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A morphometric analysis of blood vessels and perivascular nerves in the rat carotid body

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Journal of Neurocytology

Summary

This quantitative electron microscopic study was done to develop objective criteria for characterizing different types of blood vessels within the rat carotid body, and then to apply these criteria in an analysis of the distribution of sympathetic and parasympathetic nerves associated with the blood vessels. Some 72% of the 240 vessel profiles analysed were innervated. Half of the perivascular nerve endings were within 1.1 μm of smooth muscle cells, pericytes or endothelial cells of blood vessels and 95% of such nerve endings were within 6 μm of a vessel wall. First to fifth-order branches of the carotid body artery comprised 23% of the vessel profiles. These vessels had a maximal luminal diameter of 57 μm, and had a wall thickness of 2–6 μm. More than 70% of perivascular nerve endings in the carotid body were on vessels of this type. The highest innervation density (37 nerve endings/100 μm of adventitial perimeter) was found on third- to fifth-order arterioles that had a luminal diameter less than 15 μm. By comparison, arterioles exceeding 30 μm in diameter had only 5 nerve endings/100 μm of perimeter. Approximately 75% of nerve endings on arterioles contained exclusively clear-cored synaptic vesicles (SCV-type). The remainder had dense-cored synaptic vesicles (SDV-type).

Some 12% of blood vessel profiles had a wall thickness between 1 and 2 μm. All vessel profiles in this category were less than 14 μm in diameter and had a complete or nearly complete envelopment by smooth muscle cells or pericytes. Most of the smaller vessel profiles (diameter less than 7.5 μm) were terminal arterioles, precapillary sphincters, or the arterial end of small capillaries (type II capillaries as defined by McDonald & Larue, 1983). These vessels lacked endothelial fenestrations and had a high density of innervation (22 nerve endings/100 μm of perimeter). The larger vessel profiles in this category (diameter exceeding 7.5 μm) consisted of precapillary sphincters and the initial portion of large glomerular capillaries (type I capillaries), which together comprised a mixture of nonfenestrated and fenestrated vessels with an average innervation density of 9 nerve endings/100 μm of perimeter.

Blood vessel profiles with a wall thickness less than 1 μm were the most numerous in the carotid body (65% of total). They ranged in size from 3.4 to 28 μm, and consisted of type I and type II capillaries, venous capillaries, postcapillary venules and collecting venules. Some 69% of these vessel profiles were fenestrated. SDV-type and SCV-type nerve endings (in equal proportions) were associated with more than 60% of these thin-walled vessels (mean density=4 nerve endings/100 μm of perimeter). Axonal varicosities were located within 0.5 μm of pericytes and endothelial cells of some capillaries and venules. The 70% of these vessel profiles located within 3 μm of glomus cells (predominantly capillaries) had thinner walls, more fenestrations and fewer nerves than other vessels (predominantly venules) in this category. We conclude that sympathetic and parasympathetic nerves can affect all segments of the vascular bed in the carotid body, but their greatest influence is at the level of third- to fifth-order arterioles and precapillary sphincters that control blood flow through two types of capillaries and through arteriovenous anastomoses.

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McDonald, D.M. A morphometric analysis of blood vessels and perivascular nerves in the rat carotid body. J Neurocytol 12, 155–199 (1983). https://doi.org/10.1007/BF01148091

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