Skip to main content
Log in

Migration of neurons between ganglia in the metamorphosing insect nervous system

  • Original Article
  • Published:
Roux's archives of developmental biology Aims and scope Submit manuscript

Abstract

Migration of neurons over long distances occurs during the development of the adult central nervous system of the sphinx moth Manduca sexta, and the turnip moth Agrotis segetum. From each of the suboesophageal and three thoracic ganglia, bilaterally-paired clusters of immature neurons and associated glial cells migrate posteriorly along the interganglionic connectives, to enter the next posterior ganglion. The first sign of migration is observed at the onset of metamorphosis, when posterio-lateral cell clusters gradually separate from the cortex of neuronal cell bodies and enter the connectives. Cell clusters migrate posteriorly along the connective to reach the next ganglion over the first three days (approximately 15%) of pupal development. During migration, each cell cluster is completely enveloped by a single giant glial cell spanning the entire length of the connective between two adjacent ganglia. Intracellular cobalt staining reveals that each migrating neuron has an ovoid cell body and an extremely long leading process which extends as far as the next posterior ganglion; this is not a common morphology for migrating neurons that have been described in vertebrates. Once the cells arrive at the anterior cortex of the next ganglion, they rapidly intermingle with the surrounding neurons and so we were unable to determine the fate of the migrating neurons at their final location.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bacon JP, Altman JS (1977) A silver intensification method for cobalt-filled neurones in whole mount preparations. Brain Res 138:359–363

    Google Scholar 

  • Booker R, Truman JW (1987a) Postembryonic neurogenesis in the CNS of the tobacco hornworm, Manduca sexta. I. Neuroblast arrays and the fate of their progeny during metamorphosis. J Comp Neurol 255:548–559

    Google Scholar 

  • Booker R, Truman JW (1987b) Pstembryonic neurogenesis in the CNS of the tobacco hornworm, Manduca sexta. II. Hormonal control of imaginal nest cell degeneration and differentiation during metamorphosis. J Neurosci 7:4107–4114

    Google Scholar 

  • Cantera R (1993) Glial cells in adult and developing prothoracic ganglion of the hawk moth Manduca sexta. Cell Tissue Res 272:93–108

    Google Scholar 

  • Copenhaver, FP, Taghert PH (1989a) Development of the enteric nervous system in the moth. II. Stereotyped cell migration precedes the differentiation of embryonic neurons. Dev Biol 131: 85–101

    Google Scholar 

  • Copenhaver FP, Taghert PH (1989b) Development of the enteric nervous system in the moth. I Diversity of cell types and the embryonic expression of FMRFamide-related neuropeptides. Dev Biol 131:70–84

    Google Scholar 

  • Fishman RB, Hatten ME (1993) Multiple receptor systems promote CNS neural migration. J Neurosci 13:3485–3495

    Google Scholar 

  • Gray GE, Sanes JR (1991) Migratory paths and phenotypic choices of clonally related cells in the avian optic tectum. Neuron 6: 211–225

    Google Scholar 

  • Gregory WA, Edmondson JC, Hatten ME, Mason CA (1988) Cytology and neuron glial apposition of migrating cerebellar granule cells in vitro. J Neurosci 8:1728–1738

    Google Scholar 

  • Hatten ME (1990) Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain. Trends Neurosci 13: 179–184

    Google Scholar 

  • Hatten ME (1993) The role of migration in central nervous system neuronal development. Cuff Opin Neurobiol 3:38–44

    Google Scholar 

  • Klämbt C, Jacobs JR, Goodman CS (1991) The midline of the Drosophila central nervous system: A model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell 64:801–815

    Google Scholar 

  • Klämbt C, Glazer L, Shilo B-Z (1992) breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev 6:1668–1678

    Google Scholar 

  • Levine RB (1984) Changes in neuronal circuits during insect metamorphosis. J Exp Biol 112:27–44

    Google Scholar 

  • Manser J, Wood WB (1990) Mutations affecting embryonic cell migrations in Caenorhabditis elegans. Dev Genet 11:49–64

    Google Scholar 

  • Rakic P (1988) Specification of cerebral cortical areas. Science 241:170–176

    Google Scholar 

  • Rakic P (1990) Principles of neural cell migration. Experientia 46: 882–891

    Google Scholar 

  • Rakic P, Cameron RS, Komuro H (1994) Recognition, adhesion, transmembrane signaling and cell motility in guided neuronal migration. Curr Opin Neurobiol 4:63–69

    Google Scholar 

  • Sloman IS, Reynolds SE (1993) Inhibition of ecdysteroid secretion from prothoracic glands in vitro by destruxins — cyclic depsipeptide toxins from the insect pathogenic fungus Metarhizium anisopliae. Insect Biochem Mol Biol 23:43–46

    Google Scholar 

  • Wadsworth WG, Hedgecock EM (1992) Guidance of neuroblast migrations and axonal projections in Caenorhabditis elegans. Curr Opin Neurobiol 2:36–41

    Google Scholar 

  • Witten JL, Truman JW (1991) The regulation of transmitter expression in postembryonic lineages in the moth Manduca sexta. I. Transmitter identification and developmental acquisition of expression. J Neurosci 11:1980–1989

    Google Scholar 

  • Yamamori T, Fukada K, Aebersold R, Korshing S, Fann M-J, Patterson PH (1989) The cholinergic neuronal differentiation factor from heart cells is identical to leukemia inhibitory factor. Science 246:1412–1416

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cantera, R., Thompson, K.S.J., Hallberg, E. et al. Migration of neurons between ganglia in the metamorphosing insect nervous system. Roux's Arch Dev Biol 205, 10–20 (1995). https://doi.org/10.1007/BF00188839

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00188839

Key words

Navigation