Relationship between synaptogenesis and cytochrome oxidase activity in Purkinje cells of the developing rat cerebellum

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Abstract
In the adult CNS, the level of oxidative metabolism, as indicated by cytochrome oxidase cytochemistry, can be correlated with the level of neuronal activity. Specifically, heightened cytochrome oxidase activity in postsynaptic neurons can often be correlated with a greater proportion of excitatory inputs, whereas inhibitory inputs often result in a low level of cytochrome oxidase activity. This relationship has not been explored in developing neurons. To this end, cytochrome oxidase cytochemistry was used to compare the levels of oxidative metabolism in rat cerebellar Purkinje cells at various stages of their development. The results indicated that the level of cytochrome oxidase activity in Purkinje cell somata and dendrites correlated closely with the type of synaptic input (excitatory or inhibitory) received by the different segments of the cell. When the cell somata received predominantly excitatory input from climbing fibers, their mitochondria were evenly distributed between the three reactive classes: dark, moderate, and lightly reactive for cytochrome oxidase. When the cell somata received predominantly inhibitory input from basket cell terminals, lightly reactive mitochondria were the prevailing type. Further support for the correlation of excitatory synaptic input with high levels of cytochrome oxidase activity was found in the quantitation of mitochondria within Purkinje cell dendrites. These dendrites received largely excitatory input at all ages and had high levels of cytochrome oxidase activity throughout development and adulthood. There was also a relationship between the level of cytochrome oxidase activity and mitochondrial size within Purkinje cell somata and dendrites from birth to adult. Darkly reactive mitochondria had a greater mean area than moderately reactive mitochondria which, in turn, had a greater mean area than lightly reactive mitochondria. In addition, the packing density of mitochondria within the cytoplasm varied with age in both somata and dendrites. In the somata, the packing density peaked at postnatal day 7, and in dendrites, the peak occurred at postnatal day 10. These data indicate that in a developing system, postsynaptic neurons respond to sequential excitatory and inhibitory inputs by sequential heightening and lowering of their energy metabolism. Thus, cytochrome oxidase activity in a postsynaptic neuron can be correlated with the predominant type of synaptic input that it receives.