Regenerated optic fibers in goldfish reestablish a crude sectoral order in the visual pathway

Abstract

The goldfish optic pathway is regenerated after an optic nerve crush. We have examined the axonal topography of the regenerated pathway by labeling, with horseradish peroxidase (HRP), axons originating from retinal sectors or annuli. The positions of the labeled axons in the cross section of the pathway were compared to the normal and related to the factors that may influence axonal pathfinding. The positions of retinal axons in the cross section of the normal pathway are predictable from the retinal addresses of the ganglion cells described by the polar coordinates r (the distance from the optic disc) and theta (the sectoral or clockface position). The two coordinates map orthogonally onto the cross section of the pathway; r varies monotonically along one axis; theta varies along a perpendicular axis. The normal r-order, present in the nonregenerated stump of the experimental nerve, was severely degraded and perhaps lost entirely in the regenerated optic nerve, tract, and brachia. Sectoral order was also lost as the axons passed the crush site, but it was reestablished, albeit crudely, in the regenerated tract and brachia where axons tended to occupy positions appropriate to their dorsal, ventral, nasal, and temporal retinal origins. The exit sequence of the regenerated axons from the stratum opticum into the tectal neuropil was normal: temporal first, nasal last. These results suggest that the regenerating fibers followed some theta-specific cue located in the nonaxonal environment. It seems likely that the original axons probably followed the same cue. In contrast, the absence of r-order suggests that there is no r-specific cue for the regenerates to follow. It seems likely that the original r-order was a consequence of nonspecific influences--the orderly spatiotemporal growth of the retina and the existence of a permissive region for axonal growth.