Oxygen-sensitive Neuroepithelial Cells in the Gills of Aquatic Vertebrates

All vertebrates respond to acute hypoxic stress with reflex cardiorespiratory adjustments initiated by peripheral O2 chemoreceptors. In mammals, these specialized cells are stimulated by hypoxia and lead to activation of sensory nerves, allowing central integration and resulting physiological responses, such as hyperventilation. While the role of O2 chemoreceptors has been well characterized in mammals, relatively little is known about O2 chemoreception in aquatic vertebrates. This chapter reviews the morphological, physiological and developmental studies that have examined the role of O2-sensitive neuroepithelial cells (NECs), which display characteristics similar to mammalian chemoreceptors, and potential chemosensory pathways of the gills in fish and larval amphibians. The gill is a multifunctional organ that receives sensory innervation from the glossopharyngeal or vagus cranial nerves. Extracellular recordings from these nerves provide strong evidence for the gill as a site of O2 chemoreception. NECs of the gill epithelium, most of which contain the neurotransmitter serotonin, are neurosecretory and associated with nerve fibres. In agreement with the membrane hypothesis’, patch-clamp recordings have indicated that NECs isolated from the zebrafish gill respond to acute hypoxia with decreased K+ channel activity and membrane depolarization. Thus, NECs are potential O2 sensors of the gill that may initiate cardiorespiratory reflexes in aquatic vertebrates. The few available studies that have examined O2 sensing in fish have indicated that afunctional system of O2 chemoreception begins to develop before complete formation of the gills, but another extrabranchial site must regulate hypoxic responses during earlier stages. Aquatic vertebrates 2 represent attractive models for pursuing studies of O2 sensing, from cellular mechanisms to behavioural responses. These studies will provide important information about O2 sensing and respiratory regulation in aquatic species, and how this system has evolved in vertebrates. This chapter reviews the morphological and physiological studies that have focused on peripheral O2 chemoreception in the gills of aquatic vertebrates, since these animals have emerged as useful models for studying the evolution of O2 sensing at the cellular level. The gills of aquatic vertebrates are designed to maximize respiratory surface area and gas exchange in an aqueous environment with a low O2 solubility. In fish and aquatic stages of amphibians, these aortic arches course through the pharyngeal arches and provide blood to the gills once they develop. Chronic exposure to hypoxia in fish induces lasting physiological changes that may underlie long-term adaptation to hypoxic environments. Respiratory regulation and sites of gas exchange in aquatic vertebrates change dramatically throughout development. This is due primarily to organogenesis and differentiation of specialized tissues for gas exchange and transport, as well as increases in total body size.