Ipsilateral retinofugal projections in a percomorph bony fish: their experimental induction, specificity and maintenance

Abstract

Adult bony fish possess only a small ipsilateral retinofugal projection, if any. Experimental manipulation, such as unilateral enucleation, can lead to an enhancement of this projection. We examined the patterns of, as well as the conditions for the development and maintenance of an enhanced ipsilateral retinofugal projection (EIRP) after nerve crush, after enucleation, and after various combinations of both types of surgery in juvenile and adult Haplochromis burtoni (Cichlidae). Retinal projections were labeled either unilaterally with horseradish perixodase, or with the lipophilic fluorescent dye DiI in aldehyde-fixed animals, or bilaterally with differently colored fluorescent dextran amines. Unilateral nerve crush always leads to the regeneration of retinofugal fibers to the contralateral tectum but spares some contralateral diencephalic nuclei. In addition, unilateral or bilateral nerve crush in many cases, and unilateral enucleation in some cases, leads to the development of an EIRP to the ipsilateral diencephalon and tectum. This EIRP persists (4 months and longer postoperatively) in only 10% of the unilaterally enucleated animals, in none of the animals subjected to unilateral nerve crush and in 79% of the animals subjected to bilateral nerve crush. All unilaterally enucleated animals in which the remaining, contralateral optic nerve was crushed develop and maintain an EIRP. These data suggest that nerve crush alone is sufficient to cause regenerating fibers to project, at least transiently, to the ipsilateral side of the brain. When the normal contralateral projection is either absent or in the process of regeneration, an EIRP can be maintained. In the latter case, alternate bands or patches of ipsi- and contralateral fibers in the tectum may result. Ipsilateral fibers follow unusual pathways by recrossing at the rostral diencephalon. Likewise, regenerating contralateral retinal fibers grow differently in this area; here, where the optic-nerve projection is reorganized into the optic tract, many regenerating fibers are deflected to the ipsilateral side of the brain. Despite atypical routes taken by some fibers, the EIRP nevertheless ends only in specific retinorecipient areas. An EIRP develops independently of the age of the animal, independently of the time lapse between enucleation and nerve lesion, and independently of persisting debris. However, in animals receiving an optic nerve lesion a long time after unilateral enucleation, the size of the EIRP and its tectal extent are reduced compared to that in animals enucleated around the same time as receiving the crush of the contralateral optic nerve.