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Evolution and physiology of neural oxygen sensing.

Costa KM, Accorsi-Mendonça D, Moraes DJ, Machado BH - Front Physiol (2014)

Bottom Line: In this review we discuss the concept that regulating O2 homeostasis was one of the primordial roles of the nervous system.We also review the physiology of the peripheral chemoreflex, focusing on the integrative repercussions of chemoreflex activation and the evolutionary importance of this system, which is essential for the survival of complex organisms such as vertebrates.The contribution of hypoxia and peripheral chemoreflex for the development of diseases associated to the cardiovascular and respiratory systems is also discussed in an evolutionary context.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Autonomic and Respiratory Control, Department of Physiology, School of Medicine of Ribeirão Preto, University of São Paulo Ribeirão Preto, Brazil.

ABSTRACT
Major evolutionary trends in animal physiology have been heavily influenced by atmospheric O2 levels. Amongst other important factors, the increase in atmospheric O2 which occurred in the Pre-Cambrian and the development of aerobic respiration beckoned the evolution of animal organ systems that were dedicated to the absorption and transportation of O2, e.g., the respiratory and cardiovascular systems of vertebrates. Global variations of O2 levels in post-Cambrian periods have also been correlated with evolutionary changes in animal physiology, especially cardiorespiratory function. Oxygen transportation systems are, in our view, ultimately controlled by the brain related mechanisms, which senses changes in O2 availability and regulates autonomic and respiratory responses that ensure the survival of the organism in the face of hypoxic challenges. In vertebrates, the major sensorial system for oxygen sensing and responding to hypoxia is the peripheral chemoreflex neuronal pathways, which includes the oxygen chemosensitive glomus cells and several brainstem regions involved in the autonomic regulation of the cardiovascular system and respiratory control. In this review we discuss the concept that regulating O2 homeostasis was one of the primordial roles of the nervous system. We also review the physiology of the peripheral chemoreflex, focusing on the integrative repercussions of chemoreflex activation and the evolutionary importance of this system, which is essential for the survival of complex organisms such as vertebrates. The contribution of hypoxia and peripheral chemoreflex for the development of diseases associated to the cardiovascular and respiratory systems is also discussed in an evolutionary context.

No MeSH data available.


Related in: MedlinePlus

Cardiovascular and respiratory responses to peripheral chemoreflex activation: importance of the carotid body. Activation of the peripheral chemoreflex with environmental hypoxia in intact unanesthetized rats produces a marked increase in pulsatile (PAP) and mean arterial pressure (MAP), a decrease in heart rate (HR) and hyperventilation with forced inspiration and expiration, as can be seen by the strong changes in the eletromyographic (EMG) signals of the abdominal (Abd) and diaphragm (DiA) muscles. In rats that have been subjected to carotid body denervation, the hypertensive, bradycardic and respiratory responses to hypoxia are completely abolished. This fact highlights the essentiality of the peripheral chemoreflex pathway for the cardiorespiratory responses to systemic hypoxia.
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Figure 3: Cardiovascular and respiratory responses to peripheral chemoreflex activation: importance of the carotid body. Activation of the peripheral chemoreflex with environmental hypoxia in intact unanesthetized rats produces a marked increase in pulsatile (PAP) and mean arterial pressure (MAP), a decrease in heart rate (HR) and hyperventilation with forced inspiration and expiration, as can be seen by the strong changes in the eletromyographic (EMG) signals of the abdominal (Abd) and diaphragm (DiA) muscles. In rats that have been subjected to carotid body denervation, the hypertensive, bradycardic and respiratory responses to hypoxia are completely abolished. This fact highlights the essentiality of the peripheral chemoreflex pathway for the cardiorespiratory responses to systemic hypoxia.

Mentions: In mammals, the peripheral chemoreflex is mediated mainly by clusters of specialized oxygen sensitive glomus cells localized in the carotid body and, to a lesser extent, in the aortic arch (Lahiri et al., 1981; Longhurst, 2008). These cells are thought to be homologous to the chemosensitive tissue of other vertebrates (Ishii and Oosaki, 1969; Milsom and Burleson, 2007). Glomus cells have an exponential sensitivity curve to blood oxygen levels (Lahiri et al., 1981; Feldman and McCrimmon, 2008), responding rapidly and intensely as the arterial pO2 decreases to less than 100 Torr. When stimulated by hypoxic conditions, carotid body glomus cells release excitatory neurotransmitters that excite adjacent terminals of the cell bodies located in the petrosal ganglia (Feldman and McCrimmon, 2008). Removal of the carotid body abolishes cardiorespiratory responses to hypoxia, highlighting the crucial role of this sensorial pathway (Figure 3). The physiology of peripheral chemoreceptor cells per se have been recently reviewed elsewhere (Kumar and Prabhakar, 2011). It is important to note that the cells can actually respond to a variety of chemical inputs, leading some authors to classify them as multimodal receptors (Kumar and Prabhakar, 2011). While this is a very interesting concept, both from an evolutionary and physiological point of view, the focus of this review is on the role of peripheral chemoreflex pathways in hypoxia and we will henceforth discuss this particular function.


Evolution and physiology of neural oxygen sensing.

Costa KM, Accorsi-Mendonça D, Moraes DJ, Machado BH - Front Physiol (2014)

Cardiovascular and respiratory responses to peripheral chemoreflex activation: importance of the carotid body. Activation of the peripheral chemoreflex with environmental hypoxia in intact unanesthetized rats produces a marked increase in pulsatile (PAP) and mean arterial pressure (MAP), a decrease in heart rate (HR) and hyperventilation with forced inspiration and expiration, as can be seen by the strong changes in the eletromyographic (EMG) signals of the abdominal (Abd) and diaphragm (DiA) muscles. In rats that have been subjected to carotid body denervation, the hypertensive, bradycardic and respiratory responses to hypoxia are completely abolished. This fact highlights the essentiality of the peripheral chemoreflex pathway for the cardiorespiratory responses to systemic hypoxia.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4129633&req=5

Figure 3: Cardiovascular and respiratory responses to peripheral chemoreflex activation: importance of the carotid body. Activation of the peripheral chemoreflex with environmental hypoxia in intact unanesthetized rats produces a marked increase in pulsatile (PAP) and mean arterial pressure (MAP), a decrease in heart rate (HR) and hyperventilation with forced inspiration and expiration, as can be seen by the strong changes in the eletromyographic (EMG) signals of the abdominal (Abd) and diaphragm (DiA) muscles. In rats that have been subjected to carotid body denervation, the hypertensive, bradycardic and respiratory responses to hypoxia are completely abolished. This fact highlights the essentiality of the peripheral chemoreflex pathway for the cardiorespiratory responses to systemic hypoxia.
Mentions: In mammals, the peripheral chemoreflex is mediated mainly by clusters of specialized oxygen sensitive glomus cells localized in the carotid body and, to a lesser extent, in the aortic arch (Lahiri et al., 1981; Longhurst, 2008). These cells are thought to be homologous to the chemosensitive tissue of other vertebrates (Ishii and Oosaki, 1969; Milsom and Burleson, 2007). Glomus cells have an exponential sensitivity curve to blood oxygen levels (Lahiri et al., 1981; Feldman and McCrimmon, 2008), responding rapidly and intensely as the arterial pO2 decreases to less than 100 Torr. When stimulated by hypoxic conditions, carotid body glomus cells release excitatory neurotransmitters that excite adjacent terminals of the cell bodies located in the petrosal ganglia (Feldman and McCrimmon, 2008). Removal of the carotid body abolishes cardiorespiratory responses to hypoxia, highlighting the crucial role of this sensorial pathway (Figure 3). The physiology of peripheral chemoreceptor cells per se have been recently reviewed elsewhere (Kumar and Prabhakar, 2011). It is important to note that the cells can actually respond to a variety of chemical inputs, leading some authors to classify them as multimodal receptors (Kumar and Prabhakar, 2011). While this is a very interesting concept, both from an evolutionary and physiological point of view, the focus of this review is on the role of peripheral chemoreflex pathways in hypoxia and we will henceforth discuss this particular function.

Bottom Line: In this review we discuss the concept that regulating O2 homeostasis was one of the primordial roles of the nervous system.We also review the physiology of the peripheral chemoreflex, focusing on the integrative repercussions of chemoreflex activation and the evolutionary importance of this system, which is essential for the survival of complex organisms such as vertebrates.The contribution of hypoxia and peripheral chemoreflex for the development of diseases associated to the cardiovascular and respiratory systems is also discussed in an evolutionary context.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Autonomic and Respiratory Control, Department of Physiology, School of Medicine of Ribeirão Preto, University of São Paulo Ribeirão Preto, Brazil.

ABSTRACT
Major evolutionary trends in animal physiology have been heavily influenced by atmospheric O2 levels. Amongst other important factors, the increase in atmospheric O2 which occurred in the Pre-Cambrian and the development of aerobic respiration beckoned the evolution of animal organ systems that were dedicated to the absorption and transportation of O2, e.g., the respiratory and cardiovascular systems of vertebrates. Global variations of O2 levels in post-Cambrian periods have also been correlated with evolutionary changes in animal physiology, especially cardiorespiratory function. Oxygen transportation systems are, in our view, ultimately controlled by the brain related mechanisms, which senses changes in O2 availability and regulates autonomic and respiratory responses that ensure the survival of the organism in the face of hypoxic challenges. In vertebrates, the major sensorial system for oxygen sensing and responding to hypoxia is the peripheral chemoreflex neuronal pathways, which includes the oxygen chemosensitive glomus cells and several brainstem regions involved in the autonomic regulation of the cardiovascular system and respiratory control. In this review we discuss the concept that regulating O2 homeostasis was one of the primordial roles of the nervous system. We also review the physiology of the peripheral chemoreflex, focusing on the integrative repercussions of chemoreflex activation and the evolutionary importance of this system, which is essential for the survival of complex organisms such as vertebrates. The contribution of hypoxia and peripheral chemoreflex for the development of diseases associated to the cardiovascular and respiratory systems is also discussed in an evolutionary context.

No MeSH data available.


Related in: MedlinePlus