Peripheral Chemoreceptors in Air- Versus Water- Breathers

Abstract

Among the vertebrates, peripheral chemoreceptors have evolved to play a key role in matching oxygen delivery to the metabolic needs of the body cells and tissues. Specialized neuroepithelial cells (NECs) distributed within the gill filaments and/or lamellae of water-breathers appear to subserve this function by initiating an increase in ventilation in response to lowering of blood or water PO₂ (hypoxia). It is only recently, however, that these cells have become amenable for detailed investigations using electrophysiological tools. By contrast, the well-studied specialized neuroendocrine cells (i.e. glomus or type I cells) located principally in the carotid body of air-breathers initiate a similar reflex ventilatory response to hypoxia so as to maintain blood PO₂ homeostasis. In some species, however, the carotid body is immature and relatively insensitive to hypoxia at birth; it is during this period that their sympathoadrenal counterparts in the adrenal medulla act as key PO₂ receptors, critical for the proper transition to air-breathing life. It is becoming increasingly clear that in general these chemoreceptors act as polymodal receptors, i.e. capable of detecting several sensory modalities including high CO₂/H⁺ or acid hypercapnia. Given the phylogenetic and ontogenetic evidence pointing to homology between the mammalian carotid artery and the first gill arch of teleosts, the question arises whether the mechanisms of chemosensing are conserved among these cell types. This review examines some of the anatomical and functional similarities among these peripheral chemoreceptors, while raising the possibility that the fundamental mechanisms of O₂ and CO₂/H⁺ sensing arose first in water-breathers and are conserved among the vertebrates.