The organization of the fibers in the optic nerve of normal and tectum-less Rana pipiens

Abstract

We have examined the detailed order of retinal ganglion cell (RGC) axons in the optic nerve and tract of the frog, Rana pipiens. By using horseradish peroxidase (HRP) injections into small regions of the retina, the tectum, and at various points along the visual pathway, it has been possible to follow labelled fibers throughout their course in the nerve and tract. Several surprising features in the order of fibers in the visual pathway were discovered in our investigation. The fascicular pattern of RGC axons in the retina is similar to that described in other vertebrates; however, immediately central to their entry into the optic nerve head, approximately half of the fibers from the nasal or temporal retina cross over to the opposite side of the nerve. Although the axons from the dorsal and ventral regions of the retina generally remain in the dorsal and ventral regions of the nerve, some fiber crossing occurs in those axons as well. The result of this seemingly complex rearrangement is that the optic nerve of Rana pipiens contains mirror symmetric representations of the retinal surface on either side of the dorsal ventral midline of the nerve. The fibers in each of these representations are arranged as semicircles representing the full circumference of the retina. This precise fiber order is preserved in the nerve until immediately peripheral to the optic chiasm, at which point age-related axons from both sides of the nerve bundle together. Consequently, when a small pellet of HRP is placed in the chiasmic region of the nerve, an annulus of retinal ganglion cells and a corresponding annulus of RGC terminals in the tectum are labelled. As the age-related bundles of fibers emerge from the chiasm they split to form a medial bundle and a lateral bundle, which grow in the medial and lateral branches of the optic tract, respectively. Although the course followed by RGC axons in the visual pathway is complex, we propose a model in which the organization of fibers in the nerve and tract can arise from a few rules of axon guidance. To determine whether the optic tecta, the primary retinal targets, play a role in the development and organization of the optic nerve and tract, we removed the tectal primordia in Rana embryos and examined the order in the nerve when the animals had reached larval stages. We found that the order in the nerve and tract was well preserved in tectumless frogs. Therefore, we propose that guidance factors independent of the target direct axon growth in the frog visual system.