Ultrastructure of the developing sympathetic nerve cell and the storage of catecholamines

Abstract

Postnatal development of the superior cervical ganglion of the rat was studied by electron microscopy after fixation in potassium permanganate. The ultrastructural appearances were correlated with fluorescence microscopic observations on the distribution of catecholamines. Small cells with numerous granular vesicles (90–150 nm) were observed even in the newborn rat ganglion; they corresponded to small intensely fluorescent (SIF) cells. Most sympathetic cells at this stage were weakly fluorescent and contained little cytoplasm with few cytoplasmic organelles. These cells were considered early sympathicoblasts; they did not contain any granular vesicles, but multivesicular bodies were common. Outer cell membranes of neighbouring sympathicoblasts were often in direct contact, although slender satellite cell processes were sometimes seen between them. Nerve terminals with numerous empty vesicles, presumably cholinergic preganglionic synapses, were observed on the perikaryon of some early sympathicoblasts. Cells with well developed Golgi apparatus, endoplasmic reticulum, mitochondria and multivesicular bodies appeared a few days after birth. Such cells, considered late sympathicoblasts, were predominant in the ganglia of 1-week-old rats. Although an even catecholamine fluorescence was seen throughout the cytoplasm of such cells, these usually contained only a few large granular vesicles (60–110 nm) near the outer cell membrane and near the Golgi apparatus, most of the cytoplasm being devoid of them. However, occasional late sympathicoblasts showed large granular vesicles (60–110 nm) scattered throughout the cytoplasm, while other were entirely free of them. Direct cell membrane contacts between late sympathicoblasts were common. Further differentiation resulted in the formation of young nerve cells, whose diameter was about twice of that of the early sympathicoblasts, whose cytoplasm was densely filled with cell organelles, and which were completely surrounded by a layer of satellite cell cytoplasm. Young nerve cells exhibited an even catecholamine fluorescence thoughout the cytoplasm, but many cells also showed intensely fluorescent granules near the outer cell membrane. Numerous small granular vesicles (30–60 nm) were seen in the cell periphery of most young nerve cells, while the cytoplasm was devoid of them elsewhere; some granular vesicles were seen in the Golgi region. Occasional young nerve cells showed numerous small granular vesicles (30–60 nm) throughout the cytoplasm, and others were without granular vesicles altogether. It is concluded that: (1) catecholamines are stored in developing sympathetic cells mainly outside granular vesicles, although granular storage progressively increases with the cell maturation; (2) granular vesicles are large (60–110 nm) in sympathicoblasts but become small (30–60 nm) in nerve cells; (3) the 3 types of sympathicoblasts and nerve cells observed, those with some granular vesicles in the periphery, those with granular vesicles throughout the cytoplasm and those without any granular vesicles, presumably represent different functional stages of the same cell; and (4) the small granule-containing (SIF) cells are distincly different from sympathicoblasts or sympathetic nerve cells.