Topographic targeting errors in the retinocollicular projection and their elimination by selective ganglion cell death

Abstract

In adult rats, as in other rodents, the retinocollicular projection is topographically organized in a very precise manner. Experiments involving the use of the retrogradely transported fluorescent dye fast blue as either a short- or long-term marker in neonatal rats indicate that the precision of this retinotopic projection does not arise ab initio, but rather is brought about by the preferential elimination of those ganglion cells whose axons project to topographically inappropriate regions of the colliculus. Such topographic targeting errors have been identified along both the rostrocaudal and mediolateral axes of the colliculus, and their elimination occurs during the period of naturally occurring ganglion cell death, which is completed by about postnatal day 10. When impulse activity in the retinal ganglion cell axons is blocked by repeated intraocular injections of the sodium channel-blocking agent tetrodotoxin (TTX) throughout the postnatal period of ganglion cell death, the preferential loss of the incorrectly projecting ganglion cells does not occur in the activity-blocked eye, although, as reported elsewhere, the overall loss of ganglion cells is comparable to that seen in normal animals. This supports the notion that the mechanism for selecting against incorrectly projecting ganglion cells is based on impulse activity among the competing ganglion cell axons. However, under activity-block conditions, the aberrantly projecting axons appear to retract from the caudal margin of the colliculus. The death of retinal ganglion cells during development thus seems to serve 2 purposes: It provides for the quantitative matching of the ganglion cell population to the needs of its central projection fields, and, at the same time, it serves to selectively eliminate those cells whose axons project to inappropriate targets or to inappropriate regions within the correct target fields.