Regenerated synaptic connections in the damaged mammalian visual system were studied in adult hamsters in which retinal ganglion cells (RGCs) regrew their axons through autologous peripheral nerve grafts directed from the stump of the transected optic nerve to the superior colliculus (SC). Unitary responses to illumination of small areas of the visual field were recorded within the superficial laminae of the reinnervated SC 23 to 60 weeks after grafting. Each element of a typical bursting response to light consisted of a terminal potential (TP) (half width 164 +/- 25 microseconds, amplitude up to 171 microV) arising from a regenerated RGC axon terminal arborization, followed at a latency of 268 +/- 63 microseconds by a longer duration negative focal synaptic potential (FSP) (half width 938 +/- 396 msec, amplitude up to 188 microV) reflecting EPSPs in neurons within the terminal field of the regenerated RGC axon. The FSP but not the TP was attenuated in a dose- dependent manner by iontophoretic application of GABA. In some cases spikes arose from FSPs after the first two or three impulses of a train, presumably reflecting summation of EPSPs to threshold for excitation in SC neurons contacted by the regenerated RGC axon terminals. Up to one-third of the area of the SC can be infiltrated by arborizations of the regenerated RGC axons that enter the SC through a nerve graft inserted in the lateral aspect of the SC. These experiments indicate that terminal arborizations of individual regenerated RGC axons can synapse with multiple neurons in the SC and that convergence of inputs from regenerated RGC axons is not required for activation of SC neurons in response to light.