Adaptive trends in respiratory control: a comparative perspective

Abstract

In 1941, August Krogh published a monograph entitled The Comparative Physiology of Respiratory Mechanisms (Philadelphia, PA: University of Pennsylvania Press, 1941). Since that time comparative studies have continued to contribute significantly to our understanding of the fundamentals of respiratory physiology and the adaptive trends in these processes that support a broad range of metabolic performance under demanding environmental conditions. This review specifically focuses on recent advances in our understanding of adaptive trends in respiratory control. Respiratory rhythm generators most likely arose from, and must remain integrated with, rhythm generators for chewing, suckling, and swallowing. Within the central nervous system there are multiple “segmental” rhythm generators, and through evolution there is a caudal shift in the predominant respiratory rhythm-generating site. All sites, however, may still be capable of producing or modulating respiratory rhythm under appropriate conditions. Expression of the respiratory rhythm is conditional on (tonic) input. Once the rhythm is expressed, it is often episodic as the basic medullary rhythm is turned on/off subject to a hierarchy of controls. Breathing patterns reflect differences in pulmonary mechanics resulting from differences in body wall and lung architecture and are modulated in different species by various combinations of upper and lower airway mechanoreceptors and arterial chemoreceptors to protect airways, reduce dead space ventilation, enhance gas exchange efficiency, and reduce the cost of breathing.

Reversible brain inactivation induces discontinuous gas exchange in cockroaches

“…In vertebrate ectotherms, particularly, these periodic or episodic respiratory patterns appear to be intrinsic to the central nervous system (Douse and Mitchell, 1990;Kinkead et al, 1994). This similarity between the discontinuous gas exchange patterns of insects and vertebrates is even more curious when one considers that the respiratory apparatus of these two groups evolved independently, with the muscles and neural circuits used by insects for ventilation belonging to the thorax and abdomen [predominantly involving the active raising and lowering of the abdominal sterna, and longitudinal telescoping of the abdomen (Miller, 1960)] while those used by vertebrates are associated with the buccal cavity or pharynx, and are innervated by neural circuits derived from those that control feeding movements (Milsom, 2010). The similar respiratory patterns of these two very different groups may hint at common factors constraining the evolution of respiratory systems, or perhaps may simply reflect the limited number of ways in which respiratory rhythms may be produced by pattern generators.…”

Neural mechanisms underlying respiratory rhythm generation in the lamprey

“…In fact, the evolutionary origin of respiratory mechanisms in vertebrates is from structures and pumps initially associated with feeding (Rovainen, 1996;Kardong, 2006;Kinkead, 2009;Milsom, 2010;Taylor et al, 2010). At this stage, the trigeminal motor mechanism plays a prominent role and is the first mover in the respiratory sequence that also involves other cranial motor nuclei.…”

“…From an evolutionary point of view, we should recall that in air-breathing fishes, amphibians, reptiles, birds and mammals the respiratory activity changes progressively from a buccal/branchial ventilation to a ventilation primarily driven by an aspiration pump (Kinkead, 2009;Milsom, 2010;Taylor et al, 2010). Despite the differences displayed by the different species in the pattern of conveying air and in the function of the respiratory muscles, evidence is accumulating that the respiratory rhythm generator within the reticular formation has shifted from a position close to the trigeminal nucleus, that has lost its primary pumping respiratory function, to a location close to the other cranial motor nuclei.…”

Serotonergic neuroepithelial cells of the skin in developing zebrafish: morphology, innervation and oxygen-sensitive properties

“…NaCN is a metabolic poison and acts on chemoreceptors as a potent respiratory stimulant in both mammals and teleosts (González et al, 1992;Sun et al, 1992;. However, because there is no direct evidence for central O 2 or CO 2 chemoreceptors in water-breathing fish (Milsom, 2010a;Milsom, 2010b), the action of NaCN on central chemoreceptors is unlikely. In addition to its effects on chemoreceptors, NaCN may have a wide range of non-specific ) of skin neuroepithelial cells (NECs) in zebrafish is dependent on developmental stage and water P O 2 .…”