Carotid labyrinth of amphibians.

Abstract

The amphibian carotid labyrinth is a characteristic maze-like vascular expansion at the bifurcation of the common carotid artery into the internal and external carotid arteries. The carotid labyrinths of anurans are spherical and those of urodeles are oblong. In the intervascular stroma of both anuran and urodelan carotid labyrinths, the glomus cells (type I cells, chief cells) are distributed singly or in clusters between connective tissue cells and smooth muscle cells. In fluorescence histochemistry, the glomus cells emit intense fluorescence for biogenic monoamines. In fine structure, the glomus cells are characterized by a number of dense-cored vesicles in their cytoplasm. The glomus cells have long, thin cytoplasmic processes, some of which are closely associated with smooth muscle cells, endothelial cells, and pericytes. Afferent, efferent, and reciprocal synapses are found on the glomus cells. The morphogenesis of the carotid labyrinth starts in the larvae at the point where the carotid arch descends to the internal gills. Through the early stages of larval development, the slightly expanded region of the external carotid artery becomes closely connected with the carotid arch. By the end of the foot stage, the expanded region becomes globular, and at the final stage of metamorphosis the carotid labyrinth is close to its adult form. In fine structure, the glomus cells appear as early as the initial stage of larval development. At the middle stages of development, the number of dense-cored vesicles increases remarkably. Distinct afferent synapses are found in juveniles, although efferent synapses can be seen during metamorphosis. The carotid labyrinth is innervated by nerve fibers containing several kinds of regulatory neuropeptides. Double-immunolabeling in combination with a multiple dye filter system demonstrates the coexistence of two different neuropeptides. The amphibian carotid labyrinth has been electrophysiologically confirmed to have arterial chemo- and baroreceptor functions analogous to those of the mammalian carotid body and carotid sinus. The ultrastructural characteristics of the glomus cells during and after metamorphosis suggest that the glomus cells contribute to the chemoreception after metamorphosis. The three-dimensional fine structure of vascular corrosion casts suggests that the amphibian carotid labyrinth has the appropriate architecture for controlling vascular tone and the findings throughout metamorphosis reveal that the vascular regulatory function begins at an early stage of metamorphosis. In addition, immunohistochemical studies suggest that the vascular regulation in the carotid labyrinth is under peptidergic innervation. Thus, the multiple functions of the carotid labyrinth underline the importance of this relatively small organ for maintenance of homeostasis and appropriate blood supply to the cephalic region.