The neuroepithelial cells of the fish gill filament: Indolamine‐immunocytochemistry and innervation

Abstract

The neuroepithelial cells (NECs) of the fish gill filament share several morphofunctional features with the cells of the neuroepithelial bodies in the lungs of air-breathing vertebrates. In the present study, a detailed indolamine-immunocytochemical analysis of the branchial neuroepithelial cells and nerves was undertaken in non-teleost and teleost species, with particular emphasis on the latter. In the rainbow trout, Oncorhynchus mykiss, the chemical degeneration of either catecholaminergic (by 5- and 6-hydroxydopamines) or indolaminergic (by 5,6-dihydroxy-tryptamine) innervations associated with the NECs was studied using electron microscopy. In teleosts, the NECs are located primarily on the distal half of the filament. In the trout particularly, these cells are innervated mainly by non-indolaminergic nerves taking up sympathetic neurotoxins. The proximal half of the filament contains isolated NECs innervated additionally by intrinsic indolaminergic neurons. Serotonin-like immunoreactivity of the NECs is evident in the granular vesicles packed within the basal soma and processes which surround non-vascular and vascular smooth muscles in the filament. Apical processes from the neuroepithelial cells occasionally contact the water on the surface of the filament epithelium. The secretory function of the NECs is discussed with reference to the probable involvement of serotonin in the modulation of fish gill function. In addition, their connections with both central and branchial nervous systems suggest a possible chemoreceptor role.

Serotonergic and cholinergic elements of the hypoxic ventilatory response in developing zebrafish

“…Presumably, this change in distribution of non-serotonergic NECs from the gill arches to the filaments reflects a developmental programme. It has been proposed that NECs of the gill filaments that do not express 5-HT may be part of a proliferative population of cells that differentiate into serotonergic NECs (Bailly et al, 1992;Jonz and Nurse, 2003). Similar SV2-positive NECs lacking 5-HT have also been found in the gills of goldfish (Carassius auratus), trout (Oncorhynchus mykiss), trairão (Hoplias lacerdae), traira (Hoplias malabaricus) and larvae of Xenopus laevis (Saltys et al, 2006;Coolidge et al, 2008).…”

Localization of calbindin D28K-like immunoreactivity in fish gill: a light microscopic and immunoelectron histochemical study

“…Calbindin immunopositive cells of the gills qualify as paraneurons based on the basis of their immunohistochemical and ultrastructural characteristics, or as receptosecretory cells -a term proposed very recently by Bailly et al [27].…”

The control of breathing in goldfish (Carassius auratus) experiencing thermally induced gill remodelling

“…The increased ventilation in response to hypoxia arises from the stimulation of externally and/or internally oriented O 2 chemoreceptors, which respond to changes in O 2 partial pressure in the inspired water or the arterial blood, respectively (Saunders and Sutterlin, 1971;Milsom and Brill, 1986;Burleson and Smatresk, 1990) (reviewed by Burleson et al, 1992;Perry et al, 2009b). The neuroepithelial cell (NEC) of the gill filament has long been suspected as the O 2 chemoreceptor of the fish gill (DunelErb et al, 1982;Bailly et al, 1992), based on its structural similarity to the O 2 sensing glomus cell of the mammalian carotid body or pulmonary neuroepithelial bodies (Bailly et al, 1992), and some indirect evidence of its activation during severe hypoxia in trout (Dunel-Erb et al, 1982). More recently, Jonz et al (Jonz et al, 2004) and Burleson et al (Burleson et al, 2006) provided direct electrophysiological evidence that NECs of the zebrafish (Danio rerio) and catfish (Ictalurus punctatus) gill filament behave as O 2 chemoreceptors.…”