Respiratory chemoreceptor function in vertebrates comparative and evolutionary aspects

Abstract

The sensing of blood gas tensions and/or pH is an evolutionarily conserved, homeostatic mechanism, observable in almost all species studied from invertebrates to man. In vertebrates, a shift from the peripheral O(2)-oriented sensing in fish, to the central CO(2)/pH sensing in most tetrapods reflects the specific behavioral requirements of these two groups whereby, in teleost fish, a highly O(2)-oriented control of breathing matches the ever-changing and low oxygen levels in water, whilst the transition to air-breathing increased the importance of acid-base regulation and O(2)-related drive, although retained, became relatively less important. The South American lungfish and tetrapods are probably sister groups, a conclusion backed up by many similar features of respiratory control. For example, the relative roles of peripheral and central chemoreceptors are present both in the lungfish and in land vertebrates. In both groups, the central CO(2)/pH receptors dominate the ventilatory response to hypercarbia (60-80%), while the peripheral CO(2)/pH receptors account for 20-30%. Some basic components of respiratory control have changed little during evolution. This review presents studies that reflect the current trends in the field of chemoreceptor function, and several laboratories are involved. An exhaustive review on the previous literature, however, is beyond the intended scope of the article. Rather, we present examples of current trends in respiratory function in vertebrates, ranging from fish to humans, and focus on both O(2) sensing and CO(2) sensing. As well, we consider the impact of chronic levels of hypoxia-a physiological condition in fish and in land vertebrates resident at high elevations or suffering from one of the many cardiorespiratory disease states that predispose an animal to impaired ventilation or cardiac output. This provides a basis for a comparative physiology that is informative about the evolution of respiratory functions in vertebrates and about human disease. Currently, most detail is known for mammals, for which molecular biology and respiratory physiology have combined in the discovery of the mechanisms underlying the responses of respiratory chemoreceptors. Our review includes new data on nonmammalian vertebrates, which stresses that some chemoreceptor sites are of ancient origin.

Evolution and physiology of neural oxygen sensing

“…All animals, including very primitive life forms such as jellyfish and nematodes, exhibit at least some form of behavioral response to reduced oxygen levels, which usually drives the organism to relocate to an environment with an adequate supply of O 2 and produces physiological changes so as to maximize energy expenditure efficiency (Guyenet and Koshiya, 1995; Cheung et al, 2005; Hetz and Bradley, 2005; Thuesen et al, 2005; Fisher and Burggren, 2007). In animals with differentiated respiratory systems, such as insects and vertebrates, hypoxia not only evokes marked behavioral responses, but also produces changes in respiratory movements and autonomic adjustments in order to keep ideal blood flow and cellular oxygen supply (Holeton and Randall, 1967; Guyenet and Koshiya, 1995; Taylor et al, 1999; Hetz and Bradley, 2005; Vermehren et al, 2006; Sundin et al, 2007). …”

“…The need for an effective and integrative oxygen regulation mechanism has likely been one of the major driving forces in the evolution of the brain. This hypothesis makes even more sense when we consider that early life forms evolved in an aquatic environment, where O 2 levels vary greatly in relation to variables such as depth, temperature and salinity (Weiss, 1970; Childress and Seibel, 1998; Sundin et al, 2007). …”

“…In vertebrates, the CNS constantly generates and regulates the neural activity of the cardiovascular and respiratory systems in response to intrinsic or extrinsic alterations, such as high levels of exercise, the sleep-wake cycle and, of course, environmental hypoxia (Taylor et al, 1999; Sundin et al, 2007). The respiratory system indeed cannot function without constant input from CNS networks that generate the rhythmic motor activity of breathing (Smith et al, 1991; Abdala et al, 2009b).…”

“…All studied vertebrates exhibit some form of specialized peripheral oxygen chemoreflex (De Burgh Daly, 1997; Milsom and Burleson, 2007; Sundin et al, 2007). In fish, the transduction of blood oxygen level signals is performed by neuroepithelial cells located in vessels positioned all across the respiratory passages, especially in the gills, the primary sites of oxygen absorption in most species (Milsom and Burleson, 2007; Sundin et al, 2007; Jonz and Nurse, 2012).…”

Effect of temperature on chemosensitive locus coeruleus neurons of Savannah monitor lizardsVaranus exanthematicus

“…Animals primarily compensate for perturbations to acid-base status of metabolic origin by adjusting the depth and rhythm of breathing through a negative feedback loop where O 2 , CO 2 and pH are the main signals for ventilatory adjustments (Sundin et al, 2007). The negative feedback system that drives ventilation has been mainly elucidated in mammals that tightly regulate arterial pH.…”