Laminar histochemical and cytochemical localization of cytochrome oxidase in the goldfish retina and optic tectum in response to deafferentation and during regeneration

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Abstract
Cytochrome oxidase (C.O.) histochemistry and cytochemistry were used to examine the effects of optic denervation and subsequent optic fiber regeneration on oxidative metabolism in the retina and optic tectum of the goldfish. In the tectum, there was a dramatic and rapid decrease in C.O. activity within the optic layers 3–4 days after contralateral eye removal or optic nerve crush. At the E.M. level this was correlated with an initial decrease in mitochondrial reactivity within optic terminals followed by the subsequent degradation of mitochondria and phagocytosis of optic terminals. By 1 month after optic nerve crush, the entire tectum was reinnervated. However, the normal dark reactivity of the stratum fibrosum et griseum superficialis (SFGS), the main optic innervation layer, was not restored until after 3–4 months postcrush. The normal intense reactivity of the largediameter optic axons and terminals at the bottom of the SFGS required an even longer period, about 7–8 months, for full recovery. The delayed restoration of C.O. reactivity was not due to a delay in synaptogenesis or in mitochondrial accumulation within optic terminals but to a delay in the maturation of mitochondrial reactivity. Following regeneration, the normal sublaminar stratification of C.O. bands was reestablished, suggesting that metabolically distinct classes of optic fibers may reinnervate at their original sublaminae. By using a distinct and persistent C.O. reactive sublamina, a of stratum griseum centrale (SGCa), just subjacent to the SFGS, it was possible to measure the thickness of the SFGS following optic denervation and subsequent reinnervation. At 1 week after optic nerve crush, the SFGS shrank by 35%. During regeneration, the thickness of the SFGS gradually increased to about 23% above normal at 2 months postcrush and this was maintained indefinitely. In the retina, ganglion cells were hypertrophic by 1 month postcrush and exhibited elevated levels of C.O. during the same period of time when optic terminals were unreactive. This indicates that oxidative metabolic activity within perikarya and axon terminals of the same neuron may be locally and independently regulated. It also suggests that in spite of the well‐known elevation of axonal transport during the initial period of axon elongation and synaptogenesis, that oxidative metabolic energy production within the optic fibers is less than that of the mature projection. We hypothesize that the comparatively greater oxidative metabolism of the mature projection results from greater synaptic convergence of fibers having correlated activity and may be a target‐mediated metabolic response of optic axons having reached their topographically appropriate synaptic sites.