Synaptic growth in the rod terminals of mice after partial photoreceptor cell loss: a three-dimensional ultrastructural study.

Abstract

Following partial loss of photoreceptor cells in the retina of mice afflicted by mutant genes, damaging light exposure, or old age, some of the remaining rod cells exhibited a process of growth in their synapses with the second order retinal neurons. This growth was recognized by the presence of multiple synaptic sites in some of the rod terminals in the outer plexiform layer. In this study, a comparative analysis of the microanatomical changes in the synaptic structures of the rod terminals in the retina of normal, rds homozygous and heterozygous mutant and light exposed albino mice was undertaken by using a computer-aided three-dimensional reconstruction. A rod terminal normally showed the presence of 1 synaptic complex consisting of a single synaptic ribbon located between 2 processes of horizontal cells and 2 bipolar cell dendrites. In a rod terminal showing an enlarged synaptic complex, 2 or 3 separate synaptic ribbons formed the centres of separate synaptic sites; each of the sites was characterized by the presence of 2 laterally placed horizontal cell processes and 2 bipolar cell dendrites. However, these processes from the multiple synaptic sites were observed to arise from the 2 horizontal and the 2 bipolar cell elements that were normally present in the rod terminal. Thus proliferation of synaptic sites in the rod terminals occurred through growth and sprouting from the processes of the second order neuronal components present within the terminals. The altered synaptic complexes in the variously affected groups were structurally comparable and appeared to have resulted from similar microanatomical changes. The increase in the frequency of rod terminals with multiple synaptic sites occurred as a sequel to increasing photoreceptor cell loss that was recorded at different age points in the different experimental groups. It is concluded that rod synapses in the adult mammalian retina possess structural plasticity that permits compensatory growth.