Distribution of acetylcholine and catecholamines in fish gills and their potential roles in the hypoxic ventilatory response

Carotid body glomus cells in mammals contain a plethora of different neurochemicals. Several hypotheses exist to explain their roles in oxygen-chemosensing. In the present study we assessed the distribution of serotonin, acetylcholine and catecholamines in the gills of trout (Oncorhynchus mykiss) and goldfish (Carassius auratus) using immunohistochemistry, and an activity-dependent dye, Texas Red hydrazide (TXR). In fish the putative oxygen sensing cells are neuroepithelial cells (NECs) and the focus in recent studies has been on the role of serotonin in oxygen chemoreception. The NECs of trout and goldfish contain serotonin, but, in contrast to the glomus cells of mammals, not acetylcholine or catecholamines. Acetylcholine was expressed in chain and proximal neurons and in extrinsic nerve bundles in the filaments. The serotonergic NECs did not label with the HNK-1 antibody suggesting that if they are derived from the neural crest, they are no longer proliferative or migrating. Furthermore, we predicted that if serotonergic NECs were chemosensory, they would increase their activity during hypoxia (endocytose TXR), but following 30 min of hypoxic exposure (45 Torr), serotonergic NECs did not take up TXR. Based on these and previous findings we propose several possible models outlining the ways in which serotonin and acetylcholine could participate in oxygen chemoreception in completing the afferent sensory pathway.