Advertisement

Central Hypoxia Elicits Long-Term Expression of the Lung Motor Pattern in Pre-metamorphic Lithobates Catesbeianus

  • Tara A. JanesEmail author
  • Richard Kinkead
Conference paper
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1071)

Abstract

During vertebrate development, the neural networks underlying air-breathing undergo changes in connectivity and functionality, allowing lung ventilation to emerge. Yet, the factors regulating development of these critical homeostatic networks remain unresolved. In amphibians, air-breathing occurs sporadically prior to metamorphosis. However, in tadpoles of Lithobates catesbeianus (American bullfrog), hypoxia stimulates gill and lung ventilation during early development. Because accelerated metamorphosis is a useful strategy to escape deterioration of the milieu, we hypothesized that central hypoxia would elicit long-term expression of the lung motor command for air breathing in pre-metamorphic tadpoles (TK stages VI–XIII). To do this, we recorded respiratory activity from cranial nerves V and VII in isolated brainstems before, during, and up to 2 h after exposure to 15 min of mild (PwO2 range: 114–152 Torr) or moderate (PwO2 range: 38–76 Torr) hypoxia. To test for stage-dependent effects, data were compared between early (VI–IX) and mid (X–XIII) stages. Early stages responded strongly during moderate hypoxia with increased lung burst frequency (167%). Mild and moderate hypoxia increased lung burst frequency during the 2 h re-oxygenation period in early stage brainstems (136%, 497%, respectively), but produced only marginal effects on mid stage brainstems (39%, 31%, respectively). In contrast, hypoxia was not an important factor controlling fictive buccal burst frequency, which drives continuous gill ventilation in tadpoles prior to metamorphosis (all stages showed <25% increase). These preliminary results suggest that central hypoxia elicits long-term increases in lung burst frequency in a severity- and stage-dependent manner.

Keywords

Hypoxia Chemoreflex Respiration Neurodevelopment Amphibian 

Notes

Acknowledgements

This work was supported by a “Discovery Grant” and “Research Tools and Instruments” Grant from the National Sciences and Engineering Research Council of Canada awarded to R.K.

References

  1. Bavis RW, Mitchell GS (2008) Long-term effects of the perinatal environment on respiratory control. J Appl Physiol Bethesda Md 1985 104:1220–1229Google Scholar
  2. Burggren W, Doyle M (1986) Ontogeny of regulation of gill and lung ventilation in the bullfrog, Rana catesbeiana. Respir Physiol 66:279–291CrossRefGoogle Scholar
  3. Burggren WW, Reyna KS (2011) Developmental trajectories, critical windows and phenotypic alteration during cardio-respiratory development. Respir Physiol Neurobiol 178:13–21CrossRefGoogle Scholar
  4. Dawes GS, Gardner WN, Johnston BM, Walker DW (1983) Breathing in fetal lambs: the effect of brain stem section. J Physiol 335:535–553CrossRefGoogle Scholar
  5. Denver RJ (1997) Environmental stress as a developmental cue: corticotropin-releasing hormone is a proximate mediator of adaptive phenotypic plasticity in amphibian metamorphosis. Horm Behav 31:169–179CrossRefGoogle Scholar
  6. Fournier S, Kinkead R (2008) Role of pontine neurons in central O2 chemoreflex during development in bullfrogs (Lithobates catesbeiana). Neuroscience 155:983–996CrossRefGoogle Scholar
  7. Fournier S, Allard M, Roussin S, Kinkead R (2007) Developmental changes in central O2 chemoreflex in Rana catesbeiana: the role of noradrenergic modulation. J Exp Biol 210:3015–3026CrossRefGoogle Scholar
  8. Gourine AV, Funk GD (2017) On the existence of a central respiratory oxygen sensor. J Appl Physiol 123:1344–1349CrossRefGoogle Scholar
  9. Horn EM, Waldrop TG (1997) Oxygen-sensing neurons in the caudal hypothalamus and their role in cardiorespiratory control. Respir Physiol 110:219–228CrossRefGoogle Scholar
  10. Kogo N, Perry SF, Remmers JE (1994) Neural organization of the ventilatory activity in the frog, Rana catesbeiana. I. J Neurobiol 25:1067–1079CrossRefGoogle Scholar
  11. Koos BJ, Chao A, Doany W (1992) Adenosine stimulates breathing in fetal sheep with brain stem section. J Appl Physiol 72:94–99CrossRefGoogle Scholar
  12. Noronha-de-Souza CR, Bícego KC, Michel G, Glass ML, Branco LGS, Gargaglioni LH (2006) Locus coeruleus is a central chemoreceptive site in toads. Am J Physiol Regul Integr Comp Physiol 291:R997–R1006CrossRefGoogle Scholar
  13. Rousseau J-P, Bairam A, Kinkead R (2016) Aldosterone, corticosterone, and thyroid hormone and their influence on respiratory control development in Lithobates catesbeianus: an in vitro study. Respir Physiol Neurobiol 224:104–113CrossRefGoogle Scholar
  14. Sakakibara Y (1984a) The pattern of respiratory nerve activity in the bullfrog. Jpn J Physiol 34:269–282CrossRefGoogle Scholar
  15. Sakakibara Y (1984b) Trigeminal nerve activity and buccal pressure as an index of total inspiratory activity in the bullfrog. Jpn J Physiol 34:827–838CrossRefGoogle Scholar
  16. Smith CA, Forster HV, Blain GM, Dempsey JA (2010) An interdependent model of central/peripheral chemoreception: evidence and implications for ventilatory control. Respir Physiol Neurobiol 173:288–297CrossRefGoogle Scholar
  17. Solomon IC, Edelman NH, Neubauer JA (2000) Pre-Bötzinger complex functions as a central hypoxia chemosensor for respiration in vivo. J Neurophysiol 83:2854–2868CrossRefGoogle Scholar
  18. Straus C, Wilson RJ, Tezenas du Montcel S, Remmers JE (2000) Baclofen eliminates cluster lung breathing of the tadpole brainstem, in vitro. Neurosci Lett 292:13–16CrossRefGoogle Scholar
  19. Straus C, Wilson RJ, Remmers JE (2001) Oxygen sensitive chemoreceptors in the first gill arch of the tadpole, Rana catesbeiana. Can J Physiol Pharmacol 79:959–962CrossRefGoogle Scholar
  20. Taylor AC, Kollros JJ (1946) Stages in the normal development of Rana pipiens larvae. Anat Rec 94:7–13CrossRefGoogle Scholar
  21. Torgerson CS, Gdovin MJ, Remmers JE (1998) Fictive gill and lung ventilation in the pre- and postmetamorphic tadpole brain stem. J Neurophysiol 80:2015–2022CrossRefGoogle Scholar
  22. Wilson RJA, Vasilakos K, Harris MB, Straus C, Remmers JE (2002) Evidence that ventilatory rhythmogenesis in the frog involves two distinct neuronal oscillators. J Physiol 540:557–570CrossRefGoogle Scholar
  23. Wilson RJA, Vasilakos K, Remmers JE (2006) Phylogeny of vertebrate respiratory rhythm generators: the Oscillator Homology Hypothesis. Respir Physiol Neurobiol 154:47–60CrossRefGoogle Scholar
  24. Winmill RE, Chen AK, Hedrick MS (2005) Development of the respiratory response to hypoxia in the isolated brainstem of the bullfrog Rana catesbeiana. J Exp Biol 208:213–222CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of PediatricsUniversité LavalQuébecCanada
  2. 2.Institut Universitaire de Cardiologie et de Pneumologie de QuébecQuébecCanada

Personalised recommendations