Peripheral chemoreceptors in fish: A brief history and a look ahead

The story of control of cardiorespiratory reflexes by peripheral chemoreceptors includes a chapter on evolution in large part because of the work of Prof. William K. Milsom. Bill has reminded us to think comparatively about O2 and CO2/H+ sensing. We present a brief review of the fish gill and O2 chemoreceptors, as well as recent results from our laboratory, that were discussed at a symposium in honour of Prof. Milsom's extensive career. In a series of papers from the Milsom laboratory from 1986 to 1995, it was demonstrated that the fish gill is a major site of chemosensory discharge during hypoxia, and that this response is sensitive to multiple neurochemicals involved in chemosensing. These and other more recent studies by Bill et al. are now fundamental and have helped to shape the field as it is today. At the cellular level, we have shown that chemosensitive neuroepithelial cells (NECs) of the gills may possess unique adaptations compared to their mammalian homologues. In addition, we used injection of the styryl dye, FM1-43, to identify gill NECs in zebrafish and demonstrate increased vesicular activity in NECs in vitro during acute stimulation. In vivo, we have identified 5-HT2, 5-HT3, dopaminergic and nicotinic receptor activity involved in the hyperventilatory response in developing zebrafish. With this model we have also traced the fate of mitotic cells in the gills, and demonstrated the regeneration of resected gill filaments and replacement of O2-sensitive NECs.