Prenatal development of respiratory chemoreceptors in endothermic vertebrates

Hempleman, Steven C.; Pilarski, Jason Q.

doi:10.1016/j.resp.2011.04.027

Cited by 14 publications

(6 citation statements)

References 63 publications

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“…In addition to more uniform and robust CO 2 responsiveness, postmetamorphic tadpoles exhibit a central hypoxic ventilatory depression (HVD) that is absent in early-stage tadpoles (Winmill et al 2005;Fournier et al 2007). Similar trends seem to exist in rats and mice since ventilatory responses to CO 2 challenge and central HVD increase throughout pre-and postnatal development (Saiki & Mortola, 1996;Ramirez et al 1997;Viemari et al 2003;Davis et al 2006;Huang et al 2010;Hempleman & Pilarski, 2011;Ramanantsoa et al 2011). Appearance of ventilatory control through central chemosensing during development seems to have adaptive advantages for controlling breathing during acid-base disturbances, providing a drive to breathe, and maintaining energy homeostasis in air-breathing vertebrates (Milsom, 2002;Winmill et al 2005;Milsom, 2010;Guyenet & Bayliss, 2015).…”

Section: Aquatic Overwintering Eliminates Hypercapnic and Hypoxia Senmentioning

confidence: 97%

Environmentally induced return to juvenile‐like chemosensitivity in the respiratory control system of adult bullfrog, Lithobates catesbeianus

Santin

Hartzler

2016

The Journal of Physiology

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Key pointsr The degree to which developmental programmes or environmental signals determine physiological phenotypes remains a major question in physiology.r Vertebrates change environments during development, confounding interpretation of the degree to which development (i.e. permanent processes) or phenotypic plasticity (i.e. reversible processes) produces phenotypes.r Tadpoles mainly breathe water for gas exchange and frogs may breathe water or air depending on their environment and are, therefore, exemplary models to differentiate the degree to which life-stage vs. environmental context drives developmental phenotypes associated with neural control of lung breathing.r Using isolated brainstem preparations and patch clamp electrophysiology, we demonstrate that adult bullfrogs acclimatized to water-breathing conditions do not exhibit CO 2 and O 2 chemosensitivity of lung breathing, similar to water-breathing tadpoles.r Our results establish that phenotypes associated with developmental stage may arise from plasticity per se and suggest that a developmental trajectory coinciding with environmental change obscures origins of stage-dependent physiological phenotypes by masking plasticity.Abstract An unanswered question in developmental physiology is to what extent does the environment vs. a genetic programme produce phenotypes? Developing animals inhabit different environments and switch from one to another. Thus a developmental time course overlapping with environmental change confounds interpretations as to whether development (i.e. permanent processes) or phenotypic plasticity (i.e. reversible processes) generates phenotypes. Tadpoles of the American bullfrog, Lithobates catesbeianus, breathe water at early life-stages and minimally use lungs for gas exchange. As adults, bullfrogs rely on lungs for gas exchange, but spend months per year in ice-covered ponds without lung breathing. Aquatic submergence, therefore, removes environmental pressures requiring lung breathing and enables separation of adulthood from environmental factors associated with adulthood that necessitate control of lung ventilation. To test the hypothesis that postmetamorphic respiratory control phenotypes arise through permanent developmental changes vs. reversible environmental signals, we measured respiratory-related nerve discharge in isolated brainstem preparations and action potential firing from CO 2 -sensitive neurons in bullfrogs acclimatized to semi-terrestrial (air-breathing) and aquatic-overwintering (no air-breathing) habitats. We found that aquatic overwintering significantly reduced neuroventilatory responses to CO 2 and O 2 involved in lung breathing. Strikingly, this gas sensitivity profile reflects that of water-breathing tadpoles. We further demonstrated that aquatic overwintering reduced CO 2 -induced firing responses of chemosensitive neurons. In contrast, respiratory rhythm generating processes remained adult-like after submergence. Our results establish that phenotypes associated with life-stage can arise from phenotyp...

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Section: Aquatic Overwintering Eliminates Hypercapnic and Hypoxia Senmentioning

confidence: 97%

Environmentally induced return to juvenile‐like chemosensitivity in the respiratory control system of adult bullfrog, Lithobates catesbeianus

Santin

Hartzler

2016

The Journal of Physiology

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“…The ventilatory response to CO 2 of vertebrates undergoes significant changes during early life (Eugenín et al, 2006;Hempleman and Pilarski, 2011;Putnam et al, 2005;Whitaker-Fornek et al, 2019). In rodents, the response is greatest at birth and then declines to nearly undetectable values near postnatal day 5; it Fig.…”

Section: Discussionmentioning

confidence: 99%

“…then rises progressively until postnatal day 15 and then stabilizes until adulthood (Hempleman and Pilarski, 2011;Putnam et al, 2005). In birds, the response is complex; depending on the embryonic stage, acidosis and alkalosis can both stimulate fictive breathing (Whitaker-Fornek et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

Orexin-A inhibits fictive air breathing responses to respiratory stimuli in the bullfrog tadpole (Lithobates catesbeianus)

Fonseca

Janes

Fournier

et al. 2021

Journal of Experimental Biology

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In pre-metamorphic tadpoles, the neural network generating lung ventilation is present but actively inhibited; the mechanisms leading to the onset of air breathing are not well understood. Orexin (ORX) is a hypothalamic neuropeptide that regulates several homeostatic functions, including breathing. While ORX has limited effects on breathing at rest, it potentiates reflexive responses to respiratory stimuli mainly via ORX receptor 1 (OX1Rs). Here, we tested the hypothesis that OXR1 facilitate the expression of the motor command associated with air breathing in pre-metamorphic bullfrog tadpoles (Lithobates catesbeianus). To do so, we used an isolated diencephalic-brainstem preparation to determine the contributions of OX1Rs to respiratory motor output during baseline breathing, hypercapnia, and hypoxia. A selective OX1R antagonist (SB-334867; 5 – 25 µM) or agonist (ORX-A; 200 nM-1 µM) was added to the superfusion media. Experiments were performed under basal conditions (media equilibrated with 98.2% O2+1.8% CO2), hypercapnia (5% CO2) or hypoxia (5-7% O2). Under resting conditions gill, but not lung, motor output was enhanced by the OX1R antagonist and ORX-A. Hypercapnia alone did not stimulate respiratory motor output, but its combination with SB-334867 increased lung burst frequency and amplitude, lung burst episodes, and the number of bursts/episode. Hypoxia alone increased lung burst frequency and its combination with SB-334867 enhanced this effect. Inactivation of OX1Rs during hypoxia also increased gill burst amplitude, but not frequency. In contrast with our initial hypothesis, we conclude that ORX neurons provide inhibitory modulation of the CO2 and O2 chemoreflexes in pre-metamorphic tadpoles.

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“…These findings have been summarized in several recent reviews and will not be discussed in depth here (De Caro et al, 2012; Hempleman and Pilarski, 2011; Hempleman and Warburton, 2012). With respect to postnatal O 2 response maturation, the important questions are whether ultrastructural changes occur after birth and, if so, do they contribute to functional, postnatal maturation of O 2 sensing.…”

Section: 0 Structural Factors In Cb Functional Resettingmentioning

confidence: 99%

Carotid chemoreceptor “resetting” revisited

Carroll

Kim

2013

Respiratory Physiology & Neurobiology

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Carotid body (CB) chemoreceptors transduce low arterial O2 tension into increased action potential activity on the carotid sinus nerves, which contributes to resting ventilatory drive, increased ventilatory drive in response to hypoxia, arousal responses to hypoxia during sleep, upper airway muscle activity, blood pressure control and sympathetic tone. Their sensitivity to O2 is low in the newborn and increases during the days or weeks after birth to reach adult levels. This postnatal functional maturation of the CB O2 response has been termed “resetting” and it occurs in every mammalian species studied to date. The O2 environment appears to play a key role; the fetus develops in a low O2 environment throughout gestation and initiation of CB “resetting” after birth is modulated by the large increase in arterial oxygen tension occurring at birth. Although numerous studies have reported age-related changes in various components of the O2 transduction cascade, how the O2 environment shapes normal CB prenatal development and postnatal “resetting” remains unknown. Viewing CB “resetting” as environment-driven (developmental) phenotypic plasticity raises important mechanistic questions that have received little attention. This review examines what is known (and not known) about mechanisms of CB functional maturation, with a focus on the role of the O2 environment.

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Prenatal development of respiratory chemoreceptors in endothermic vertebrates

Cited by 14 publications

References 63 publications

Environmentally induced return to juvenile‐like chemosensitivity in the respiratory control system of adult bullfrog, Lithobates catesbeianus

Environmentally induced return to juvenile‐like chemosensitivity in the respiratory control system of adult bullfrog, Lithobates catesbeianus

Orexin-A inhibits fictive air breathing responses to respiratory stimuli in the bullfrog tadpole (Lithobates catesbeianus)

Carotid chemoreceptor “resetting” revisited

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