RP3 and SBM in [C]) were labelled.
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pbio.0000041-g001: Organisation of the Larval Motor System(A) Diagrams of abdominal body wall muscles of one half segment (top) and of the VNC (bottom). These diagrams are included in most subsequent figures as reference for the relative positions of muscles and their innervating motor neurons. Internal muscles are red; external muscles, green. Muscle nomenclature is according to Bate (1993): muscle position (D, dorsal; L, lateral; V, ventral), followed by orientation (A, acute; L, longitudinal; O, oblique; T, transverse) and SBM. In the VNC, cell bodies of motor neurons innervating an abdominal half-segment are indicated: red shows ISN with internal muscle targets; green shows SN with external muscle targets. The TN (brown) coincides approximately with the segment boundary. TN exit glia (asterisk) located on the ventral midline are also shown. The neuropile is indicated in black.(B and C) Retrograde fills of ISN and SN motor neurons in 15-h-old wild-type embryos. The neuropile (blue) was visualised with anti-HRP. ISN and SN motor neurons innervating muscles in the same segment elaborate their dendrites (arrows) in distinct regions. In (B), groups of ISN and SN motor neurons are labelled in two consecutive segments. In (C), individual ISN and SN motor neurons of a segment are shown.(D) The separation between ISN and SN motor neuron dendrites appears to be maintained, at least until 19 h AEL, when the motor system is functional.Anterior is left and dorsal is up. Symbols and abbreviations: triangles, ventral midline; AC, anterior commissure; PC, posterior commissure; asterisks, TN exit glia in (A) and dorsoventral channels, which are landmarks for the segment borders, in (B)–(D). Scale bar (not applicable to diagrams of CNS and muscle field): (B) 18 μm; (C–D) 14 μm. n numbers refer to the number of segments in which the same types of motor neurons (e.g., RP3 and SBM in [C]) were labelled.

Mentions: Motor axons project into the muscle field via two main nerves, the intersegmental (ISN) and the segmental nerve (SN) (Bate 1982; Thomas et al. 1984; Landgraf et al. 1997). The transverse nerve (TN) runs along the segment border and has few motor axons (Figure 1A) (Chiang et al. 1994; Gorczyca et al. 1994; Thor and Thomas 1997; Schmid et al. 1999). Choice of nerve root is one of several features that divide the motor neurons into two principal sets, the ISN and SN. First, the cell bodies of SN motor neurons are located in the same segment as the muscles that they innervate, whereas ISN motor neuron somata are located in the segment next anterior (with the exception of the RP2 and two neuromodulatory efferent ventral unpaired median [VUM] neurons; Figure 1A) (Landgraf et al. 1997). Second, ISN motor neurons innervate internal muscles, which span a segment from anterior to posterior, whereas SN (and the TN) motor neurons innervate external muscles. External muscles are distinct from the internal set in several respects: (a) they are generally transverse; (b) unlike internal muscles, they require wingless (wg) signalling for their specification (Baylies et al. 1995); (c) external (but not internal) muscles and their innervating motor neurons express the cell adhesion molecule (CAM) Connectin, with the single exception of muscle ventral transverse 1 (VT1) (Nose et al. 1992; Meadows et al. 1994; (Prokop et al. 1996).


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)

Organisation of the Larval Motor System(A) Diagrams of abdominal body wall muscles of one half segment (top) and of the VNC (bottom). These diagrams are included in most subsequent figures as reference for the relative positions of muscles and their innervating motor neurons. Internal muscles are red; external muscles, green. Muscle nomenclature is according to Bate (1993): muscle position (D, dorsal; L, lateral; V, ventral), followed by orientation (A, acute; L, longitudinal; O, oblique; T, transverse) and SBM. In the VNC, cell bodies of motor neurons innervating an abdominal half-segment are indicated: red shows ISN with internal muscle targets; green shows SN with external muscle targets. The TN (brown) coincides approximately with the segment boundary. TN exit glia (asterisk) located on the ventral midline are also shown. The neuropile is indicated in black.(B and C) Retrograde fills of ISN and SN motor neurons in 15-h-old wild-type embryos. The neuropile (blue) was visualised with anti-HRP. ISN and SN motor neurons innervating muscles in the same segment elaborate their dendrites (arrows) in distinct regions. In (B), groups of ISN and SN motor neurons are labelled in two consecutive segments. In (C), individual ISN and SN motor neurons of a segment are shown.(D) The separation between ISN and SN motor neuron dendrites appears to be maintained, at least until 19 h AEL, when the motor system is functional.Anterior is left and dorsal is up. Symbols and abbreviations: triangles, ventral midline; AC, anterior commissure; PC, posterior commissure; asterisks, TN exit glia in (A) and dorsoventral channels, which are landmarks for the segment borders, in (B)–(D). Scale bar (not applicable to diagrams of CNS and muscle field): (B) 18 μm; (C–D) 14 μm. n numbers refer to the number of segments in which the same types of motor neurons (e.g., RP3 and SBM in [C]) were labelled.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC261881&req=5

pbio.0000041-g001: Organisation of the Larval Motor System(A) Diagrams of abdominal body wall muscles of one half segment (top) and of the VNC (bottom). These diagrams are included in most subsequent figures as reference for the relative positions of muscles and their innervating motor neurons. Internal muscles are red; external muscles, green. Muscle nomenclature is according to Bate (1993): muscle position (D, dorsal; L, lateral; V, ventral), followed by orientation (A, acute; L, longitudinal; O, oblique; T, transverse) and SBM. In the VNC, cell bodies of motor neurons innervating an abdominal half-segment are indicated: red shows ISN with internal muscle targets; green shows SN with external muscle targets. The TN (brown) coincides approximately with the segment boundary. TN exit glia (asterisk) located on the ventral midline are also shown. The neuropile is indicated in black.(B and C) Retrograde fills of ISN and SN motor neurons in 15-h-old wild-type embryos. The neuropile (blue) was visualised with anti-HRP. ISN and SN motor neurons innervating muscles in the same segment elaborate their dendrites (arrows) in distinct regions. In (B), groups of ISN and SN motor neurons are labelled in two consecutive segments. In (C), individual ISN and SN motor neurons of a segment are shown.(D) The separation between ISN and SN motor neuron dendrites appears to be maintained, at least until 19 h AEL, when the motor system is functional.Anterior is left and dorsal is up. Symbols and abbreviations: triangles, ventral midline; AC, anterior commissure; PC, posterior commissure; asterisks, TN exit glia in (A) and dorsoventral channels, which are landmarks for the segment borders, in (B)–(D). Scale bar (not applicable to diagrams of CNS and muscle field): (B) 18 μm; (C–D) 14 μm. n numbers refer to the number of segments in which the same types of motor neurons (e.g., RP3 and SBM in [C]) were labelled.
Mentions: Motor axons project into the muscle field via two main nerves, the intersegmental (ISN) and the segmental nerve (SN) (Bate 1982; Thomas et al. 1984; Landgraf et al. 1997). The transverse nerve (TN) runs along the segment border and has few motor axons (Figure 1A) (Chiang et al. 1994; Gorczyca et al. 1994; Thor and Thomas 1997; Schmid et al. 1999). Choice of nerve root is one of several features that divide the motor neurons into two principal sets, the ISN and SN. First, the cell bodies of SN motor neurons are located in the same segment as the muscles that they innervate, whereas ISN motor neuron somata are located in the segment next anterior (with the exception of the RP2 and two neuromodulatory efferent ventral unpaired median [VUM] neurons; Figure 1A) (Landgraf et al. 1997). Second, ISN motor neurons innervate internal muscles, which span a segment from anterior to posterior, whereas SN (and the TN) motor neurons innervate external muscles. External muscles are distinct from the internal set in several respects: (a) they are generally transverse; (b) unlike internal muscles, they require wingless (wg) signalling for their specification (Baylies et al. 1995); (c) external (but not internal) muscles and their innervating motor neurons express the cell adhesion molecule (CAM) Connectin, with the single exception of muscle ventral transverse 1 (VT1) (Nose et al. 1992; Meadows et al. 1994; (Prokop et al. 1996).

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