Anomalous retrograde labeling of brain cells from the eye in the goldfish: evidence for long distance growth of sprouted neurites.

We have used retrograde labeling with horseradish peroxidase (HRP) and a wheat germ agglutinin conjugate of HRP (WGA:HRP) to investigate the projections of the nucleus postglomerulosus (nPg) both in normal goldfish and in animals which had undergone retinal removal. In normal animals, our evidence indicates that nPg projects only to the optic tectum. Using small HRP and WGA:HRP application sites in the tectum, we have shown that nPg cells have broadly spread terminals in the tectal neuropil and that there is no obvious correspondence between the rostrocaudal axis of the nPg and the deployment of the terminal arbors of its cells along the rostrocaudal axis of the tectum. In addition, we found no evidence for an nPg projection to the eye in normal animals. After retinal removal we found that nPg cells were more readily backfilled from small tectal applications of HRP. However, our most interesting observation was that at 4-6 weeks and more after ocular surgery, we could retrogradely label the cells of the nPg with intraocular or retroocular injections of WGA:HRP. At the same postoperative times, we were also able to label neurites in the atrophied optic nerve by microinjecting WGA:HRP into the contralateral midbrain tegmentum. Finally, we found that the cells of the nPg undergo a hypertrophic response, similar to that seen in other neurons after axotomy, following retinal removal or section of the dorsomedial brachium of the optic tract. Thus, these cells respond to retinal denervation of the tectum with a response characteristic of axotomized cells although their axons have not been cut. Similar changes were also seen in the nucleus isthmi on both sides of the brain following retinal removal. We interpret our data to indicate that cells of the nPg can respond to optic (and thus heterotypic) denervation of their terminal field by sprouting processes which grow away from the terminal field, through denervated optic pathways, to the retinaless eye. This interpretation requires that the sprouted processes grow for several millimeters.