Anaerobiosis in a frog, <i>Rana pipiens</i>

Rose, Francis L.; Drotman, Robert B.

doi:10.1002/jez.1401660314

Cited by 29 publications

(11 citation statements)

References 8 publications

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“…Evidence for this decrease in metabolic costs in the face of hypoxia has been observed in vivo. For example, adult Rana pipiens exposed to anoxia demonstrate a rapid decrease in pulmonary respiratory movements, with respiratory cessation occurring after approximately 30·min of anoxic exposure (Rose and Drotman, 1967). Interestingly, this time course in vivo is nearly identical with the time course of respiratory cessation for postmetamorphic tadpoles and adult bullfrog brainstems in this study (Fig.·2B).…”

Section: Discussionsupporting

confidence: 71%

“…The adult brainstem does not appear to use glycolysis to maintain respiratory activity because the cessation of respiratory activity was identical in hypoxia with or without inhibition of anaerobic metabolism (Fig.·3C). Most adult brainstems exposed to hypoxia with IAA recovered upon reoxygenation, but this differs from the response in vivo where Rana pipiens given IAA died after 20·min exposure to anoxia (Rose and Drotman, 1967). This difference may be due to IAA affecting other organ systems (e.g.…”

Section: Discussionmentioning

confidence: 79%

“…The progressive changes in brain ATP levels and changes in ionic homeostasis are also likely to compromise respiratory motor activity in amphibians, but this has not been examined in any detail. In the adult grass frog Rana pipiens, anoxia results in a progressive decline in respiratory activity and a complete cessation of breathing in about 30·min (Rose and Drotman, 1967).…”

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confidence: 99%

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Development of the respiratory response to hypoxia in the isolated brainstem of the bullfrogRana catesbeiana

Winmill

Chen

Hedrick

2005

Journal of Experimental Biology

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SUMMARY The aim of this study was to examine the effects of cellular hypoxia, and the contribution of anaerobic metabolism, on respiratory activity in bullfrogs at different stages of development. Respiratory-related neural activity was recorded from cranial nerve rootlets in isolated brainstem preparations from pre-metamorphic (Taylor–Köllros (T-K) stages VIII-XVI) and postmetamorphic tadpoles (T-K stages XXIV-XXV) and adults. Changes in fictive gill/lung activity in brainstems from pre-metamorphic tadpoles and lung activity in postmetamorphic tadpoles and adults were examined during superfusion with control (98% O2/2% CO2) or hypoxic (98%N2/2% CO2) artificial cerebrospinal fluid (aCSF). Iodoacetate (IAA; 100 μmol l–1) was used in conjunction with hypoxic aCSF to inhibit glycolysis. Gill burst frequency in pre-metamorphic brainstems did not change over a 3 h exposure to hypoxia and fictive lung burst frequency slowed significantly, but only after 3 h hypoxia. Blockade of glycolysis with IAA during hypoxia significantly reduced the time respiratory activity could be maintained in pre-metamorphic, but not in adult,brainstems. In brainstems from post-metamorphic tadpoles and adults, lung burst frequency became significantly more episodic within 5–15 min hypoxic exposure, but respiratory neural activity was subsequently abolished in every preparation. The cessation of fictive breathing was restored to control levels upon reoxygenation. Neither tadpole nor adult brainstems exhibited changes in neural bursts resembling `gasping' that is observed in mammalian brainstems exposed to severe hypoxia. There was also a significant increase in the frequency of `non-respiratory' bursts in hypoxic postmetamorphic and adult brainstems, but not in pre-metamorphic brainstems. These results indicate that pre-metamorphic tadpoles are capable of maintaining respiratory activity for 3 h or more during severe hypoxia and rely to a great extent upon anaerobic metabolism to maintain respiratory motor output. Upon metamorphosis, however, hypoxia results in significant changes in respiratory frequency and pattern, including increased lung burst episodes,non-ventilatory bursts and a reversible cessation of respiratory activity. Adults have little or no ability to maintain respiratory activity through glycolysis but, instead, stop respiratory activity until oxygen is available. This `switch' in the respiratory response to hypoxia coincides morphologically with the loss of gills and obligate air-breathing in the postmetamorphic frog. We hypothesize that the cessation of respiratory activity in post-metamorphic tadpoles and adults is an adaptive, energy-saving response to low oxygen.

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Section: Discussionsupporting

confidence: 71%

Section: Discussionmentioning

confidence: 79%

mentioning

confidence: 99%

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Development of the respiratory response to hypoxia in the isolated brainstem of the bullfrogRana catesbeiana

Winmill

Chen

Hedrick

2005

Journal of Experimental Biology

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“…Although the use of less severe hypoxia may be more physiologically relevant, we chose this level mainly to reproduce previous in vitro studies (Brockhaus et al, 1993;Winmill et al, 2005). Even so, results obtained in adult bullfrog brainstems were similar to the hypoxic responses reported in intact frogs (Rose and Drotman, 1967), newborn lambs (Dawes et al, 1983;Moore et al, 1996) and newborn rats in vitro (Brockhaus et al, 1993). This protocol allowed us to note that the fictive breathing response to central hypoxia is restricted to lung ventilation as fictive buccal movements were not affected by this stimulus.…”

Section: Critique Of Methodsmentioning

confidence: 97%

“…This ventilatory chemoreflex is well conserved amongst vertebrates, as exposing adult frogs to hypoxia also leads to ventilatory depression (Rose and Drotman, 1967). Furthermore, reducing O 2 levels of the artificial cerebrospinal fluid (aCSF) superfusing in vitro brainstems preparations decreases fictive lung ventilation frequency in Rana catesbeiana (Winmill et al, 2005) and newborn rat (Brockhaus et al, 1993).…”

Section: Introductionmentioning

confidence: 99%