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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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Related in: MedlinePlus

Central Myotopic Representation of the Muscle FieldMotor neurons with external (A–C) and internal (D–G) muscle targets (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) Motor neurons with ventral and lateral external muscle targets at a similar location in the anteroposterior axis elaborate their dendritic arbors in a common region of the neuropile, within the SN dendritic domain, which represents external muscles.(B) Differences in muscle positions in the anteroposterior axis are reflected centrally by corresponding distinctions in the anteroposterior locations of motor neuron dendritic fields.(C) Muscle VT1 is innervated by a TN motor neuron (and frequently also by its contralateral homologue, partly shown). Dendrites of the VT1 motor neuron (arrow) coincide with those of the SBM motor neuron of the next anterior segment. Note that in (A) the position of the SBM dendritic field is shifted somewhat anteriorly relative to the commissural landmarks as compared to (B) and (C). We observe such shifts relative to the commissural landmarks in 13% (n = 52) of SBM (and other) motor neurons at this developmental stage. Importantly, the relative positions of dendritic fields within the myotopic map remain constant. Such shifts relative to the commissures may be linked to the condensation of the nerve cord, which is underway at this stage.(D) Motor neurons with ventral internal muscle targets elaborate their dendrites in the ISN dendritic domain, which is located in the posterior part of the next anterior segment.(E) Motor neurons with dorsolateral internal targets put their dendrites (arrow) in the most-posterior part of the ISN dendritic domain, i.e., posterior to the dendritic domain, which represents dorsal internal muscles (arrowhead).(F) Motor neurons innervating ventral (ventral longitudinal 3–4 [VL3–VL4]; RP3) and dorsal (DA1; aCC) internal muscles elaborate their dendritic arbors in distinct regions of the ISN dendritic domain. Both motor neurons shown are bipolar and each has a second, smaller contralateral (with respect to the target muscle) dendritic arbor that mirrors the distribution of the ipsilateral dendrites.(G) Muscle DA2 is innervated by the RP2 (red) and a U/CQ neuron (magenta). The RP2 axonal trajectory through the posterior root of the ISN demarcates the boundary between ISN (magenta and red) and the SN (green) dendritic fields.(H) On the left are two examples of RP2 neurons filled in different 19-h-old embryos with Lucifer Yellow. As at the earlier stages shown in (G), most of the RP2 dendrites project anterior of the axon into the ISN dendritic domains representing dorsolateral and dorsal internal muscles. On the right is a Nomarski micrograph of a Lucifer Yellow-filled RP2 axon in the periphery at 19 h AEL. Swellings (arrowheads), likely neuromuscular junctions, are not specific to muscle DA2 (arrow), but are seen on all dorsolateral and dorsal muscles.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 and micrograph of muscle field in [H]): 10 μm.
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pbio.0000041-g002: Central Myotopic Representation of the Muscle FieldMotor neurons with external (A–C) and internal (D–G) muscle targets (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) Motor neurons with ventral and lateral external muscle targets at a similar location in the anteroposterior axis elaborate their dendritic arbors in a common region of the neuropile, within the SN dendritic domain, which represents external muscles.(B) Differences in muscle positions in the anteroposterior axis are reflected centrally by corresponding distinctions in the anteroposterior locations of motor neuron dendritic fields.(C) Muscle VT1 is innervated by a TN motor neuron (and frequently also by its contralateral homologue, partly shown). Dendrites of the VT1 motor neuron (arrow) coincide with those of the SBM motor neuron of the next anterior segment. Note that in (A) the position of the SBM dendritic field is shifted somewhat anteriorly relative to the commissural landmarks as compared to (B) and (C). We observe such shifts relative to the commissural landmarks in 13% (n = 52) of SBM (and other) motor neurons at this developmental stage. Importantly, the relative positions of dendritic fields within the myotopic map remain constant. Such shifts relative to the commissures may be linked to the condensation of the nerve cord, which is underway at this stage.(D) Motor neurons with ventral internal muscle targets elaborate their dendrites in the ISN dendritic domain, which is located in the posterior part of the next anterior segment.(E) Motor neurons with dorsolateral internal targets put their dendrites (arrow) in the most-posterior part of the ISN dendritic domain, i.e., posterior to the dendritic domain, which represents dorsal internal muscles (arrowhead).(F) Motor neurons innervating ventral (ventral longitudinal 3–4 [VL3–VL4]; RP3) and dorsal (DA1; aCC) internal muscles elaborate their dendritic arbors in distinct regions of the ISN dendritic domain. Both motor neurons shown are bipolar and each has a second, smaller contralateral (with respect to the target muscle) dendritic arbor that mirrors the distribution of the ipsilateral dendrites.(G) Muscle DA2 is innervated by the RP2 (red) and a U/CQ neuron (magenta). The RP2 axonal trajectory through the posterior root of the ISN demarcates the boundary between ISN (magenta and red) and the SN (green) dendritic fields.(H) On the left are two examples of RP2 neurons filled in different 19-h-old embryos with Lucifer Yellow. As at the earlier stages shown in (G), most of the RP2 dendrites project anterior of the axon into the ISN dendritic domains representing dorsolateral and dorsal internal muscles. On the right is a Nomarski micrograph of a Lucifer Yellow-filled RP2 axon in the periphery at 19 h AEL. Swellings (arrowheads), likely neuromuscular junctions, are not specific to muscle DA2 (arrow), but are seen on all dorsolateral and dorsal muscles.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 and micrograph of muscle field in [H]): 10 μm.

Mentions: Having established that there is a central representation of the muscle field, we examined the organisation of the motor neuron dendrites in greater detail. We looked first at the set of external muscles and their innervating (SN) motor neurons. Muscles of similar anteroposterior positions, such as the ventral acute muscle (VA3) and the segment border muscle (SBM), are innervated by motor neurons whose dendritic arbors lie in a common region of the neuropile (Figure 2A). Conversely, motor neurons supplying the anterior (lateral transverse 1–2 [LT1–LT2) versus the posterior (SBM) muscles have dendritic arbors that are correspondingly separated in the anteroposterior axis of the CNS (Figure 2B).


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)

Central Myotopic Representation of the Muscle FieldMotor neurons with external (A–C) and internal (D–G) muscle targets (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) Motor neurons with ventral and lateral external muscle targets at a similar location in the anteroposterior axis elaborate their dendritic arbors in a common region of the neuropile, within the SN dendritic domain, which represents external muscles.(B) Differences in muscle positions in the anteroposterior axis are reflected centrally by corresponding distinctions in the anteroposterior locations of motor neuron dendritic fields.(C) Muscle VT1 is innervated by a TN motor neuron (and frequently also by its contralateral homologue, partly shown). Dendrites of the VT1 motor neuron (arrow) coincide with those of the SBM motor neuron of the next anterior segment. Note that in (A) the position of the SBM dendritic field is shifted somewhat anteriorly relative to the commissural landmarks as compared to (B) and (C). We observe such shifts relative to the commissural landmarks in 13% (n = 52) of SBM (and other) motor neurons at this developmental stage. Importantly, the relative positions of dendritic fields within the myotopic map remain constant. Such shifts relative to the commissures may be linked to the condensation of the nerve cord, which is underway at this stage.(D) Motor neurons with ventral internal muscle targets elaborate their dendrites in the ISN dendritic domain, which is located in the posterior part of the next anterior segment.(E) Motor neurons with dorsolateral internal targets put their dendrites (arrow) in the most-posterior part of the ISN dendritic domain, i.e., posterior to the dendritic domain, which represents dorsal internal muscles (arrowhead).(F) Motor neurons innervating ventral (ventral longitudinal 3–4 [VL3–VL4]; RP3) and dorsal (DA1; aCC) internal muscles elaborate their dendritic arbors in distinct regions of the ISN dendritic domain. Both motor neurons shown are bipolar and each has a second, smaller contralateral (with respect to the target muscle) dendritic arbor that mirrors the distribution of the ipsilateral dendrites.(G) Muscle DA2 is innervated by the RP2 (red) and a U/CQ neuron (magenta). The RP2 axonal trajectory through the posterior root of the ISN demarcates the boundary between ISN (magenta and red) and the SN (green) dendritic fields.(H) On the left are two examples of RP2 neurons filled in different 19-h-old embryos with Lucifer Yellow. As at the earlier stages shown in (G), most of the RP2 dendrites project anterior of the axon into the ISN dendritic domains representing dorsolateral and dorsal internal muscles. On the right is a Nomarski micrograph of a Lucifer Yellow-filled RP2 axon in the periphery at 19 h AEL. Swellings (arrowheads), likely neuromuscular junctions, are not specific to muscle DA2 (arrow), but are seen on all dorsolateral and dorsal muscles.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 and micrograph of muscle field in [H]): 10 μm.
© Copyright Policy
Related In: Results  -  Collection

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

pbio.0000041-g002: Central Myotopic Representation of the Muscle FieldMotor neurons with external (A–C) and internal (D–G) muscle targets (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) Motor neurons with ventral and lateral external muscle targets at a similar location in the anteroposterior axis elaborate their dendritic arbors in a common region of the neuropile, within the SN dendritic domain, which represents external muscles.(B) Differences in muscle positions in the anteroposterior axis are reflected centrally by corresponding distinctions in the anteroposterior locations of motor neuron dendritic fields.(C) Muscle VT1 is innervated by a TN motor neuron (and frequently also by its contralateral homologue, partly shown). Dendrites of the VT1 motor neuron (arrow) coincide with those of the SBM motor neuron of the next anterior segment. Note that in (A) the position of the SBM dendritic field is shifted somewhat anteriorly relative to the commissural landmarks as compared to (B) and (C). We observe such shifts relative to the commissural landmarks in 13% (n = 52) of SBM (and other) motor neurons at this developmental stage. Importantly, the relative positions of dendritic fields within the myotopic map remain constant. Such shifts relative to the commissures may be linked to the condensation of the nerve cord, which is underway at this stage.(D) Motor neurons with ventral internal muscle targets elaborate their dendrites in the ISN dendritic domain, which is located in the posterior part of the next anterior segment.(E) Motor neurons with dorsolateral internal targets put their dendrites (arrow) in the most-posterior part of the ISN dendritic domain, i.e., posterior to the dendritic domain, which represents dorsal internal muscles (arrowhead).(F) Motor neurons innervating ventral (ventral longitudinal 3–4 [VL3–VL4]; RP3) and dorsal (DA1; aCC) internal muscles elaborate their dendritic arbors in distinct regions of the ISN dendritic domain. Both motor neurons shown are bipolar and each has a second, smaller contralateral (with respect to the target muscle) dendritic arbor that mirrors the distribution of the ipsilateral dendrites.(G) Muscle DA2 is innervated by the RP2 (red) and a U/CQ neuron (magenta). The RP2 axonal trajectory through the posterior root of the ISN demarcates the boundary between ISN (magenta and red) and the SN (green) dendritic fields.(H) On the left are two examples of RP2 neurons filled in different 19-h-old embryos with Lucifer Yellow. As at the earlier stages shown in (G), most of the RP2 dendrites project anterior of the axon into the ISN dendritic domains representing dorsolateral and dorsal internal muscles. On the right is a Nomarski micrograph of a Lucifer Yellow-filled RP2 axon in the periphery at 19 h AEL. Swellings (arrowheads), likely neuromuscular junctions, are not specific to muscle DA2 (arrow), but are seen on all dorsolateral and dorsal muscles.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 and micrograph of muscle field in [H]): 10 μm.
Mentions: Having established that there is a central representation of the muscle field, we examined the organisation of the motor neuron dendrites in greater detail. We looked first at the set of external muscles and their innervating (SN) motor neurons. Muscles of similar anteroposterior positions, such as the ventral acute muscle (VA3) and the segment border muscle (SBM), are innervated by motor neurons whose dendritic arbors lie in a common region of the neuropile (Figure 2A). Conversely, motor neurons supplying the anterior (lateral transverse 1–2 [LT1–LT2) versus the posterior (SBM) muscles have dendritic arbors that are correspondingly separated in the anteroposterior axis of the CNS (Figure 2B).

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