Intrapulmonary Carbon Dioxide Sensitive Receptors: Amphibians to Mammals

  • M. R. Fedde
  • W. D. Kuhlmann
Part of the Proceedings in Life Sciences book series (LIFE SCIENCES)

Summary

Direct neural recordings have been made from intrapulmonary CO2-sensitive receptors in all classes of tetrapods. Specific characteristics of these receptors, such as their relative sensitivity to chemical (CO2, O2, and several drugs) and mechanical stimuli, the responsiveness to static and dynamic CO2 concentrations in their microenvironment, their location in the lung, and the influence of intracellular H+ in controlling their discharge have been studied in detail in some animals.

Amphibian lungs, as exemplified by the bullfrog, possess both rapidly and slowly adapting CO2-sensitive mechanoreceptors, but no receptors whose sole physiological stimulus is CO2 concentration. Reptilian lungs, at least in turtles and Tegu lizards, possess CO2-sensitive mechanoreceptors as well as receptors strikingly sensitive to CO2 but not to stretch of the lung. The CO2 receptors respond to static concentration of CO2 in the lungs as well as to rapid changes in intrapulmonary CO2 concentration. Avian lungs apparently possess only CO2 receptors without mechanical sensitivity. Mammalian lungs seemingly have only CO2-sensitive mechanoreceptors (slowly adapting pulmonary stretch receptors).

In all vertebrate classes studied, the discharge from both CO2 receptors and CO2-sensitive mechanoreceptors inhibits respiratory neuronal output from the brain. Intensive investigations in many laboratories are currently in progress to determine the importance of these receptors in controlling breathing.

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References

  1. Adrian, E.D.: Afferent impulses in the vagus and th eir effect on respiration. J. Physiol. (London) 79, 332–357 (1933)Google Scholar
  2. Banzett, R.B., Burger, R.E.: Response of avian intrapulmonary chemoreceptors to venous CO2 and ventilatory gas flow. Respir. Physiol. 29, 63–72 (1977)CrossRefGoogle Scholar
  3. Banzett, R.B., Coleridge, H.M., Coleridge, J.C.G.: Effect of CO2 on pulmonary vagal afferents in dogs. Physiologist 19, 115 (1976)Google Scholar
  4. Barnas, G.M.: Relationship between the discharge of avian intrapulmonary CO2 receptors and bronchial smooth muscle contraction. M.S. thesis, Univ. Nebraska, Lincoln, Nebraska 1977Google Scholar
  5. Bartlett, D., Jr., Sant’Ambrogio, G.: Effect of local and systemic hypercapnia on the discharge of stretch receptors in the airways of the dog. Respir. Physiol. 26, 91–99 (1976)CrossRefGoogle Scholar
  6. Bartoli, A., Cross, B.A., Guz, A., Jain, S.K., Noble, M.I.M., Trenchard, D.W.: The effect of carbon dioxide in the airways and alveoli on ventilation; a vagal reflex studied in the dog. J. Physiol. (London) 240, 91–109 (1974)Google Scholar
  7. Bitensky, L., Chambers, D.J., Chayen, J., Cross, B.A., Guz, A., Jain, S.K., Johnston, J.J.: Evidence concerning the site of receptors mediating the Hering-Breuer inflation reflex. J. Physiol. (London) 249, 30–31 (1975)Google Scholar
  8. Boelaert, R.B.: Sur la physiologie de la respiration de lacentiens. Arch. Int. pharmacodyn. Ther. 51, 379–436 (1941)Google Scholar
  9. Bonhoeffer, K., Kolatat, T.: Druckvolumendiagramm and Dehnungsrezeptoren der Froschlunge. Pflügers Arch. 265, 477–484 (1958)PubMedCrossRefGoogle Scholar
  10. Sordoni, L.: Sull’apnea spermentale. Sperimentale 61, 113–132 (1888)Google Scholar
  11. Bradley, G.W., Noble, M.I.M., Trenchard, D.: The direct effect of pulmonary stretch receptor discharge produced by changing lung carbon dioxide concentration in dogs on cardiopulmonary bypass and its action on breathing. J. Physiol. (London) 261 359–373 (1976)Google Scholar
  12. Burger, R.E.: Pulmonary chemosensitivity in the domestic fowl. Federation Proc. 27, 328 (1968)Google Scholar
  13. Burger, R.E., Osborne, J.L., Banzett, R.B.: Intrapulmonary chemoreceptors in Gallus domesticus: Adequate stimulus and functional localization. Respir. Physiol. 22, 87–97 (1974)CrossRefGoogle Scholar
  14. Burger, R.E., Nye, P.C.G., Powell, F.L., Ehlers, C., Barker, M., Fedde, M.R.: Response to CO2 of intrapulmonary chemoreceptors in the emu. Respir. Physiol. 28, 315–324 (1976a)CrossRefGoogle Scholar
  15. Burger, R.E., Coleridge, J.C.G., Coleridge, H.M., Nye, P.C.G., Powell, F.L., Ehlers, C., Banzett, R.B.: Chemoreceptors in the paleopulmonic lung of the emu: Discharge patterns during cyclic ventilation. Respir. Physiol. 28, 249–259 (1976b)CrossRefGoogle Scholar
  16. Dickinson, C.J., Paintal, A.S.: Stimulation of type-J pulmonary receptors in the cat by carbon dioxide. Clin. Sci. 38, 33P (1970)Google Scholar
  17. Dooley, M.S., Koppanyi, T.: The control of respiration in the domestic duck (Anas. boscos). J. Pharmac. Exp. Ther. 36, 507–518 (1929)Google Scholar
  18. Downing, S.E., Torrance, R.W.: Vagal baroreceptors of the bull-frog. J. Physiol. (London) 156, 13P (1961)Google Scholar
  19. Duke, G.E., Kuhlmann, W.D., Fedde, M.R.: Evidence for mechanoreceptors in the muscular stomach of the chicken. Poultry Sci. 56, 297–299 (1977)Google Scholar
  20. Eaton, J.A., Jr., Fedde, M.R., Burger, R.E.: Sensitivity to inflation of the respiratory system in the chicken. Respir. Physiol. 11, 167–177 (1971)CrossRefGoogle Scholar
  21. Fedde, M.R., Burger, R.E., Kitchell, R.L.: Localization of vagal afferents involved in the maintenance of normal avian respiration. Poultry Sci. 42, 1224–1236 (1963)Google Scholar
  22. Fedde, M.R., Gatz, R.N., Slama, H., Scheid, P.: Intrapulmonary CO2 receptors in the duck: I. Stimulus specificity. Respir. Physiol. 22, 99–114 (1974a)CrossRefGoogle Scholar
  23. Fedde, M.R., Gatz, R.N., Slama, H., Scheid, P.: Intrapulmonary CO2 receptors in the duck. II. Comparison with mechanoreceptors. Respir. Physiol. 22, 115–121 (1974b)CrossRefGoogle Scholar
  24. Fedde, M.R., Kuhlmann, W.D., Scheid, P.: Intrapulmonary receptors in the tegu lizard: I. Sensitivity to CO2. Respir. Physiol. 29, 35–48 (1977)CrossRefGoogle Scholar
  25. Fedde, M.R., Peterson, D.F.: Intrapulmonary receptor response to changes in airway- gas composition in Gallus domesticus. J. Physiol. (London) 209, 609–625 (1970)Google Scholar
  26. Foa, C.: Recherches sur l’apnée des oiseaux. Archs. ital. Biol. 55, 412–422 (1911)Google Scholar
  27. Gatz, R.N., Fedde, M.R., Crawford, E.C., Jr.: Lizard lungs: CO2-sensitive receptors in Tupinambis nigropunctatus. Experentia 31, 455 (1975)CrossRefGoogle Scholar
  28. Kostreva, D.R., Zuperka, E.J., Hess, G.L., Coon, R.L., Kampine, J.P.: Pulmonary afferent activity recorded from sympathetic nerves. J. Appl. Physiol. 39, 37–40 (1975)PubMedGoogle Scholar
  29. Kunz, A.L., Kawashiro, T., Scheid, P.: Study of CO2-sensitive vagal afferents in the cat lung. Respir. Physiol. 27, 347–355 (1976)CrossRefGoogle Scholar
  30. Kunz, A.L., Miller, D.A.: Pacing of avian respiration with CO2 oscillation. Respir. Physiol. 22, 167–177 (1974a)CrossRefGoogle Scholar
  31. Kunz, A.L., Miller, D.A.: Effects of feedback delay upon the apparent damping ratio of the avian respiratory control system. Respir. Physiol. 22, 179–189 (1974b)CrossRefGoogle Scholar
  32. Leitner, L.-M.: Pulmonary mechanoreceptor fibres in the vagus of the domestic fowl. Respir. Physiol. 16, 232–244 (1972)CrossRefGoogle Scholar
  33. Leitner, L.-M., Roumy, M.: Vagal afferent activities related to the respiratory cycle in the duck: Sensitivity to mechanical, chemical and electrical stimuli. Respir. Physiol. 22, 41–56 (1974)CrossRefGoogle Scholar
  34. McKean, T.A.: A linear approximation of the transfer function of pulmonary mechanoreceptors of the frog. J. Appl. Physiol. 27, 775–781 (1969)PubMedGoogle Scholar
  35. Miller, D.A., Kunz, A.L.: Avian ventilatory response to dynamic CO2 signals. J. Appl. Physiol. 39, 129–134 (1975)PubMedGoogle Scholar
  36. Milsom, W.K., Jones, D.R.: Are reptilian pulmonary receptors mechano-or chemosensitive. Nature (London) 261 327–328 (1976)CrossRefGoogle Scholar
  37. Molony, V.: A study of vagal afferent activity in phase with breathing and its role in the control of breathing in Gallus domesticus. Ph.D. thesis, Univ. Liverpool, Liverpool, England 1972Google Scholar
  38. Molony, V.: Classification of vagal afferents firing in phase with breathing in Gallus domesticus. Respir. Physiol. 22, 57–76 (1974)CrossRefGoogle Scholar
  39. Mustafa, M.E.K.Y., Purves, M.J.: The effect of CO2 upon discharge from slowly adapt-ing stretch receptors in the lungs of rabbits. Respir. Physiol. 16, 197–212 (1972)CrossRefGoogle Scholar
  40. Neil, E., Ström, L., Zotterman, Y.: Action potential studies of afferent fibres in the IXth and Xth cranial nerves of the frog. Acta physiol. Scand. 20, 338–350 (1950)CrossRefGoogle Scholar
  41. Nielsen, B.: On the regulation of the respiration in reptiles. I. The effect of temperature and CO2 on the respiration of lizards (Lacerta). J. exp. Biol. 38, 301–314 (1961)Google Scholar
  42. Nye, P.C.G.: Stimulus-response relations and location of intrapulmonary chemoreceptors in the lung of Gallus domesticus. Ph.D. thesis, Univ. California, Davis, California 1977Google Scholar
  43. Osborne, J.L., Burger, R.E.: Static and dynamic response characteristics of CO2-sensitive chemoreceptors in the avian lung. Physiologist 14, 205 (1971)Google Scholar
  44. Osborne, J.L., Burger, R.E.: Intrapulmonary chemoreceptors in Gallus domesticus. Respir. Physiol. 22, 77–85 (1974)CrossRefGoogle Scholar
  45. Partridge, R.C.: Afferent impulses in the vagus nerve. J. Cell. Comp. Physiol. 2, 367–380 (1933)CrossRefGoogle Scholar
  46. Perkins, J.F., Jr.: Historical development of respiratory physiology. In: Handbook of Physiology, Section 3, Respiration, Vol. I. Fenn, W.A., Rahn, H. (eds.). Washington, D.C.: Am. Physiol. Soc., 1964, pp. 1–62Google Scholar
  47. Peterson, D.F., Fedde, M.R.: Receptors sensitive to carbon dioxide in lungs of chicken. Science 162 1499–1501 (1968)PubMedCrossRefGoogle Scholar
  48. Peterson, D.F., Nightingale, T.E.: Functional significance of thoracic vagal branches in the chicken. Respir. Physiol. 27, 267–275 (1976)CrossRefGoogle Scholar
  49. Saalfeld, E. von: Die nervöse Regulierung der Atembewegungen bei Uromastix. Pflügers Arch. ges. Physiol. 233 449–468 (1934)Google Scholar
  50. Sampson, S.R., Vidruk, E.H.: Properties of irritant receptors in canine lung. Respir. Physiol. 25, 9–22 (1975)CrossRefGoogle Scholar
  51. Sant’Ambrogio, G., Miserocchi, G., Mortola, J.: Transient response of pulmonary stretch receptors in the dog to inhalation of carbon dioxide. Respir. Physiol. 22, 191–197 (1974)CrossRefGoogle Scholar
  52. Scheid, P., Kuhlmann, W.D., Fedde, M.R.: Intrapulmonary receptors in the tegu lizard: H. Functional characteristics and localization. Respir. Physiol. 29, 49–62 (1977)CrossRefGoogle Scholar
  53. Scheid, P., Slama, H., Gatz, R.N., Fedde, M.R.: Intrapulmonary CO2 receptors in the duck: III. Functional localization. Respir. Physiol. 22, 123–136 (1974)CrossRefGoogle Scholar
  54. Schoener, E.P., Frankel, H.M.: Effect of hyperthermia and PaCO2 on the slowly adapting pulmonary stretch receptor. Am. J. Physiol. 222, 68–72 (1972)PubMedGoogle Scholar
  55. Smyth, D.H.: The central and reflex control of respiration in the frog. J. Physiol. (London) 95, 305–327 (1939)Google Scholar
  56. Taglietti, V., Casella, C.: Stretch receptors stimulation in frog’s lungs. Pflügers Arch. 292, 297–308 (1966)CrossRefGoogle Scholar
  57. Taglietti, V., Casella, C.: Deflation receptors in frog’s lung. Pflügers Arch. 304, 81–89 (1968)PubMedCrossRefGoogle Scholar
  58. Templeton, J.R., Dawson, W.R.: Respiration in the lizard Crolophytus collaris. Physiol. Zool. 36, 104–121 (1963)Google Scholar
  59. Tschorn, R.R., Fedde, M.R.: Effects of carbon monoxide on avian intrapulmonary carbon dioxide-sensitive receptors. Respir. Physiol. 20, 313–324 (1974)CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1978

Authors and Affiliations

  • M. R. Fedde
    • 1
  • W. D. Kuhlmann
    • 1
  1. 1.Department of Anatomy and physiologyKansas State UniversityManhattanUSA

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