The capacity of regenerating axons for long-term growth and synaptic plasticity was investigated in the visual system of adult hamsters. Four to six and 8-10 months after the eye and the superior colliculus (SC) were linked by a peripheral nerve (PN) graft, the retinal ganglion cell (RGC) axons that had regrown into the SC were examined ultrastructurally. Together with the data from hamsters with similar PN grafts for 2 months (Carter et al., 1989), this study spans most of the life of these animals. The overall findings indicate that (1) the RGC axons extended twice as far into the SC and the number of RGC terminals increased 30-fold between 2 and 4-6 months. These parameters did not change thereafter. The highest density of regenerated RGC terminals observed in the SC was 11.5% of controls. (2) The new RGC terminals acquired most of their normal ultrastructural characteristics by 2 months. (3) The mean size of the terminals was larger than in controls but decreased gradually, and there was a small increase in the size of the regenerated synapses. (4) At all times, the RGC terminals remained confined to the layers of the SC that normally receive retinal inputs, and their synapses were formed in normal proportions with the dendritic shafts and spines of SC neurons. Thus, there is a protracted long-term growth and remodeling of the RGC axons that have regenerated into the SC of these adult mammals.(ABSTRACT TRUNCATED AT 250 WORDS)