FUNCTIONAL SYNAPTIC CONNECTIONS MADE BY REGENERATED RETINAL GANGLION-CELL AXONS IN THE SUPERIOR COLLICULUS OF ADULT HAMSTERS

Regenerated synaptic connections in the damaged mammalian visual syste m were studied in adult hamsters in which retinal ganglion cells (RGCs ) regrew their axons through autologous peripheral nerve grafts direct ed from the stump of the transected optic nerve to the superior collic ulus (SC). Unitary responses to illumination of small areas of the vis ual field were recorded within the superficial laminae of the reinnerv ated SC 23 to 60 weeks after grafting, Each element of a typical burst ing response to light consisted of a terminal potential (TP) (half wid th 164 +/- 25 mu sec, amplitude up to 171 mu V) arising from a regener ated RGC axon terminal arborization, followed at a latency of 268 +/- 63 mu sec by a longer duration negative focal synaptic potential (FSP) (half width 938 +/- 396 msec, amplitude up to 188 mu V) reflecting EP SPs 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 io ntophoretic application of GABA. In some cases spikes arose from FSPs after the first two or three impulses of a train, presumably reflectin g summation of EPSPs to threshold for excitation in SC neurons contact ed 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 a xons that enter the SC through a nerve graft inserted in the lateral a spect of the SC. These experiments indicate that terminal arborization s of individual regenerated RGC axons can synapse with multiple neuron s in the SC and that convergence of inputs from regenerated RGC axons is not required for activation of SC neurons in response to light.