Laminar and sublaminar ultracytochemical localization of cytochrome oxidase in the optic tectum of normal goldfish.

Distinct laminae and sublaminae in the goldfish optic tectum exhibit substantial differences in cytochrome oxidase (C.O.) reactivity. To determine whether these differences are associated with differential reactivity of different neuronal profiles, each tectal sublamina was examined at the ultrastructural level following C.O. treatment. The greatest abundance of darkly reactive mitochondria was found in the optically innervated layers within both pre- and postsynaptic profiles in correspondence with the most intense staining of these layers at the light microscopic level. Many reactive mitochondria were localized within terminals that were presumed to be optic on the basis of cytological criteria or were shown to be optic by filling optic fibers with HRP and processing so as to simultaneously demonstrate both mitochondrial C.O. reactivity and HRP labeling. These optic terminals tended to differ from each other in size and level of reactivity. The largest terminals were located within sublamina d of the stratum fibrosum et griseum superficials (SFGSd), and these were the most intensely reactive and contained the greatest number of darkly reactive mitochondria. Medium-sized terminals were found within sublaminae SFGSa, SFGSb, and a and c of the stratum album centrale (SACa,c). These were also darkly reactive but contained fewer mitochondria. Other medium-to-small optic terminals were found in stratum opticum a and b (60a,b), SFGSb, SFGSc, and stratum griseum centrale c (SGCc). These typically contained fewer mitochondria that also tended to be relatively less reactive, although darkly reactive mitochondria were also present. We suggest that the metalbolic differences within optic terminals of different size and sublaminar stratification arise from different ganglion cell classes and that the different optic layers of tectum are functionally substratified. As expected, darkly reactive mitochondria were most abundant in the intensely stained sublaminae, which included the optic lamina SFGS and nonoptic sublamina SGCa, and they were found not only within optic terminals but also within dendrites, presynaptic dendrites, and nonoptic terminals as well. Glial processes tended to contain less reactive mitochondria. The most prominent of the nonoptic terminals were the large-diameter P1 terminals, which contained pleomorphic vesicles and formed symmetric (presumed inhibitory) synapses. In stratum marginale most of the darkly reactive mitochondria were localized within dendrites. In the rest of the tectal layers most of the darkly reactive mitochondria were found in both presynaptic terminals and dendrites. The localization of numerous reactive mitochondria to terminals contrasts with several mammalian CNS structures in which reactive mitochondria are found predominantly in dendrites. The darkly reactive layers also tended to have more complex neuropils with a greater variety of presynaptic profiles. The less reactive neuropil strata contained comparatively few P1 terminals. The remaining layers, which contained mainly cell bodies (stratum periventriculare) or axons (SOa, SOc, SACb), were only lightly to moderately reactive. These laminar differences further support our previous light-level observations that the goldfish optic tectum may be subdivided into metabolically and, presumably, functionally distinct sublaminae.