Development of a glia-rich axon-sorting in the olfactory pathway of the moth Manduca sexta

Wolfgang Rössler, Lynne A. Oland, Mark R. Higgins, John G. Hildebrand, Leslie P. Tolbert

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Abstract

Olfactory receptor cells (ORCs) of a particular odor tuning are dispersed in the olfactory epithelium, but their axons converge on distinct glomeruli in primary olfactory centers. As a consequence, axon associations must change to bring axons of ORCs with the same odor specificity together. Studies in Manduca sexta have indicated that just before they enter the antennal lobe (AL), ORC axons undergo extreme reorganization, finally entering the AL in fascicles destined for subsets of glomeruli. This axon- sorting zone is heavily populated by glial cells, and ORC axon growth cones often are in close physical contact with the glia. In moths rendered gila deficient, ORC axons fail to fasciculate in this region. Using propidium iodide to label nuclei and 5-bromo-2'-deoxyuridine to monitor proliferation, we found that the gila in the sorting zone arise from the AL, appearing shortly after the first ORC axons arrive. Experimental removal of some or all of the sensory innervation revealed that proliferation of sorting-zone glia is triggered by ORC axons. A second set of glia arises in the antenna and migrates along the antennal nerve toward the brain, populating the nerve after the establishment of the sorting zone. Development of this type of glial cell is independent of contact of the ORC axons with their central targets. We conclude that the sorting zone arises from CNS glia in response to ingrowth of ORC axons, and a critical number of glia must be present in the sorting zone for axons to correctly establish new neighbor-neighbor associations.

Original languageEnglish (US)
Pages (from-to)9865-9877
Number of pages13
JournalJournal of Neuroscience
Volume19
Issue number22
StatePublished - Nov 15 1999

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Keywords

  • Antennal lobe
  • Cell birth
  • Cell-cell interactions
  • Glial cells
  • Olfactory glomeruli
  • Sensory mapping

ASJC Scopus subject areas

  • Neuroscience(all)

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