Synaptic plasticity in the rod terminals after partial photoreceptor cell loss in the heterozygous rds mutant mouse.

Abstract

In the retina of mice heterozygous for the retinal degeneration slow gene (rds/+) the photoreceptor cells, both rods and cones, develop abnormal outer segments but establish normal synaptic contacts. The other retinal layers also show normal structural organization. Starting from the age of 2 months, a very slow loss of photoreceptor cells progresses throughout life. As a result, the photoreceptor cell population in the retina of the affected mice is reduced to less than half at the age of 9-18 months. In some of the surviving rod terminals during this period, an increase in the number of synaptic ribbons is recorded. At the same time, the profiles of processes originating from the second order neurons and participating in these synapses are also increased in number so that the multiple ribbons appear as centres of multiple synaptic sites. Morphometric measurements of the perimeter of the synaptic profiles in rod terminals show a significant increase in the rds/+ retina over that of the control retina. Observations based on serial electron microscopy indicate that multiple synaptic sites are developed while the number of the second order neuronal processes, entering the terminals, remains unchanged. The frequency of terminals with multiple synapses in the rds/+ retina increases with progressive photoreceptor cell loss. Similar changes do not occur in the terminals of the cones. It is postulated that loss of some rod photoreceptor cells within a group that is presynaptic to common bipolars or horizontal cells results in partial deafferentation which in turn stimulates the growth of the remaining synaptic elements. The possible compensatory effect and functional significance of such synaptic growth are discussed.