Development, Vol 107, Issue 3 553-573, Copyright © 1989 by Company of Biologists

JOURNAL ARTICLES

The development of the Xenopus retinofugal pathway: optic fibers join a pre-existing tract

SS Easter and JS Taylor
Department of Zoology, University of Edinburgh, United Kingdom.

The developing optic nerve and tract have received considerable attention in recent years, but the cellular and subcellular microenvironment of the growing axons has not been described. In the belief that such a description is essential (though certainly not sufficient) for an understanding of pathway formation, we have examined the normal development of the retinofugal projection of Xenopus laevis. Optic fibers were labeled anterogradely at the retina with horseradish peroxidase (HRP) or the carbocyanine dye, DiI, at stages 32 to postmetamorphosis. The brains were examined both as whole mounts and in sections, light- and electron-microscopically, with the emphasis on tracts associated with the route of the optic fibers. At stage 32, two ventral commissures were present, the anterior and postoptic. They were immediately subjacent to the pia. All tracts and even isolated axons were in similarly superficial locations. The first deep pathway (separated from the pia by cell nuclei) was seen at stage 46; it was a dorsal commissure, probably the posterior. The first retinal axons passed from the optic stalk into the ventral part of the diencephalon, where they coursed along the rostral edge of the postoptic commissure, and maintained this position, relative to the other fibers in the tract of the commissure, throughout the remainder of their contralateral trajectory. They reached the presumptive thalamic and tectal termination sites and arborized. Subsequent optic axons followed this same route, thus enlarging the optic pathway relative to the more slowly growing nonoptic part of the commissure and its tract. Electron microscopy revealed, as early as stage 35, specialized contacts between cellular processes in the neuropil. These contacts had the form of symmetric membranous thickenings; some were associated with vesicles and were presumed to be synapses. We conclude that the early forebrain and midbrain have only two ventral commissural pathways, and most axons that grow out after these pathways have formed add to them rather than establish new tracts. The optic axons travel a stereotyped pathway alongside a pre-existing tract associated with the postoptic commissure. The possibility that optic fiber outgrowth is normally influenced by pre-existing tracts is discussed in relation to recent experimental investigations of fiber growth from ectopic eyes.

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