Comparison of the ultrastructure of cortical and retinal terminals in the rat superior colliculus

Abstract

We compared the ultrastructure and synaptic targets of terminals of cortical or retinal origin in the stratum griseum superficiale and stratum opticum of the rat superior colliculus. Following injections of biotinylated dextran amine into cortical area 17, corticotectal axons were labeled by anterograde transport. Corticotectal axons were of relatively small caliber with infrequent small varicosities. At the ultrastructural level, corticotectal terminals were observed to be small profiles (0.44 +/- 0.27 microm(2)) that contained densely packed round vesicles. In tissue stained for gamma amino butyric acid (GABA) using postembedding immunocytochemical techniques, corticotectal terminals were found to contact small (0.51 +/- 0.69 microm(2)) non-GABAergic dendrites and spines (93%) and a few small GABAergic dendrites (7%). In the same tissue, retinotectal terminals, identified by their distinctive pale mitochondria, were observed to be larger than corticotectal terminals (3.34 +/- 1.79 microm(2)). In comparison to corticotectal terminals, retinotectal terminals contacted larger (1.59 +/- 1.70 microm(2)) non-GABAergic dendrites and spines (73%) and a larger proportion of GABAergic profiles (27%) of relatively large size (2.17 +/- 1.49 microm(2)), most of which were vesicle-filled (71%). Our results suggest that cortical and retinal terminals target different dendritic compartments within the neuropil of the superficial layers of the superior colliculus.

Fig. 1

A: The photomicrograph illustrates the distribution of labeled terminals in a coronal section through the SC following an injection of biotinylated dextran amine in the visual cortex. The laminae of the SC are indicated. SGS, stratum griseum superficiale; SO, stratum opticum; SGI, stratum griseum intermediale. Scale bar = 1 mm. B–D: The photomicrographs illustrate the labeled terminals of A at higher magnification. Scale bars = 30 μm (B); = 20 μm (C, which also applies to D).

Fig. 2

The drawings illustrate the locations within parasagittal sections of the superior colliculus, where blocks of tissue were sampled for analysis at the ultrastructural level. Two cases were analyzed: R03-14 and R03-115. The laminae of the SC are indicated. C, caudal; D, dorsal; IC, inferior colliculus; PT, pretectum; R, rostral; V, ventral.

Fig. 3

Examples of corticotectal terminals labeled by the anterograde transport of biotinylated dextran amine. These terminals primarily contact (white arrows) small non-GABAergic (−, low density of gold particles) dendrites (A, C, and D). Occasional contacts were made onto GABAergic (+, high density of gold particles) dendrites (B). Scale bar = 1 μm and applies to all panels.

Fig. 4

Examples of retinotectal terminals identified by their pale mitochondria. These terminals primarily contact (arrows) both non-GABAergic (−, low density of gold particles) dendrites and GABAergic (+, high density of gold particles) dendrites that contain vesicles. Scale bar =1 μm and applies to all panels. A: A retinotectal terminal contacts a GABAergic dendrite that contains vesicles and a nonGABAergic dendrite. B: A retinotectal contacts a small nonGABAergic dendrite. C: A retinotectal terminal contacts a small nonGABAergic dendrite and 3 GABAergic dendrites that contain vesicles.

Fig. 5

The histograms compare the sizes of retinotectal and corticotectal terminals and their GABAergic and non-GABAergic postsynaptic targets. Data from both cases are combined.

Fig. 6

The scatter plot compares the areas of presynaptic corticotectal and retinotectal terminals and their postsynaptic targets.