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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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Territories of Initial Dendritic Elaboration Are Not Defined by Mutual Exclusion(A) Dendrites of DO3 (as well as DO4–DO5 and DT1) (green) motor neurons always project posterior to the region in which the dendritic arbors of the aCC and U/CQ motor neurons (red) form.(B and C) eve-expressing motor neurons (aCC, U/CQs, and RP2) in stage 13 (approximately 10.5-h-old) wild-type embryos (B) and those in which the aCC, RP2, and U/CQ neurons had been selectively ablated (C). In (C), all medial eve-expressing neurons have been ablated by this stage, and only one, possibly the U/CQ neuron (likely the LL1 motor neuron), is still present in several segments. U in (B) marks all U/CQ neurons as well as the aCC motor and the pCC and fpCC interneurons contained in this group; EL marks the lateral eve-expressing interneurons.(D) Dendritic arborisations of the DO3–DO4 motor neurons do not elaborate anteriorly into the territory vacated by ablated aCC and U/CQ neurons.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 in (A) and (D): 10 μm; in (B) and (C): 45 μm.
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pbio.0000041-g008: Territories of Initial Dendritic Elaboration Are Not Defined by Mutual Exclusion(A) Dendrites of DO3 (as well as DO4–DO5 and DT1) (green) motor neurons always project posterior to the region in which the dendritic arbors of the aCC and U/CQ motor neurons (red) form.(B and C) eve-expressing motor neurons (aCC, U/CQs, and RP2) in stage 13 (approximately 10.5-h-old) wild-type embryos (B) and those in which the aCC, RP2, and U/CQ neurons had been selectively ablated (C). In (C), all medial eve-expressing neurons have been ablated by this stage, and only one, possibly the U/CQ neuron (likely the LL1 motor neuron), is still present in several segments. U in (B) marks all U/CQ neurons as well as the aCC motor and the pCC and fpCC interneurons contained in this group; EL marks the lateral eve-expressing interneurons.(D) Dendritic arborisations of the DO3–DO4 motor neurons do not elaborate anteriorly into the territory vacated by ablated aCC and U/CQ neurons.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 in (A) and (D): 10 μm; in (B) and (C): 45 μm.

Mentions: One likely explanation for the division of dendrites into separate domains is that there is a process of mutual exclusion between the arborisations of neighbouring cells. Such a process of dendritic ‘tiling' has so far only been documented between particular classes of sensory neurons (Wassle et al. 1981; Grueber et al. 2002, 2003), but could also occur in the motor system. We tested the idea of tiling by considering two groups of motor neurons whose axons have a common trajectory, but whose dendritic fields form in adjacent territories. The DO3–DO5 and DT1 motor neurons project their dendrites posteriorly, and at their most-anterior point, these dendrites meet the axons and dendrites of the anterior corner cell (aCC) and U/CQ neurons (Figure 8A). To show whether the aCC and U/CQ axons and/or dendrites inhibit the growth of DO3–DO5 and DT1 dendrites anteriorly, we selectively ablated these neurons (as well as RP2 and the posterior corner cell [pCC] interneuron) (Fujioka et al. 2003). Using anti-Even-skipped (Eve) staining as a marker for aCC, RP2, and U/CQs (there are an additional two medially located eve-expressing interneurons, pCC and friend of pCC [fpCC] [Goodman and Doe 1993; Bossing et al. 1996]), we find that we can efficiently ablate these neurons before they form dendrites (at approximately 11 h AEL): on average, by 10.5 h AEL all but 0.6 (Figure 8B–8C) and by 12 h AEL all but 0.06 of the seven medially located eve-expressing neurons have been ablated per half-neuromere (n = ≥60). In no instance did we observe a concomitant anterior expansion of the DO3–DO5 and DT1 motor neuron dendrites into the regions vacated by the aCC and U/CQ dendrites (n = 13; Figure 8D). We conclude that, at least in this instance, the initial dendritic territory of one set of motor neurons (DO3–DO5 and DT1) is not defined by a process of tiling, in which they are excluded by neighbouring (aCC and U/CQ) dendritic arbors. However, it is possible that the elaboration of motor neuron dendritic arbors during later developmental stages may involve interactions between neighbouring dendritic territories, activity-dependent processes, or both.


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)

Territories of Initial Dendritic Elaboration Are Not Defined by Mutual Exclusion(A) Dendrites of DO3 (as well as DO4–DO5 and DT1) (green) motor neurons always project posterior to the region in which the dendritic arbors of the aCC and U/CQ motor neurons (red) form.(B and C) eve-expressing motor neurons (aCC, U/CQs, and RP2) in stage 13 (approximately 10.5-h-old) wild-type embryos (B) and those in which the aCC, RP2, and U/CQ neurons had been selectively ablated (C). In (C), all medial eve-expressing neurons have been ablated by this stage, and only one, possibly the U/CQ neuron (likely the LL1 motor neuron), is still present in several segments. U in (B) marks all U/CQ neurons as well as the aCC motor and the pCC and fpCC interneurons contained in this group; EL marks the lateral eve-expressing interneurons.(D) Dendritic arborisations of the DO3–DO4 motor neurons do not elaborate anteriorly into the territory vacated by ablated aCC and U/CQ neurons.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 in (A) and (D): 10 μm; in (B) and (C): 45 μm.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC261881&req=5

pbio.0000041-g008: Territories of Initial Dendritic Elaboration Are Not Defined by Mutual Exclusion(A) Dendrites of DO3 (as well as DO4–DO5 and DT1) (green) motor neurons always project posterior to the region in which the dendritic arbors of the aCC and U/CQ motor neurons (red) form.(B and C) eve-expressing motor neurons (aCC, U/CQs, and RP2) in stage 13 (approximately 10.5-h-old) wild-type embryos (B) and those in which the aCC, RP2, and U/CQ neurons had been selectively ablated (C). In (C), all medial eve-expressing neurons have been ablated by this stage, and only one, possibly the U/CQ neuron (likely the LL1 motor neuron), is still present in several segments. U in (B) marks all U/CQ neurons as well as the aCC motor and the pCC and fpCC interneurons contained in this group; EL marks the lateral eve-expressing interneurons.(D) Dendritic arborisations of the DO3–DO4 motor neurons do not elaborate anteriorly into the territory vacated by ablated aCC and U/CQ neurons.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 in (A) and (D): 10 μm; in (B) and (C): 45 μm.
Mentions: One likely explanation for the division of dendrites into separate domains is that there is a process of mutual exclusion between the arborisations of neighbouring cells. Such a process of dendritic ‘tiling' has so far only been documented between particular classes of sensory neurons (Wassle et al. 1981; Grueber et al. 2002, 2003), but could also occur in the motor system. We tested the idea of tiling by considering two groups of motor neurons whose axons have a common trajectory, but whose dendritic fields form in adjacent territories. The DO3–DO5 and DT1 motor neurons project their dendrites posteriorly, and at their most-anterior point, these dendrites meet the axons and dendrites of the anterior corner cell (aCC) and U/CQ neurons (Figure 8A). To show whether the aCC and U/CQ axons and/or dendrites inhibit the growth of DO3–DO5 and DT1 dendrites anteriorly, we selectively ablated these neurons (as well as RP2 and the posterior corner cell [pCC] interneuron) (Fujioka et al. 2003). Using anti-Even-skipped (Eve) staining as a marker for aCC, RP2, and U/CQs (there are an additional two medially located eve-expressing interneurons, pCC and friend of pCC [fpCC] [Goodman and Doe 1993; Bossing et al. 1996]), we find that we can efficiently ablate these neurons before they form dendrites (at approximately 11 h AEL): on average, by 10.5 h AEL all but 0.6 (Figure 8B–8C) and by 12 h AEL all but 0.06 of the seven medially located eve-expressing neurons have been ablated per half-neuromere (n = ≥60). In no instance did we observe a concomitant anterior expansion of the DO3–DO5 and DT1 motor neuron dendrites into the regions vacated by the aCC and U/CQ dendrites (n = 13; Figure 8D). We conclude that, at least in this instance, the initial dendritic territory of one set of motor neurons (DO3–DO5 and DT1) is not defined by a process of tiling, in which they are excluded by neighbouring (aCC and U/CQ) dendritic arbors. However, it is possible that the elaboration of motor neuron dendritic arbors during later developmental stages may involve interactions between neighbouring dendritic territories, activity-dependent processes, or both.

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