William K. Milsom

During hibernation, golden-mantled ground squirrels (Spermophilus lateralis) breathe in distinct multi-breath episodes separated by prolonged periods of apnea. We hypothesized that vagal afferent feedback from pulmonary stretch receptors, and N-methyl-D-aspartate (NMDA) type glutamate receptor-mediated processes in the pons are instrumental in the production of this breathing pattern and analyzed the effects of disrupting vagal feedback, and blockade of NMDA type receptors by the non-competitive antagonist (+)-5-methyl-10,11-dihydro-5 H-dibenzo[a, d]-cyclohepten-5,10-imine maleate (MK-801), on breathing pattern and ventilatory responses to hypoxia and hypercapnia in ground squirrels during natural hibernation. The hibernating squirrels breathed episodically and exhibited a robust ventilatory response to hypercapnia but not hypoxia. The breathing episode (not the individual breath) was the major regulated variable in the breathing pattern. Vagal blockade did not alter breathing on a breath-by-breath basis but did decrease the breaths per episode decreasing overall ventilation and abolished the hypercapnic ventilatory response. MK-801 increased the number of breaths per episode and the frequency of breathing during episodes but did not alter overall ventilation nor the hypercapnic ventilatory response. Combined treatment with MK-801 and vagal blockade abolished episodic breathing but also initiated arousal from hibernation. The data suggest that in golden-mantled ground squirrels hibernating at 5°C body temperature, vagal feedback and NMDA receptor mediated processes still modulate breathing. Whether they are responsible for clustering breaths into episodes is suggested but remains equivocal.

High-altitude life poses physiological challenges to all animals due to decreased environmental oxygen (O ₂ ) availability (hypoxia) and cold. Supporting high metabolic rates and body temperatures with limited O ₂ is challenging. Many birds, however, thrive at high altitudes. The O ₂ -transport cascade describes the pathway involved in moving O ₂ from the environment to the tissues encompassing: (i) ventilation, (ii) pulmonary O ₂ diffusion, (iii) circulation, (iv) tissue O ₂ diffusion, and (v) mitochondrial O ₂ use for ATP production. Shared avian traits such as rigid lungs with cross-current gas exchange and unidirectional airflow aid in O ₂ acquisition and transport in all birds. Many high-altitude birds, however, have evolved enhancements to some or all steps in the cascade. In this review, we summarize the current literature on gas exchange and O ₂ transport in high-altitude birds, providing an overview of the O ₂ -transport cascade that principally draws on the literature from high-altitude waterfowl, the most well-studied group of high-altitude birds. We close by discussing two important avenues for future research: distinguishing between the influences of plasticity and evolution and investigating whether the morphological and physiological differences discussed contribute to enhanced locomotor or thermogenic performance, a potential critical link to fitness. This article is part of the theme issue ‘The biology of the avian respiratory system’.

The dive response involves three main components – breath holding, reduced heart rate and increased peripheral vasoconstriction – and is ubiquitous during forced dives in air-breathing vertebrates; however, numerous studies in free-diving animals have shown that the heart rate response to diving varies considerably in a manner that suggests cognitive control. Furthermore, studies on free-diving animals and controlled experiments in trained animals both indicate that the dive response can be conditioned, such that the reduction in heart rate begins before submergence and the extent of the reduction is set early in the dive. In addition, numerous species also experience an increase in heart rate and blood flow during ascent at the end of a dive, a phenomenon commonly called ‘ascent tachycardia’. Collectively, these data suggest that although the dive response is under autonomic control, many species can vary its magnitude depending on the length and type of the planned dive – an indication of a role for cognition in the overall physiological responses associated with diving. Here, we provide examples of the conditioned cardiac responses – including anticipatory changes in heart rate – in several diving species and propose potential underlying mechanisms. We also discuss how the anticipatory cardiovascular responses not only improve diving capacity, but also prevent diving-related problems, such as decompression sickness or barotrauma, through a mechanism described by the selective gas exchange hypothesis.

In this review, we explore the inconsistencies in the data and gaps in our knowledge that exist in what is currently known regarding gill chemosensors which drive the cardiorespiratory reflexes in fish. Although putative serotonergic neuroepithelial cells (NEC) dominate the literature, it is clear that other neurotransmitters are involved (adrenaline, noradrenaline, acetylcholine, purines, and dopamine). And although we assume that these agents act on neurons synapsing with the NECs or in the afferent or efferent limbs of the paths between chemosensors and central integration sites, this process remains elusive and may explain current discrepancies or species differences in the literature. To date it has been impossible to link the distribution of NECs to species sensitivity to different stimuli or fish lifestyles and while the gills have been shown to be the primary sensing site for respiratory gases, the location (gills, oro-branchial cavity or elsewhere) and orientation (external/water or internal/blood sensing) of the NECs are highly variable between species of water and air breathing fish. Much of what has been described so far comes from studies of hypoxic responses in fish, however, changes in CO₂, ammonia and lactate have all been shown to elicit cardio-respiratory responses and all have been suggested to arise from stimulation of gill NECs. Our view of the role of NECs is broadening as we begin to understand the polymodal nature of these cells. We begin by presenting the fundamental picture of gill chemosensing that has developed, followed by some key unanswered questions about gill chemosensing in general.

Many animal species do not breathe in a continuous, rhythmic fashion, but rather display a variety of breathing patterns characterized by prolonged periods between breaths (inter‐breath intervals), during which the heart continues to beat. Examples of intermittent breathing abound across the animal kingdom, from crustaceans to cetaceans. With respect to human physiology, intermittent breathing—also termed ‘periodic’ or ‘episodic’ breathing—is associated with a variety of pathologies. Cardiovascular phenomena associated with intermittent breathing in diving species have been termed ‘diving bradycardia’, ‘submersion bradycardia’, ‘immersion bradycardia’, ‘ventilation tachycardia’, ‘respiratory sinus arrhythmia’ and so forth. An examination across the literature of terminology applied to these physiological phenomena indicates, unfortunately, no attempt at standardization. This might be viewed as an esoteric semantic problem except for the fact that many of the terms variously used by different authors carry with them implicit or explicit suggestions of underlying physiological mechanisms and even human‐associated pathologies. In this article, we review several phenomena associated with diving and intermittent breathing, indicate the semantic issues arising from the use of each term, and make recommendations for best practice when applying specific terms to particular cardiorespiratory patterns. Ultimately, we emphasize that the biology—not the semantics—is what is important, but also stress that confusion surrounding underlying mechanisms can be avoided by more careful attention to terms describing physiological changes during intermittent breathing and diving.

This book covers broad grounds: The origins of hypoxia adaptation, the impact of oxygen on circulatory transition at birth, the biochemistry of hypoxia in the pulmonary circulation and the diagnosis and clinical management of hypoxic respiratory failure. In other words: What we once were; why we have been protected; what happens when that protection is lifted; how to diagnose when we have entered the maelstrom; what to do next, and what we still don't know.