Spontaneous retinal activity is tonic and does not drive tectal activity during activity-dependent refinement in regeneration.

During development, waves of activity periodically spread across retina to produce correlated activity that is thought to drive activity-dependent ordering in optic fibers. We asked whether similar waves of activity are produced in the retina of adult goldfish during activity-dependent refinement by regenerating optic fibers. Dual-electrode recordings of spontaneous activity were made at different distances across retina but revealed no evidence of retinal waves in normal retina or during regeneration. Retinal activity was tonic and lacked the episodic bursting associated with waves. Cross-correlation analysis showed that the correlated activity that was normally restricted to near neighbors (typically seen across 100-200 microm and absent at >500 microm) was not altered during regeneration. The only change associated with regeneration was a twofold reduction in ganglion cell firing rates. Because spontaneous retinal activity is known to be sufficient to generate refinement during regeneration in goldfish, we examined its effect on tectal activity. In normal fish, acutely eliminating retinal activity with TTX rapidly reduced tectal unit activity by >90%. Surprisingly, during refinement at 4-6 weeks, eliminating retinal activity had no detectable effect on tectal activity. Similar results were obtained in recordings from torus longitudinalis. After refinement at 3 months, tectal activity was again highly dependent on ongoing retinal activity. We conclude that spontaneous retinal activity drives tectal cells in normal fish and after regeneration but not during activity-dependent refinement. The implications of these results for the role of presynaptic activity in refinement are considered.