The postnatal development of retinocellular projections in normal hamsters and in hamsters following neonatal monocular enucleation: A horseradish peroxidase tracing study

Abstract

The pattern of distribution of the retinal projections to the superior colliculus (SC) has been studied in developing normal hamsters and in hamsters following unilateral eye enucleation at birth, using the anterograde horseradish peroxidase (HRP) method. The results show that in normal hamsters the contralateral retinocollicular projection has already reached the caudal pole of the SC on the day of birth, and covered the entire SC by day 1. The ipsilateral retinocollicular projection is distributed only to the rostrolateral portion of the SC on day 0, but has covered the entire area of the SC on day 1. The innervation of the SC by the ipsilateral projection increases gradually until it reaches its maximum density on day 3 or day 4. Beginning on day 6, the density of the ipsilateral projection decreases markedly except in areas where there is a distinct clumping of retinal fibers. The normal adult pattern, which consists of dense clumps of ipsilateral retinal projections in the rostral half of the SC and a sparse ipsilateral retinal projection distributing in almost the entire extent of the SC, is established on day 10. In animals in which one eye was removed on the day of birth, the ipsilateral projection is observed in the rostral two-thirds of the SC on day 1, and innervates the entire extent of the colliculus on day 2. On day 3 or day 4, this projection is denser than that found in normal animals of the same age. The SC remains heavily innervated by ipsilateral fibers on and after day 6. The abnormal adult pattern, which consists of dense ipsilateral retinal projections in most parts of the SC, is observed on day 10. The anomalous ipsilateral retinocollicular projection which develops in eye-enucleated animals suggests that there is a competitive interaction between fibers from the two eyes during development which is critical in shaping the normal adult pattern of the ipsilateral retinocollicular projection. The early development of the contralateral projection is in advance of the ipsilateral projection, and removal of the contralateral fibers by eye enucleation at birth seems to result in a further delay in the development of the ipsilateral projection. This suggests that in the hamster the contralateral fibers may play a role in guiding the ipsilateral fibers to reach their target region. The normal development of the ipsilateral projection can be divided into two phases: there is an initial progressive increase in the density of the projection, followed by a decrease in the extent and, in some regions, the density of the projection. This implies that some of the ipsilateral fibers are transient in nature and are eliminated during development. In unilaterally enucleated hamsters the ipsilateral projection remains substantial after day 6 which suggests that some of the uncrossed fibers which would normally be eliminated are retained. In addition, the absolute extent of the enhanced ipsilateral projection is larger than the absolute extent of the normal projection at its greatest. These observations suggest that rerouting and/or sprouting of the uncrossed retinal fibers may also be important in generating the enlarged projection observed in hamsters with one eye removed at birth.