Developmental disinhibition: Turning off inhibition turns on breathing in vertebrates

Straus, Christian; Wilson, Richard J. A.; Remmers, John E.

doi:10.1002/1097-4695(20001105)45:2<75::aid-neu2>3.0.co;2-5

Cited by 48 publications

(29 citation statements)

References 27 publications

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“…As Straus and colleagues mentioned in their discussion, this 'developmental disinhibition' may act via reductions in excitation, if the excitation (by exciting a functionally inhibitory pathway) leads to the suppression of behaviours (Straus et al, 2000). This interpretation is supported by the present work and results obtained in rats showing that the transition from excitatory to inhibitory is an important mechanism in the maturation of respiratory rhythmogenesis (Ren and Greer, 2006).…”

Section: Mechanisms Of Action Of Corticosteronesupporting

confidence: 81%

“…To ensure a successful transition from water to air breathing, such changes must occur within the neural networks that generate and regulate the act of breathing. While the anatomical and functional reorganisation of the respiratory control system of bullfrogs has been detailed elegantly Straus et al, 2000;Vasilakos et al, 2006;Wilson et al, 2002), the mechanism responsible for initiating such changes is unknown. Environmental cues trigger the secretion of several hormones including thyroxin and corticosterone.…”

Section: Conclusion and Perspectivementioning

confidence: 99%

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Corticosterone promotes emergence of fictive air breathing in Xenopus laevis Daudin tadpole brainstems

Fournier

Dubé

Kinkead

2012

Journal of Experimental Biology

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SUMMARY The emergence of air breathing during amphibian metamorphosis requires significant changes to the brainstem circuits that generate and regulate breathing. However, the mechanisms controlling this developmental process are unknown. Because corticosterone plays an important role in the neuroendocrine regulation of amphibian metamorphosis, we tested the hypothesis that corticosterone augments fictive air breathing frequency in Xenopus laevis. To do so, we compared the fictive air breathing frequency produced by in vitro brainstem preparations from pre-metamorphic tadpoles and adult frogs before and after 1 h application of corticosterone (100 nmol l–1). Fictive breathing measurements related to gill and lung ventilation were recorded extracellularly from cranial nerve rootlets V and X. Corticosterone application had no immediate effect on respiratory-related motor output produced by brainstems from either developmental stage. One hour after corticosterone wash out, fictive lung ventilation frequency was increased whereas gill burst frequency was decreased. This effect was stage specific as it was significant only in preparations from tadpoles. GABA application (0.001–0.5 mmol l–1) augmented fictive air breathing in tadpole preparations. However, this effect of GABA was no longer observed following corticosterone treatment. An increase in circulating corticosterone is one of the endocrine processes that orchestrate central nervous system remodelling during metamorphosis. The age-specific effects of corticosterone application indicate that this hormone can act as an important regulator of respiratory control development in Xenopus tadpoles. Concurrent changes in GABAergic neurotransmission probably contribute to this maturation process, leading to the emergence of air breathing in this species.

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Section: Mechanisms Of Action Of Corticosteronesupporting

confidence: 81%

Section: Conclusion and Perspectivementioning

confidence: 99%

Corticosterone promotes emergence of fictive air breathing in Xenopus laevis Daudin tadpole brainstems

Fournier

Dubé

Kinkead

2012

Journal of Experimental Biology

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“…Further, hypercapnia stimulates lung burst activity but not gill bursting activity (Taylor et al, 2003a,b). Lung bursts are infrequent in the early stages of metamorphosis, but they seem to be actively inhibited, since a combination of bicuculline and strychnine (antagonists of GABA and glycine) increased the frequency of lung bursts even in the early stages of metamorphosis (Straus et al, 2000). The effect of inhibition of GABAergic mechanisms is similar in tadpoles and in neonatal mice (Bissonnette and Knopp, 2004) in that the frequency response is unleashed.…”

Section: Developmental Patterns In Non-mammalsmentioning

confidence: 99%

Neonatal maturation of the hypercapnic ventilatory response and central neural CO2 chemosensitivity

Putnam

Conrad

Gdovin

et al. 2005

Respiratory Physiology & Neurobiology

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The ventilatory response to CO 2 changes as a function of neonatal development. In rats, a ventilatory response to CO 2 is present in the first 5 days of life, but this ventilatory response to CO 2 wanes and reaches its lowest point around postnatal day 8. Subsequently, the ventilatory response to CO 2 rises towards adult levels. Similar patterns in the ventilatory response to CO 2 are seen in some other species, although some animals do not exhibit all of these phases. Different developmental patterns of the ventilatory response to CO 2 may be related to the state of development of the animal at birth. The triphasic pattern of responsiveness (early decline, a nadir, and subsequent achievement of adult levels of responsiveness) may arise from the development of several processes, including central neural mechanisms, gas exchange, the neuromuscular junction, respiratory muscles and respiratory mechanics. We only discuss central neural mechanisms here, including altered CO 2 sensitivity of neurons among the various sites of central CO 2 chemosensitivity, changes in astrocytic function during development, the maturation of electrical and chemical synaptic mechanisms (both inhibitory and excitatory mechanisms) or changes in the integration of chemosensory information originating from peripheral and multiple central CO 2 chemosensory sites. Among these central processes, the maturation of synaptic mechanisms seems most important and the relative maturation of synaptic processes may also determine how plastic the response to CO 2 is at any particular age.

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“…These motor rhythms consist almost entirely of lung and buccal bursts that are clearly visible on the neurograms from cranial nerves. The buccal and the lung oscillators, located in the brainstem, are coupled but physiologically and anatomically distinct (20,52,63,66). The first governs gill or buccal ventilation, according to the developmental stage, while the other drives lung ventilation.…”

mentioning

confidence: 99%

Effects of maturation and acidosis on the chaos-like complexity of the neural respiratory output in the isolated brainstem of the tadpole,Rana esculenta

Straus

Samara²,

Fiamma³

et al. 2011

American Journal of Physiology-Regulatory, Integrative and Comp

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Human ventilation at rest exhibits mathematical chaos-like complexity that can be described as long-term unpredictability mediated (in whole or in part) by some low-dimensional nonlinear deterministic process. Although various physiological and pathological situations can affect respiratory complexity, the underlying mechanisms remain incompletely elucidated. If such chaos-like complexity is an intrinsic property of central respiratory generators, it should appear or increase when these structures mature or are stimulated. To test this hypothesis, we employed the isolated tadpole brainstem model [ Rana ( Pelophylax) esculenta] and recorded the neural respiratory output (buccal and lung rhythms) of pre- ( n = 8) and postmetamorphic tadpoles ( n = 8), at physiologic (7.8) and acidic pH (7.4). We analyzed the root mean square of the cranial nerve V or VII neurograms. Development and acidosis had no effect on buccal period. Lung frequency increased with development ( P < 0.0001). It also increased with acidosis, but in postmetamorphic tadpoles only ( P < 0.05). The noise-titration technique evidenced low-dimensional nonlinearities in all the postmetamorphic brainstems, at both pH. Chaos-like complexity, assessed through the noise limit, increased from pH 7.8 to pH 7.4 ( P < 0.01). In contrast, linear models best fitted the ventilatory rhythm in all but one of the premetamorphic preparations at pH 7.8 ( P < 0.005 vs. postmetamorphic) and in four at pH 7.4 (not significant vs. postmetamorphic). Therefore, in a lower vertebrate model, the brainstem respiratory central rhythm generator accounts for ventilatory chaos-like complexity, especially in the postmetamorphic stage and at low pH. According to the ventilatory generators homology theory, this may also be the case in mammals.

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Developmental disinhibition: Turning off inhibition turns on breathing in vertebrates

Cited by 48 publications

References 27 publications

Corticosterone promotes emergence of fictive air breathing in Xenopus laevis Daudin tadpole brainstems

Corticosterone promotes emergence of fictive air breathing in Xenopus laevis Daudin tadpole brainstems

Neonatal maturation of the hypercapnic ventilatory response and central neural CO2 chemosensitivity

Effects of maturation and acidosis on the chaos-like complexity of the neural respiratory output in the isolated brainstem of the tadpole,Rana esculenta

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