Innervation of abdominal paraganglia: An ultrastructural study

Abstract

Abdominal extra-adrenal chromaffin tissue, or paraganglia, was examined at the ultrastructural level to elucidate the innervation of this adrenal medullary homologue. Paraganglia display unmyelinated nerve fibers surrounded by Schwann cell cytoplasm. These nerves are separated from the paraganglion Type I (granule-containing) cells by cytoplasmic projections of paraganglion Type I1 (satellite) cells. However, serial sections show that the nerves eventually make synaptic contact with the Type I cell. At the axon-chromaffin cell junction, only the outer aspect of the nerve is covered by the satellite cell. The presynaptic endings contain numerous synaptic vesicles, mitochondria and glycogen particles. The vesicles are predominantly of the clear-cored variety, but a few possess centers which are electron opaque. The pre-and postsynaptic membranes are separated by a subsynaptic space and occasionally exhibit the membranal densities usually associated with synaptic areas. These ultrastructural studies establish definite evidence that abdominal paraganglion cells are innervated.The ultrastructure and probable function of abdominal extra-adrenal chromaffin tissue, or paraganglia, have been reported by several investigators (Viragh and Both, '67; Coupland and Weakley, '68; Mascorro and Yates, '70), and detailed morphological studies indicate that paraganglionic tissue is essentially the same as that of the adrenal medulla (Mascorro and Yates, in press). While a preganglionic sympathetic innervation for the adrenal medulla has been described (Cummings, '69), few ultrastructural reports have dealt with this aspect of the paraganglia, and synaptic contacts on these cells have not been reported.Earlier studies with various staining techniques and silver impregnation methods demonstrated unmyelinated nerve fibers within the paraganglia and suggested that extra-adrenal chromaffin tissue receives a preganglionic sympathetic innervation (Pines, '24; Kofmann, '35; Hollinshead, '37). Also, studies on the chromaffin cells in the ganglia of the sympathetic trunks indicated that these receive a direct innervation via the anterior roots of the spinal cord (Karpenko, '64). Recent work has failed to demonstrate an innervation of paraganglion cells (Hervonen, '71 ; Mascor-J. MORPH., 142: 153-164, ro and Yates, '72a). The present study provides evidence that such cells are innervated. MATERIALS AND METHODS Syrian hamsters (Mesocricetus auratus;Lakeview Hamster Colony, Newfield, N J.) 1 to 13 days of age and young squirrel monkeys (Saimiri sciureus; Tarpon Zoo, Florida) were anesthetized with sodium amobarbital (Amytal; 1 mg/kg) and perfused through the heart with a solution of 3.0% glutaraldehyde buffered with 0.2 M sodium phosphate to pH 7.2-7.4. The retroperitoneal area from the renal vessels caudal to the abdominal aortic bifurcation was removed, divided into several transverse slices and fixed in the perfusion fluid an additional two hours. After a two hour wash in phosphate buffer containing 10 % sucrose, the tissue slices we...

Location and size of carotid body-like organs (paraganglia) revealed in rats by the permeability of blood vessels to Evans blue dye

“…However, nerve endings are comparatively infrequent in extra-adrenal chromaffin tissue (Mascorro & Yates, 1974), and there is little information on whether secretions from extra-adrenal chromaffin tissue contribute significantly to levels of catecholamines in blood. In the rat, extra-adrenal chromaffin tissue degenerates after birth and little is present in the adult (Lempinen, 1964;Coupland, 1965b).…”

From proliferation to target innervation: signaling molecules that direct sympathetic nervous system development

“…The role of nerves in the function of endocrine extra-adrenal chromaffin cells is uncertain. Abdominal extradrenal ganglia lack innervation in some species (Coupland and Weakley, 1970b, Mascorro, et al, 1994, Mascorro and Yates, 1977, including the mouse, (Mascorro and Yates, 1971), but nerve fibres of unknown origin are present in others (Coupland, et al, 1982, Mascorro and Yates, 1974, Partanen, et al, 1984a, Partanen, et al, 1984b where they appear much less dense than those associated with adrenal chromaffin cells. In all these cases it remains to be established that any innervation is motor rather than sensory.…”

Normal Function of Extra-Adrenal Chromaffin Tissues in the Young Rabbit and Guinea-Pig

“…In other forms, e.g. in man (Hervonen, 1971;Coupland, 1972), Syrian hamster and squirrel monkey (Mascorro & Yates, 1974) extra-adrenal chromaffin bodies are innervated, albeit less richly than the adrenal medulla. Work in this laboratory over the past 5 years has demonstrated that the main extra-adrenal chromaffin body of the guinea-pig, described previously using light microscopy (Coupland, 1960;Costa & Furness, 1973) as lying adjacent to and usually posterior to the left renal vein, also comes into the category of innervated extra-adrenal chromaffin tissue, and typical cholinergic nerve endings have been observed on extraadrenal cells on many occasions, even though they are less frequently observed per unit area of chromaffin cells than they are in the adrenal medulla (R. E. Coupland, unpublished observations).…”