Patterns of convergence and divergence of retinal and cortical synaptic terminals in the cat superior colliculus

Abstract

The spatial distributions of retinal and area 17 synapses in the zonal, superficial gray, and upper optic layers of the cat superior colliculus have been examined quantitatively. The colliculus was systematically sampled throughout its rostral-caudal extent. The position of every retinal and ipsilateral area 17 synaptic terminal was mapped with a computer microscope plotter. From these plots, the depth, medial-lateral position, and synaptic density were calculated. Retinal terminals (RT) were identified by their characteristic pale mitochondria, cortical terminals (CT) by degeneration after area 17 lesions. Of 14,939 plotted terminals, 58% were retinal, 42% from area 17. The two sets of synapses were partially segregated along both the dorsal-ventral and rostral-caudal planes of the colliculus. In the dorsal ventral plane, nearly 2/3 of RT were concentrated in a dense band within the upper superficial gray layer. The remainder were lightly distributed throughout the deep superficial gray and upper optic layers. By contrast, almost 3/4 of all CT lay in a 100–300 μm band just below the retinal dense band, within the deep superficial gray. The two sets of terminals were also partly segregated in the rostral-caudal plane. The rostral tip of the colliculus, which has a representation of the ipsilateral hemifield, had a very dense accumulation of RT, but almost no CT. The area centralis representation, just behind the rostral pole, showed a marked decrease in RT density. CT were most densely distributed in this region. In more caudal regions of the colliculus, RT gradually increased while CT decreased in density. The medial to lateral distribution of both RT and CT had obvious peaks and troughs, but these were randomly distributed. These results indicate that: (1) RT and CT synapses in the colliculus overlap less than previously reported. It is, therefore, likely that many cells in the superior colliculus do not receive afferents from both sources. (2) Although retinal and cortical terminals have a patchy distribution, there is no indication that they form regular, alternating columns in the superior colliculus.