Further study of the outward displacement of retinal ganglion cells during optic nerve regeneration, with a note on the normal cells of Dogiel in the adult frog

Abstract

In a previous study we observed massive retinal ganglion cell death in adult Rana pipiens after periods of optic nerve regeneration, and reported that large numbers of the surviving cells had become displaced bodily into the inner plexiform layer of the affected eye (Scalia et al.: Brain Research 344:267-280, 1985). The outwardly displaced cells could be identified as retinal ganglion cells because they could be back-filled with horseradish peroxidase (HRP) injected into the regenerated optic nerve. Quantitative observations on the abnormal outward displacement of ganglion cells are reported here. Parallel observations on normally displaced ganglion cells (cells of Dogiel) are also reported to clarify the distinctions between these two classes of cells. For the present work, injections of HRP of varying size were placed in the optic tectum bilaterally in 3 normal frogs and 9 frogs sustaining unilateral optic nerve regeneration. Most injections were centered at loci mapping the middle region of the nasal retina. The retinas were examined as flat-mounts and in-section. In 8 other frogs sustaining optic nerve regeneration, the HRP was administered bilaterally directly to the optic nerves in the orbit. Ganglion cells were labeled by retrograde transport of the HRP in the retinal ganglion cell layer in both the normal and affected eyes in areas topographically isomorphic with the tectal areas subtended by the injections. In the normal eyes, the orthotopic ganglion cells formed a strict monolayer, and virtually no cells existed in the inner plexiform layer. In the retinas sustaining optic nerve regeneration, the retinal ganglion cells abnormally displaced into the inner plexiform layer were also labeled topographically in correspondence with the injection sites. The abnormally displaced cells comprised 5.5% of the total population of surviving neurons in the retinal ganglion cell and inner plexiform layers. The mean outward dislocation of the displaced cells, as measured in one frog surviving optic nerve crush for 8 weeks, was 69.9 +/- 2.4% of the distance across the inner plexiform layer, which itself was uniformly 14.3 +/- 0.39 microns thick. Cells of Dogiel, which were embedded within the inner nuclear layer, were also labeled when the injections of HRP spread to include the area of representation of the optic disc. The labeled cells were restricted to a dorsal, peripapillary locus capping the optic disc. Therefore, some cells of Dogiel project to the tectum normally, but only from the central retina.(ABSTRACT TRUNCATED AT 400 WORDS)