Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2003 Nov;1(2):E41.
doi: 10.1371/journal.pbio.0000041. Epub 2003 Nov 17.

Embryonic origins of a motor system: motor dendrites form a myotopic map in Drosophila

Matthias Landgraf  1 , Victoria Jeffrey, Miki Fujioka, James B Jaynes, Michael Bate
Affiliations

Embryonic origins of a motor system: motor dendrites form a myotopic map in Drosophila

Matthias Landgraf et al. PLoS Biol. 2003 Nov.

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.

PubMed Disclaimer

Conflict of interest statement

The authors have declared that no conflicts of interest exist.

Figures

Figure 1
Figure 1. 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.
Figure 2
Figure 2. Central Myotopic Representation of the Muscle Field
Motor 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.
Figure 3
Figure 3. Motor Neuron Dendrites Form a Myotopic Map of the Muscle Field
Collage 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.
Figure 4
Figure 4. Parasegmental Organisation of the Motor System
(A) Distribution of motor neuron dendritic arbors relative to the domains of en expression. Neurons expressing the en gene were visualised (blue) using en-GAL4;UAS-CD8-GFP. ISN motor neuron dendrites (red) elaborate in the En domain (blue) of the neuromere, whereas SN motor neuron dendrites (green) form in the anterior half of the next posterior segment (asterisks indicate the segment borders). Thus, the motor system appears to be parasegmental in nature. The diagrams to the right indicate which motor neurons were labelled. (B–H) ISN motor neurons (red) with dorsal internal and SN motor neurons (green) with lateral external muscle targets were retrogradely labelled in 15-h-old wild-type embryos (B) and those mutant for different segment polarity genes (C–H). (C) to (H) should be compared with the wild-type control in (B). As far as could be ascertained, similar sets of motor neurons were labelled in the wild-type (B) and mutants (C–H). The neuropile, visualised with anti-HRP, is shown in blue (except for [F]). In all mutant embryos, with the exception of Df(gsb) (H), ISN and SN motor neurons have separate nerve roots and dendritic fields, as in the wild-type. As (H) shows, in Df(gsb) mutant embryos, ISN and SN nerve roots are frequently fused, yet the respective dendritic fields (arrows) do not appear to intermingle. Anterior is left and dorsal is up. Symbols and abbreviations: triangles, ventral midline; AC, anterior commissure; PC, posterior commissure (RP2 cell bodies, the most posterior of the ISN motor neurons, are indicated in [C] and [E]); asterisks, dorsoventral channels (landmarks for the segment borders). Scale bar (not applicable to diagrams of CNS and muscle field): 10 μm.
Figure 5
Figure 5. The Myotopic Map Forms by an Active Process of Dendritic Growth and Arborisation
ISN 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.
Figure 6
Figure 6. The Myotopic Map Forms Independently of Target Muscles
ISN motor neurons (red) with internal and SN motor neurons (green) with external muscle targets in a 15-h-old wild-type (A) and in an embryo, in which muscle formation had been suppressed by targeted expression of an activated form (intracellular domain) of Notch (24B-GAL4; UAS-Notch*) (B). In such muscleless embryos, the main nerve trunks (ISN and SN) still form and project into the periphery along distinctive paths. Thus, motor neurons whose axons project through these nerves can be retrogradely labelled. The neuropile, visualised with anti-HRP, is shown in blue. ISN and SN motor neuron dendritic domains show a normal separation despite absence of target muscles. Note that the ISN (red) and SN (green) dendritic arbors in (B) appear to be in closer proximity than those shown in (A). This is because in (B) the RP2 neuron (indicated) is labelled, which is the most posterior of the ISN motor neurons and therefore closest to the SN dendritic domain. See also Figure 2G, where RP2 and its dendrites are shown relative to the most posterior of the SN motor neuron (SBM) dendritic fields. 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.
Figure 7
Figure 7. Glial Cell Differentiation Is Not Required for Neuropile Subdivision
ISN (red) and SN (green) motor neurons labelled in 15-h-old wild-type (A and C) and gcm mutant (B and D) embryos. The neuropile, visualised with anti-HRP, is shown in blue. (A and B) Motor neurons innervating ventral (VL3–VL4, RP3) internal (red) and external (green) muscles of a segment elaborate their dendrites in separate regions of the neuropile on either side of the segment border (asterisks). This is accentuated when neuromeres separate in gcm mutant embryos (B). (C and D) The DT1 motor neuron (red) is the only ISN motor neuron whose dendrites branch in the SN dendritic domain (green). This dendritic projection pattern is maintained in gcm mutant embryos (D). An SN VUM efferent neuron has also been labelled. 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.
Figure 8
Figure 8. 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.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Atwood HL, Govind CK, Wu C-F. Neuromuscular junction ultrastructure of ventral abdominal muscles in Drosophila larvae. J Neurobiol. 1993;24:1008–1024. - PubMed
    1. Baines RA, Bate M. Electrophysiological development of central neurons in the Drosophila embryo. J Neurosci. 1998;18:4673–4683. - PMC - PubMed
    1. Baines RA, Robinson SG, Fujioka M, Jaynes JB, Bate M. Postsynaptic expression of tetanus toxin light chain blocks synaptogenesis in Drosophila. Curr Biol. 1999;9:1267–1270. - PMC - PubMed
    1. Baines RA, Uhler JP, Thompson A, Sweeney ST, Bate M. Altered electrical properties in Drosophila neurons developing without synaptic transmission. J Neurosci. 2001;21:1523–1531. - PMC - PubMed
    1. Baines RA, Seugnet L, Thompson A, Salvaterra PM, Bate M. Regulation of synaptic connectivity: Levels of fasciclin II influence synaptic growth in the Drosophila CNS. J Neurosci. 2002;22:6587–6595. - PMC - PubMed

Publication types

MeSH terms

Substances

LinkOut - more resources