Differential glutamatergic innervation in cytochrome oxidase-rich and -poor regions of the macaque striate cortex: quantitative EM analysis of neurons and neuropil.

One of the hallmarks of the primate striate cortex is the presence of cytochrome oxidase (CO)-rich puffs and CO-poor interpuffs in its supragranular layers. However, the neurochemical basis for their differences in metabolic activity and physiological properties is not well understood. The goals of the present study were to determine whether CO levels in postsynaptic neuronal compartments were correlated with the proportion of excitatory glutamate-immunoreactive (Glu-IR) synapses they received and if Glu-IR terminals and synapses in puffs differed from those in interpuffs. By combining CO histochemistry and postembedding Glu immunocytochemistry on the same ultrathin sections, the simultaneous distribution of the two markers in individual neuronal profiles was quantitatively analyzed. As a comparison, adjacent sections were identically processed for the double labeling of CO and GABA, an inhibitory neurotransmitter. In both puffs and interpuffs, most axon terminals forming asymmetric synapses (84%)--but not symmetric ones, which were GABA-IR--were intensely immunoreactive for Glu. GABA-IR neurons received mainly Glu-IR synapses on their cell bodies, and they had three times as many mitochondria darkly reactive for CO than Glu-rich neurons, which received only GABA-IR axosomatic synapses. In puffs, GABA-IR neurons received a significantly higher ratio of Glu-IR to GABA-IR axosomatic synapses and contained about twice as many darkly CO-reactive mitochondria than those in interpuffs. There were significantly more Glu-IR synapses and a higher ratio of Glu- to GABA-IR synapses in the neuropil of puffs than of interpuffs. Moreover, Glu-IR axon terminals in puffs contained approximately three times more darkly CO-reactive mitochondria than those in interpuffs, suggesting that the former may be synaptically more active. Thus, the present results are consistent with our hypothesis that the levels of oxidative metabolism in postsynaptic neurons and neuropil are positively correlated with the proportion of excitatory synapses they receive. Our findings also suggest that excitatory synaptic activity may be more prominent in puffs than in interpuffs, and that the neurochemical and synaptic differences may constitute one of the bases for physiological and functional diversities between the two regions.