Activity and the formation of ocular dominance patches in dually innervated tectum of goldfish

Abstract

This study tested (1) whether blocking impulse activity in both eyes of fish with one tectum prevents the formation of ocular dominance patches, (2) whether areas receiving a high density of innervation from one eye receive a low density from the other, and (3) whether there is an electrophysiological correlate to the anatomical patches. One tectum was removed in goldfish so that the optic nerve fibers from both eyes would compete for synaptic space in the remaining tectum. The terminal arbors from the two projections initially overlapped but by 50 to 60 days segregated into ocular dominance patches, demonstrated by labeling both projections, the normal one with horseradish peroxidase and the regenerating one with tritiated proline radioautography. Alternate sections were processed for radioautography and histochemistry. All projections were drawn by 'blind' observers using a camera lucida and were fully reconstructed. Both the level of patchiness within each projection and the correspondence of patches and holes between the two projections were quantified from these reconstructions. Binocular tetrodotoxin (TTX) injections from 18 to 75 days after surgery significantly reduced patchiness, as compared to controls injected with citrate-Ringers solution. When the binocular block was continued until 95 days, segregation was still significantly reduced relative to controls. These results support a hypothesis for an activity-dependent mechanism of segregation of ocular dominance patches. In controls but not TTX-blocked fish, there was a significant tendency for high density areas in one projection to receive a lower density projection from the other eye, and vice versa. However, the two projections were not entirely complementary. Survival of control fish for an additional 5 months resulted in more sharply defined patches but no increase in complementarity. Recordings of field potentials evoked by shocking either optic nerve demonstrated an electrophysiological correlate to the anatomical patches in single tectal fish. Large field potentials from one eye were generally associated with small potentials from the other eye, and vice versa. When the recording sites were marked with electrolytic lesions, there was a direct and significant correlation between the magnitude of the field potentials and the density of the anatomical ocular dominance patches.