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.

A comparative analysis of putative oxygen-sensing cells in the fish gill.

We investigated the distribution of serotonin (5-HT)-containing neuroepithelial cells (NECs), the putative O(2) sensing cells, in the gills of four species of fish: trout (Oncorhynchus mykiss), goldfish (Carassius auratus), trairão (Hoplias lacerdae) and traira (Hoplias malabaricus) using immunohistochemical markers for 5-HT, synaptic vesicles and neural innervation. We found that all fish had a cluster of innervated, serotonergic NECs at the filament tips, but there were species-specific distributions of serotonin-containing NECs within the primary gill filaments. Trout gill filaments had a greater number of serotonin-containing NECs than both trairão and traira, whereas goldfish primary filaments had none. Serotonin-containing NECs in the secondary lamellae were most numerous in goldfish, present in trairão and traira, but absent in trout. Those found in the primary filament were generally associated with the efferent filamental artery. Innervated, serotonin-containing cells (NECs or Merkel-like cells) were also found in the gill rakers of trout and goldfish although vesicular serotonin was only found in the gill rakers of goldfish. These differences in serotonergic NEC distribution appear to reflect paracrine versus chemoreceptive roles related to hypoxia tolerance in the different fish species.