Parvalbumin (PV) and calbindin-D 28K (CaBP) are calcium binding proteins involved in calcium regulation in the brain. In some regions they coexist in the same neuron, while in other regions they are found in different cell types. We have studied the distribution and morphology of PV labeled neurons in the cat superior colliculus (SC) with antibody immunocytochemistry and compared this labeling to that of CaBP. PV neurons were concentrated in a dense tier within the deep superficial gray and upper optic layers. Scattered PV neurons also were found within the deep layers of SC. By contrast, CaBP neurons were concentrated in three tiers: one within the zonal and upper superficial gray layers, a second within the deep optic and upper intermediate gray layers (IGL), and a third within the deep gray layer. The distribution of PV neurons is thus complementary to that of CaBP neurons, with the CaBP cell tiers bordering the dense tier of PV neurons. PV neurons varied in size and morphology. The average diameter of labeled cells was 20 microns, almost twice the size of CaBP neurons. The cells were predominantly round, vertical fusiform, or stellate, and included the very large neurons found scattered in the IGL. Horseradish peroxidase injections into the lateral geniculate nucleus, the lateral posterior nucleus, the opposite superior colliculus, the dorsal lateral pontine gray nucleus, and two descending pathways--the crossed predorsal bundle and the tecto-ponto-bulbar tracts--each labeled SC neurons that were also labeled by PV. A large percentage (84%) of projection neurons contained PV. This result also differs from CaBP neurons in SC, most of which are interneurons. Two antigen double-label experiments did not produce any cells that contained both PV and CaBP. The two calcium binding proteins thus reveal a unique sublaminar organization in SC that consists of alternating small cell interneuron groups and large cell projection neuron groups.
The calcium binding protein calbindin-D 28K (CaBP) has been localized in the cat superior colliculus (SC). Four important features of SC organization have been revealed by using CaBP immunocytochemistry. 1) CaBP neurons formed three laminar tiers in SC, one within the upper one half of the superficial gray layer (SGL), the second bridging the deep optic (OL) and intermediate gray layers (IGL), and the third within the deep gray layer (DGL). 2) CaBP labeled several classes of interneuron in SC. In the upper CaBP tier, the labeled neurons were all small, but they varied in morphology and included horizontal, pyriform, and stellate neurons. A unique class of interneuron was labeled by anti-CaBP in the OL-IGL tier. This cell was stellate-like with highly varicose dendrites and broad dendritic trees. Other labeled neurons in the intermediate and deep tiers included nonvaricose stellate neurons and rare large neurons in the DGL. 3) A few anti-CaBP neurons were projection neurons. Virtually no CaBP neurons were retrogradely labeled after injections of HRP into the predorsal bundle and dorsolateral midbrain tegmentum or into the lateral posterior nucleus. However, 2.4% of anti-CaBP neurons were retrogradely labeled after HRP injections into the dorsal and ventral lateral geniculate nuclei. These represented 14.7% of all neurons projecting to the LGN complex. 4) A small percentage of CaBP neurons co-localized GABA. A two-chromagen double-labeling technique showed that about 4.0% of labeled neurons were labeled by both antibodies. In summary, antibodies to CaBP densely labeled subpopulations of neurons in the cat SC, most of which were interneurons, some of which projected to the LGN, and a few of which co-localized GABA.
Although the excitatory neurotransmitter glutamate is known to be present in the cat superior colliculus (SC), the types of synapses that contain glutamate have not been examined. We, therefore, studied the ultrastructure of synaptic profiles labeled by a glutamate antibody by using electron microscopic postembedding immunocytochemistry. In addition, unilateral aspiration lesions of areas 17-18 were made at 5-28 days before death in order to determine whether degenerating terminals from visual cortex were glutamate immunoreactive (Glu-ir). Three types of axon terminal were glu-ir: 1) those containing large, round synaptic vesicles and pale mitochondria, characteristic of retinal terminals (RT profiles); 2) those containing small, round synaptic vesicles and dark mitochondria (RSD profiles); and 3) those containing large, round synaptic vesicles and dark mitochondria (RLD profiles). Measures of mean gold particle density revealed that RT, RSD, and RLD profiles had similar average grain densities (11.3-12.7 particles/unit area). Other labeled profile types included cell bodies, large-calibre dendrites, and myelinated axons. Axon terminals containing flattened synaptic vesicles and vesicle-containing presynaptic dendrites, both of which contain gamma-aminobutyric acid (GABA), had many fewer gold particles (3.6 and 4.8 mean particles/unit area, respectively). Following unilateral removal of visual cortex, normal RSD terminals were observed infrequently in the SC ipsilateral to the lesion. Synaptic terminals in the initial stages of degeneration were heavily labeled by the glutamate antibody, as were axon terminals and myelinated axons undergoing hypertrophied or neurofilamentous degeneration. These results show that both major sensory afferents to the superficial layers of cat SC contain glutamate--RT terminals from the retina and RSD terminals from visual cortex. The origin of RLD terminals is unknown.
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