Abstract
During development of the nervous system, growth cones navigate very precisely to their appropriate, often distant, targets. In insects, the task of establishing the earliest pathways is accomplished by a small number of neurons, termed pioneers. These neurons have axons that lay down an early scaffold, which provides a substrate for many later-developing axons. Here we show that a similar type of cell exists in the embryonic vertebrate brain. Using light- and electron-microscopic techniques we have examined the formation of one of the earliest tracts in the zebrafish brain. We find that it is pioneered at a precise time by the growth cone of a single neuron present in a predictable location. These observations show a fundamental similarity in the establishment of axonal pathways in the central nervous systems of both invertebrates and vertebrates.
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- Bastiani M. J., Goodman C. S. Neuronal growth cones: specific interactions mediated by filopodial insertion and induction of coated vesicles. Proc Natl Acad Sci U S A. 1984 Mar;81(6):1849–1853. doi: 10.1073/pnas.81.6.1849. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bate C. M. Pioneer neurones in an insect embryo. Nature. 1976 Mar 4;260(5546):54–56. doi: 10.1038/260054a0. [DOI] [PubMed] [Google Scholar]
- Bentley D., Keshishian H. Pathfinding by peripheral pioneer neurons in grasshoppers. Science. 1982 Dec 10;218(4577):1082–1088. doi: 10.1126/science.218.4577.1082. [DOI] [PubMed] [Google Scholar]
- Chitnis A. B., Kuwada J. Y. Axonogenesis in the brain of zebrafish embryos. J Neurosci. 1990 Jun;10(6):1892–1905. doi: 10.1523/JNEUROSCI.10-06-01892.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Easter S. S., Jr, Purves D., Rakic P., Spitzer N. C. The changing view of neural specificity. Science. 1985 Nov 1;230(4725):507–511. doi: 10.1126/science.4048944. [DOI] [PubMed] [Google Scholar]
- Easter S. S., Jr, Taylor J. S. The development of the Xenopus retinofugal pathway: optic fibers join a pre-existing tract. Development. 1989 Nov;107(3):553–573. doi: 10.1242/dev.107.3.553. [DOI] [PubMed] [Google Scholar]
- Eisen J. S., Myers P. Z., Westerfield M. Pathway selection by growth cones of identified motoneurones in live zebra fish embryos. Nature. 1986 Mar 20;320(6059):269–271. doi: 10.1038/320269a0. [DOI] [PubMed] [Google Scholar]
- Eisen J. S., Pike S. H., Debu B. The growth cones of identified motoneurons in embryonic zebrafish select appropriate pathways in the absence of specific cellular interactions. Neuron. 1989 Jan;2(1):1097–1104. doi: 10.1016/0896-6273(89)90234-1. [DOI] [PubMed] [Google Scholar]
- Harrelson A. L., Goodman C. S. Growth cone guidance in insects: fasciclin II is a member of the immunoglobulin superfamily. Science. 1988 Nov 4;242(4879):700–708. doi: 10.1126/science.3187519. [DOI] [PubMed] [Google Scholar]
- Ho R. K., Goodman C. S. Peripheral pathways are pioneered by an array of central and peripheral neurones in grasshopper embryos. Nature. 1982 Jun 3;297(5865):404–406. doi: 10.1038/297404a0. [DOI] [PubMed] [Google Scholar]
- Holley J. A., Silver J. Growth pattern of pioneering chick spinal cord axons. Dev Biol. 1987 Oct;123(2):375–388. doi: 10.1016/0012-1606(87)90396-4. [DOI] [PubMed] [Google Scholar]
- Honig M. G., Hume R. I. Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures. J Cell Biol. 1986 Jul;103(1):171–187. doi: 10.1083/jcb.103.1.171. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Keshishian H., Bentley D. Embryogenesis of peripheral nerve pathways in grasshopper legs. III. Development without pioneer neurons. Dev Biol. 1983 Mar;96(1):116–124. doi: 10.1016/0012-1606(83)90316-0. [DOI] [PubMed] [Google Scholar]
- Klose M., Bentley D. Transient pioneer neurons are essential for formation of an embryonic peripheral nerve. Science. 1989 Sep 1;245(4921):982–984. doi: 10.1126/science.2772651. [DOI] [PubMed] [Google Scholar]
- Kuwada J. Y. Cell recognition by neuronal growth cones in a simple vertebrate embryo. Science. 1986 Aug 15;233(4765):740–746. doi: 10.1126/science.3738507. [DOI] [PubMed] [Google Scholar]
- Letourneau P. C., Madsen A. M., Palm S. L., Furcht L. T. Immunoreactivity for laminin in the developing ventral longitudinal pathway of the brain. Dev Biol. 1988 Jan;125(1):135–144. doi: 10.1016/0012-1606(88)90066-8. [DOI] [PubMed] [Google Scholar]
- McConnell S. K., Ghosh A., Shatz C. J. Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science. 1989 Sep 1;245(4921):978–982. doi: 10.1126/science.2475909. [DOI] [PubMed] [Google Scholar]
- Mendelson B. Development of reticulospinal neurons of the zebrafish. II. Early axonal outgrowth and cell body position. J Comp Neurol. 1986 Sep 8;251(2):172–184. doi: 10.1002/cne.902510204. [DOI] [PubMed] [Google Scholar]
- Myers P. Z., Eisen J. S., Westerfield M. Development and axonal outgrowth of identified motoneurons in the zebrafish. J Neurosci. 1986 Aug;6(8):2278–2289. doi: 10.1523/JNEUROSCI.06-08-02278.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nordlander R. H. Developing descending neurons of the early Xenopus tail spinal cord in the caudal spinal cord of early Xenopus. J Comp Neurol. 1984 Sep 1;228(1):117–128. doi: 10.1002/cne.902280111. [DOI] [PubMed] [Google Scholar]
- Patterson P. H. On the importance of being inhibited, or saying no to growth cones. Neuron. 1988 Jun;1(4):263–267. doi: 10.1016/0896-6273(88)90074-8. [DOI] [PubMed] [Google Scholar]
- Pike S. H., Eisen J. S. Identified primary motoneurons in embryonic zebrafish select appropriate pathways in the absence of other primary motoneurons. J Neurosci. 1990 Jan;10(1):44–49. doi: 10.1523/JNEUROSCI.10-01-00044.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silver J., Rutishauser U. Guidance of optic axons in vivo by a preformed adhesive pathway on neuroepithelial endfeet. Dev Biol. 1984 Dec;106(2):485–499. doi: 10.1016/0012-1606(84)90248-3. [DOI] [PubMed] [Google Scholar]
- Singer M., Nordlander R. H., Egar M. Axonal guidance during embryogenesis and regeneration in the spinal cord of the newt: the blueprint hypothesis of neuronal pathway patterning. J Comp Neurol. 1979 May 1;185(1):1–21. doi: 10.1002/cne.901850102. [DOI] [PubMed] [Google Scholar]
- Stainier D. Y., Gilbert W. Pioneer neurons in the mouse trigeminal sensory system. Proc Natl Acad Sci U S A. 1990 Feb;87(3):923–927. doi: 10.1073/pnas.87.3.923. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tosney K. W., Landmesser L. T. Growth cone morphology and trajectory in the lumbosacral region of the chick embryo. J Neurosci. 1985 Sep;5(9):2345–2358. doi: 10.1523/JNEUROSCI.05-09-02345.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilson S. W., Ross L. S., Parrett T., Easter S. S., Jr The development of a simple scaffold of axon tracts in the brain of the embryonic zebrafish, Brachydanio rerio. Development. 1990 Jan;108(1):121–145. doi: 10.1242/dev.108.1.121. [DOI] [PubMed] [Google Scholar]
- Yaginuma H., Shiga T., Homma S., Ishihara R., Oppenheim R. W. Identification of early developing axon projections from spinal interneurons in the chick embryo with a neuron specific beta-tubulin antibody: evidence for a new 'pioneer' pathway in the spinal cord. Development. 1990 Apr;108(4):705–716. doi: 10.1242/dev.108.4.705. [DOI] [PubMed] [Google Scholar]