Morphological differentiation of the embryonic peripheral neurons in Drosophila (original) (raw)
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Summary
The stereotyped segmental and dorso-ventral organization of the peripheral nervous system (PNS) of Drosophila embryos allows the identification of all the neurons in the body wall. Distinct classes of neurons are distinguishable according to their location, the targets they innervate, the particular shape of their dendrites and their cell size. Those neurons innervating external sensory structures (es) and chordotonal organs (ch) have single dendrites and have been previously described (Ghysen et al. 1986; Dambly-Chaudiere and Ghysen 1986; Campos-Ortega and Hartenstein 1985). We describe here the identity and morphological features of three other classes of neurons in the body segments which have multiple dendrites (md neurons): 1) neurons that give rise to elaborate dendritic arborisations (da neurons); 2) neurons that have bipolar dendrites (bd neurons); 3) neurons that arborize around particular tracheal branches (td neurons). The thoracic hemisegment (T2 and T3) contains 13 da, one bd, one td, 21 es and four ch neurons; the abdominal hemisegment (A1 to A7) contains 14 da, three bd, three td, 15 es and eight ch neurons. The arrangement of the segmented peripheral neurons is highly invariant and provides a favorable assay system for the genetic analysis of neurodevelopment.
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References
- Bate CM (1976) Pioneer neurons in an insect embryo. Nature (Lond) 260:54–56
Google Scholar - Bate CM (1978) Development of sensory systems in arthropods. In: Jacobson M (ed) Handbook of sensory physiology, vol. IX. Springer, Berlin Heidelberg New York, pp 1–53
Google Scholar - Bentley D, Caudy M (1983) Pioneer axons lose directed growth after selective killing of guidepost cells. Nature (Lond) 304:62–65
Google Scholar - Berlot J, Goodman CS (1984) Guidance of peripheral pioneer neurons in grasshopper: Adhesive hierarchy of epithelial and neuronal surfaces. Science 223:493–496
Google Scholar - Blackshaw SE (1981) Morphology and distribution of touch cell terminals in the skin of the leech. J Physiol 320:219–228
PubMed Google Scholar - Campos-Ortega JA, Hartenstein V (1985) The embryonic development of Drosophila melanogaster. Springer, Berlin Heidelberg New York Tokyo
Google Scholar - Caudy M, Bentley D (1986) Pioneer growth cone morphologies reveal proximal increases in substrate affinity within leg segments of grasshopper embryos. J Neurosci 6:364–379
PubMed Google Scholar - Dambly-Chaudière C, Ghysen A (1986) The pattern of sense organs in Drosophila embryos and larvae. Roux's Arch Dev Biol 195:222–228
Google Scholar - Dethier VG (1963) The Physiology of Insect Senses. Methuen's monographs on biological subjects. John Wiley & Sons Inc., New York
Google Scholar - Escherich K (1902) Zur Entwicklung des Nervensystems der Musciden, mit besonderer Berücksichtigung des sog. Mittelstrangs. Z Wiss Zool 71:525–549
Google Scholar - Ghysen A, Dambly-Chaudière C, Aceves E, Jan LY, Jan YN (1986) Sensory neurons and peripheral pathways in Drosophila embryos. Roux's Arch Dev Biol 195:281–289
Google Scholar - Hartenstein V, Campos-Ortega JA (1986) The peripheral nervous system of mutants of early neurogenesis in Drosophila melanogaster. Roux's Arch Dev Biol 195:210–221
Google Scholar - Hertweck H (1931) Anatomie und Variabilität des Nervensystems und der Sinnesorgane von Drosophila melanogaster (Meigen). Z Wiss Zool 139:559–663
Google Scholar - Jan LY, Jan YN (1982) Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and in grasshopper embryos. Proc Natl Acad Sci (USA) 72:2700–2704
Google Scholar - Jan YN, Bodmer R, Ghysen A, Dambly-Chaudiere Ch, Jan L (1987) Mutations affecting the peripheral nervous system in Drosophila embryos. J Cellular Biochem Proceedings of the UCLA Symposia “Molecular Entomology” (in press)
- Jürgens G, Wieschaus E, Nüsslein-Volhard C, Kluding H (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. II. Zygotic loci on the third chromosome. Wilhelm Roux's Arch 193:283–295
Google Scholar - Karr TL, Ali Z, Drees B, Kornberg T (1985) The engrailed locus of D. melanogaster provides an essential zygotic function in precellular embryos. Cell 43:591–601
Article PubMed Google Scholar - Kramer AP, Kuwada JY (1983) Formation of the receptive fields of leech mechanosensory neurons during embryonic development. J Neurosci 3:2474–2486
PubMed Google Scholar - Lawrence PA (1975) The structure and properties of a compartment border: the intersegmental boundary in Oncopeltus. In: Cell patterning. Ciba Symposium 29:3–23
Google Scholar - Nardi JB (1983) Neuronal pathfinding in developing wings of the moth Manduca sexta. Dev Biol 95:163–174
PubMed Google Scholar - Nüsslein-Volhard C, Wieschaus E, Kluding H (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the second chromosome. Wilhelm Roux's Arch 193:267–282
Google Scholar - Taghert PH, Bastiani J, Ho RK, Goodman CS (1982) Guidance of pioneer growth cones: Filapodial contacts and coupling revealed with an antibody to Lucifer Yellow. Dev Biol 94:391–399
PubMed Google Scholar - Wieschaus E, Nüsslein-Volhard C, Jürgens G (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. III. Zygotic loci on the X-chromosome and fourth chromosome. Wilhelm Roux's Arch 193:296–307
Google Scholar - Wigglesworth VB (1938) The absorption of fluid from the tracheal system of mosquito larvae at hatching and molting. J Exp Biol 15:248–254
Google Scholar - Wigglesworth VB (1953) The origin of sensory neurones in an insect, Rhodnius prolixus (Hemiptera). Quart J Micro Sci 94:93–112
Google Scholar - Zawarzin A (1912a) Histologische Studien über Insekten. II. Das sensible Nervensystem der Aeschnalarven. Z Wiss Zool 100:245–286
Google Scholar - Zawarzin A (1912b) Histologische Studien über Insekten. III. Über das sensible Nervensystem der Larven von Melolontha vulgaris. Z Wiss Zool 100:447–457
Google Scholar
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- Howard Hughes Medical Institute and Department of Physiology and Biochemistry, University of California, 94143, San Francisco, CA, USA
Rolf Bodmer & Yuh Nung Jan
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- Rolf Bodmer
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Bodmer, R., Jan, Y.N. Morphological differentiation of the embryonic peripheral neurons in Drosophila.Roux's Arch Dev Biol 196, 69–77 (1987). https://doi.org/10.1007/BF00402027
- Received: 06 June 1986
- Accepted: 14 August 1986
- Issue Date: February 1987
- DOI: https://doi.org/10.1007/BF00402027