The paracrine role of 5-HT in the control of gill blood flow

Abstract

Storage of serotonin in teleost gill cells has been detected in neurons, polymorphous granular cells and in neuroepithelial cells. Innervation from the glossopharyngeal nerve (first gill arch) and the vagus nerve (all gill arches) carries afferent as well as efferent fibers. This innervation extends to the efferent filament artery, including the sphincter muscle associated with the efferent filament artery, but except for the Antarctic fish does not reach the afferent filament artery. Serotonergic nerves as well as neuroepithelial cells have been shown to release serotonin, while very little is known about the polymorphous granular cells. The paracrine action of the released serotonin may affect vascular smooth muscle cells and pillar cells, which also contain contractile filaments. Already the earliest functional studies revealed a severe increase in branchial resistance as a result of serotonin application, combined with an increase in the perfusion of the arterio-venous path and the central sinus spaces of the gills. Pharmacological analysis demonstrated that this is a serotonin specific effect, which in Antarctic fish is due to activation of the 5-HT2 receptor, while inhibition of the 5-HT1 receptor does not reduce the serotonin induced vasoconstriction of gill blood vessels. Hypoxic degranulation of serotonergic cells evoked the hypothesis that serotonergic vasoconstriction might result in more even and overall better perfusion of gill lamellae. Microscopic analysis indicated, however, that perfusion of distal lamellae was reduced after serotonin application. Furthermore, a serotonergic increase in branchial resistance caused a decrease in dorsal arterial oxygen saturation, not an increase as would be expected as a result of a better perfusion of gill lamellae. A detailed analysis of hypoxic effects on gill perfusion revealed that hypoxia induced changes in gill blood flow are due to cholinergic effects, but serotonergic influences could not be detected. These observations contradict the hypothesis that serotonergic vasoconstriction might support hypoxic gas exchange. The functional significance of the serotonergic control of gill blood flow therefore is not yet totally clear. Recent observations indicate that specific inhibitors of serotonin re-uptake accumulate in freshwater and in estuaries. Considering the negative effect of serotonin on arterial blood oxygenation this may become a threat to teleost species.