Skip to main content
SpringerLink
Log in

Molecular Mechanisms of Carotid Body Afferent Neuron Development

  • Chapter
Response and Adaptation to Hypoxia

Part of the book series: Clinical Physiology Series ((CLINPHY))

Abstract

Peripheral chemoreflexes undergo marked developmental changes in the perinatal period (11, 16, 21, 22, 26, 27, 45). In the fetus, for example, it is generally agreed that the carotid chemoreceptors are relatively ineffective in increasing respiration during hypoxia (11, 14, 27, 45). In neonates, on the other hand, hypoxia produces a transient hyperventilation, followed by a return to normal or below normal levels of ventilation (11, 14, 16, 21, 22, 44, 45). In adults, however, hypoxia evokes a relatively sustained increase in ventilation, primarily by acting on the carotid bodies (17). Although physiologic studies have delineated how chemoreflexes change with development, the underlying cellular and molecular mechanisms remain undefined. What, for example, triggers the emergence of peripheral chemoreflexes after birth? What regulates the transition from a transient to a sustained ventilatory response to hypoxia? Moreover, what can these developmental changes tell us about the underlying plasticity of the neural pathways that mediate peripheral chemoreflexes?

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Acker, H., D. W. Lubbers, M. J. Purves, And E. D. Tan. Measurements of the partial pressure of oxygen in the carotid body of fetal sheep and newborn lambs. J. Devel. Physiol. 2: 323 - 338, 1980.

    CAS  Google Scholar 

  2. Almaraz, L. And S. Fidone. Carotid sinus nerve C-fibers release catecholamines from the cat carotid body. Neurosci. Letts. 67: 153 - 158, 1986.

    Article  CAS  Google Scholar 

  3. Altman, J., And S. Bayer. Development of the cranial nerve ganglia and related nuclei in the rat. Adv. Anat. Embryol. Cell Biol. 74: 1 - 90, 1982.

    Article  PubMed  CAS  Google Scholar 

  4. Ayer-Lelievre, C. S., And A. Seiger. Development of substance P-immunoreactive neurons in cranial sensory ganglia of the rat. Int. J. Devel. Neurosci. 2: 451 - 463, 1984.

    Article  Google Scholar 

  5. Baccaglini, P. I., And E. Cooper. Influences on the expression of acetylcholine receptors on rat nodose neurons in cell culture. J. Physiol. 324: 429 - 439, 1981.

    Google Scholar 

  6. Biscoe, T. J., M. J. Purves, And S. R. Sampson. Types of nervous activity which may be recorded from the carotid sinus nerve in the sheep fetus. J. Physiol. 202:1-23, 1969.

    Google Scholar 

  7. Black, I. B. Regulation of autonomic development. Ann. Reu. Neurosci. 1: 183 - 214, 1978.

    Article  CAS  Google Scholar 

  8. Black, I. B., J. E. Adler, C. F. Dreyfus, W. F. Friedman, E. F. Lagamma, And A. H. Roach. Biochemistry of information storage in the nervous system. Science 236: 1263 - 1268, 1987.

    Article  PubMed  CAS  Google Scholar 

  9. Black, I. B., D. M. Chikaraishi, And E. J. Lewis. Transsynaptic increase in Rna coding for tyrosine hydroxylase in a rat sympathetic ganglion. Br. Res. 339:151-153, 1985.

    Google Scholar 

  10. Blanco, C. E., G. S. Dawes, M. A. Hanson, And H. B. MccooKE. The response to hypoxia of arterial chemoreceptors in fetal sheep and new-born lambs. J. Physiol. (London) 351: 25 - 37, 1984.

    CAS  Google Scholar 

  11. Bryan, A. C., G. Bowes, And J. E. Maloney. Control of breathing in the fetus and the newborn. In: Handbook of Physiology, Vol. II, eds. Cherniack, N. S. and Widdicombe, J. G. Bethesda, MD: American Physiological Society, 1986, pp. 621 - 647.

    Google Scholar 

  12. Bureau M. A., J. Lamarche, P. Foulon, And D. Dalle. The ventilatory response to hypoxia in the newborn lamb after carotid body denervation. Respir. Physiol. 60: 109 - 119, 1985.

    Article  PubMed  CAS  Google Scholar 

  13. Cadieux, A., D. R. Springall, P. K. Mulderry, J. Rodrigo, M. A. Ghatei, G. Terenghi, S. R. Bloom, And J. M. Polak. Occurrence, distribution and ontogeny of Cgrp immunoreactivity in the rat lower respiratory tract: Effect of capsaicin treatment and surgical denervations. Neurosci. 19: 605 - 627, 1986.

    Article  CAS  Google Scholar 

  14. Dawes, G. S. The central control of fetal breathing and skeletal movements. J. Physiol. 346:1-18, 1982.

    Google Scholar 

  15. Dawes, G. S., L. B. Duncan, B. V. Lewis, C. L. Merlet, J. B. Owen-Thomas, And J. T. Reeves. Cyanide stimulation of the systemic arterial chemoreceptors in foetal lambs. J. Physiol. 201: 117 - 128, 1968.

    Google Scholar 

  16. Eden, G. J., And M. A. Hanson. The effect of hypoxia from birth on the biphasic respiratory response of the newborn rat to acute hypoxia. J. Physiol. 366: 59P, 1985.

    Google Scholar 

  17. Fidone, S. J., And C. Gonzales. Initiation and control of chemoreceptor activity in the carotid body. In: Handbook of Physiology, Vol. II, eds. Cherniack, N. S. and Widdicombe, J. G. Bethesda, MD: American Physiological Society, 1986, pp. 247 - 312.

    Google Scholar 

  18. Gaudin-Chazal, G., P. Portalier, M. C. Barrit, And J. J. Puizillout. Serotonin-like immunoreactivity in paraffin-sections of the nodose ganglia of the cat. Neurosci. Letts. 33: 169 - 172, 1982.

    Article  Google Scholar 

  19. Gaudin-Chazal, G., L. Segu, N. Seyfritz, And J. J. Puizillout. Visualization of serotonin neurons in the nodose ganglia of the cat. An autoradiographic study. Neuroscience 6: 1127 - 1137, 1981.

    Article  Google Scholar 

  20. Green, T., And G. J. Dockray. Calcitonin gene-related peptide and substance P in afferents to the upper gastrointestinal tract in the rat. Neurosci. Letts. 76: 151 - 156, 1987.

    Article  CAS  Google Scholar 

  21. Haddad, G. G., And R. B. Mellins. Hypoxia and respiratory control in early life. Ann. Rev. Physiol. 46: 629 - 643, 1984.

    Article  CAS  Google Scholar 

  22. Hanson, M. A. Maturation of the peripheral chemoreceptor and Cns components of respiratory control in perinatal life. In: Neurobiology of the Control of Breathing, eds. Euler, C. von and Lagercrantz, H. New York: Raven Press, 1986, pp. 59 - 65.

    Google Scholar 

  23. Hefti, F., H. Gnahn, M. E. Schwab, And H. Thoenen. Induction of tyrosine hydroxylase by nerve growth factor and by elevated K * concentrations in cultures of dissociated sympathetic neurons. J. Neurosci. 2:1554-1566, 1982.

    Google Scholar 

  24. Helke, C. J., And K.M. Hill. Immunohistochemical study of neuropeptides in vagal and glossopharyngeal afferent neurons in the rat. Neuroscience 26: 539 - 551, 1988.

    Article  PubMed  CAS  Google Scholar 

  25. Hertzberg, T., S. Hellstrom, J.-M. Pequignot, And H. Lagercrantz. Carotid body catecholamines and the development of the arterial chemoreflex in newborn rats. Salt Lake City; Faredrag, August, 1988.

    Google Scholar 

  26. Hertzberg, T., And H. Lagercrantz. Postnatal sensitivity of the peripheral chemoreceptors in newborn infants. Arch. Dis. Child. 62: 1238 - 1241, 1987.

    Article  PubMed  CAS  Google Scholar 

  27. Jansen, A. M., And V. Chernick. Development of respiratory control. Physiol. Rev. 63: 437483, 1983.

    Google Scholar 

  28. Katz, D. M. Expression and regulation of tyrosine hydroxylase in adult sensory neurons in

    Google Scholar 

  29. culture: Effects of elevated potassium and nerve growth factor. Brain Res. 385: 68 - 73, 1986.

    Article  Google Scholar 

  30. Katz, D. M., And M. J. Erb Developmental regulation of tyrosine hydroxylase expression in primary sensory neurons of the rat. Deu. Biol. 137: 233 - 242, 1990.

    Article  CAS  Google Scholar 

  31. Katz, D. M., And I. B. Black. Expression and regulation of catecholaminergic traits in primary sensory neurons: relationship to target innervation in vivo. J. Neurosci. 6: 983 - 989, 1986.

    PubMed  CAS  Google Scholar 

  32. Katz, D. M., And H. J. Karten. Substance P in the vagal sensory ganglia: localization in cell bodies and pericellular arborizations. J. Comp. Neurol. 193: 549 - 564, 1980.

    Article  PubMed  CAS  Google Scholar 

  33. Katz, D. M., K. A. Markey, M. Goldstein, And I. B. Black. Expression of catecholaminergic characteristics by primary sensory neurons in the normal adult rat in vivo. Proc. Natl. Acad. Sci.Us 80: 3526 - 3530, 1983.

    Article  PubMed  CAS  Google Scholar 

  34. Lahiri, S., J. S. Brody, E. K. Motoyama, And T. M. Velasques. Regulation of breathing in newborns at high altitude. J. Appl. Physiol. 44: 673 - 678, 1978.

    PubMed  CAS  Google Scholar 

  35. Lahiri, S., N. Smatresk, M. Pokorski, P. Barnard, A. Mokashi, And K. H. Mcgregor. Dopaminergic efferent inhibition of carotid body chemoreceptors in chronically hypoxic cats. Am. J. Physiol., 247: R24 — R28, 1984.

    PubMed  CAS  Google Scholar 

  36. Lundberg, J. M., T. Hokfelt, G. Nilsson, L. Terenius, J. Rehfeld, R. Elde, And S. Said. Peptide neurons in the vagus, splanchnic and sciatic nerves. Acta Physiol. Scand. 104: 499 - 501, 1978.

    Article  PubMed  CAS  Google Scholar 

  37. Markey, K. A., S. Kondo, And M. Goldstein. Purification and characterization of tyrosine hydroxylase from a clonal pheochromocytoma cell line. Mol. Pharmacol. 17: 79 - 85, 1980.

    PubMed  CAS  Google Scholar 

  38. Mcdonald, D. M., And R. A. Mitchell. The innervation of glomus cells, ganglion cells and blood vessels in the rat carotid body: a quantitative ultrastructural analysis. J. Neurocytol. 4: 177 - 230, 1975.

    Article  Google Scholar 

  39. Mcdonald, D. M., And R. A. Mitchell. The neural pathway involved in "efferent inhibition" of chemoreceptors in the cat carotid body. J. Comp. Neurol. 201: 457 - 476, 1981.

    Article  PubMed  CAS  Google Scholar 

  40. Patterson, P. H. Environmental determination of autonomic neurotransmitter functions. Ann. Rey. Neurosci. 1: 1 - 18, 1978.

    Article  Google Scholar 

  41. Purves, M. J. The effect of a single breath of oxygen on respiration in the newborn lamb. Respir. Physiol. 1: 297 - 307, 1966.

    Article  PubMed  CAS  Google Scholar 

  42. Purves, M. J. The effects of hypoxia in the newborn lamb before and after denervation of the carotid chemoreceptors.. J. Physiol. 185: 60 - 77, 1966.

    PubMed  CAS  Google Scholar 

  43. Purves, M. J. Respiratory and circulatory effects of breathing 100% oxygen in the newborn lamb before and after denervation of the carotid chemoreceptors. J. Physiol. 185: 4259, 1966.

    Google Scholar 

  44. Rigatto, H., J. P. Brady, B. Chir, And R. DE LA Torre Verduzco. Chemoreceptor reflexes in preterm infants. Pediatrics 55: 604 - 613, 1974.

    Google Scholar 

  45. Saetta, M., And J. P. Mortola. Interaction of hypoxic and hypercapnic stimuli on breathing patterns in the newborn rat. J. Appl. Physiol. 62: 506 - 512, 1987.

    PubMed  CAS  Google Scholar 

  46. Walker, D. Peripheral and central chemoreceptors in the fetus and newborn. Ann. Reu. Physiol. 46: 687 - 703, 1984.

    Article  CAS  Google Scholar 

  47. Yoshida, M., Y. Kondo, N. Karasawa, K. Yamada, I. Takagi, And I. Nagatsu. Immunohistocytochemical localization of catecholamine-synthesizing enzymes in suprarenal, superior cervical and nodose ganglia of dogs. Acta Histochem. Cytochem. 14: 588 - 595, 1981.

    Article  CAS  Google Scholar 

  48. Zigmond, R. E., And Y. Ben-Ari. Electrical stimulation of preganglionic nerve increases tyrosine hydroxylase activity in sympathetic ganglia. Proc. Natl. Acad. Sci. (Usa) 74: 3078 - 3080, 1977.

    Article  CAS  Google Scholar 

Download references

Authors
  1. David M. Katz
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Department of Physiology, School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Sukhamay Lahiri

  2. Department of Medicine, Case Western Reserve University and University Hospitals of Cleveland, Cleveland, Ohio, USA

    Neil S. Cherniack

  3. Departments of Environmental Health, Sciences and of Physiology, The Johns Hopkins Medical Institutions, Baltimore, Maryland, USA

    Robert S. Fitzgerald

Rights and permissions

Reprints and permissions

Copyright information

© 1991 American Physiological Society

About this chapter

Cite this chapter

Katz, D.M. (1991). Molecular Mechanisms of Carotid Body Afferent Neuron Development. In: Lahiri, S., Cherniack, N.S., Fitzgerald, R.S. (eds) Response and Adaptation to Hypoxia. Clinical Physiology Series. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7574-3_12

Download citation

  • DOI: https://doi.org/10.1007/978-1-4614-7574-3_12

  • Publisher Name: Springer, New York, NY

  • Online ISBN: 978-1-4614-7574-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation