Physiology

  • Donald Heath
  • Paul Smith

Abstract

Although well over half a century has elapsed since the classic studies of de Castro (1928) and Heymans et al. (1930) revealed the carotid body to be the main peripheral arterial chemoreceptor, neither the mechanism of the process nor the identification of the transducer has yet been established. Throughout this book we give an account of the histological and ultrastructural features of the various tissue components of the glomus in health, at different ages throughout life, and in disease. In this chapter we consider the physiology of chemoreception and its relation to the cells, nerves and blood vessels of the carotid body. This affords us an opportunity to refer to part at least of the prodigious volume of research by many distinguished physiologists working in this field. It will become apparent that, in spite of all this intense activity, the precise mechanism of chemoreception is still far from being understood. It must also always be kept in mind that the carotid body may subserve other functions, perhaps of an endocrinological nature, in addition to that of chemoreception.

Keywords

Respiration Bicarbonate Methionine Adrenaline Choline 

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References

  1. Acker H (1987) The involvement of nerve terminals in the paraganglionic chemoreceptor system. Ann NY Acad Sci 519: 369–384PubMedCrossRefGoogle Scholar
  2. Band DM, Linton RAF (1983) Plasma potassium and the carotid body chemoreceptor in the cat. J Physiol (Lond) 345: 33 PGoogle Scholar
  3. Band DM, Linton RAF (1987) The interaction of hypoxia and K+ on the carotid chemoreceptor in anaesthetized cats. J Physiol (Lond) 394: 65 PGoogle Scholar
  4. Barer G, Wach R, Pallot D, Bee D (1986) Almitrine, hypoxia, systemic hypertension and the carotid body. In: Heath D (ed) Aspects of hypoxia. Liverpool University Press, Liverpool, pp 113–129Google Scholar
  5. Bingman D, Kienecker EW (1984) Effects of hypoxia on regenerated sinus nerve fibres in vivo and on neurons in vitro. In: Pallot DJ (ed) The peripheral arterial chemoreceptors. Croom Helm, Beckenham, Kent, pp 243–252Google Scholar
  6. Biscoe TJ, Duchen MR (1990) Cellular basis of transduction in carotid chemoreceptors. Am J Physiol 258: L271–L278PubMedGoogle Scholar
  7. Biscoe TJ, Bradley GW, Purves MJ (1970a) The relation between carotid body chemoreceptor discharge, carotid sinus pressure and carotid body venous flow. J Physiol (Lond) 208: 99–120Google Scholar
  8. Biscoe TJ, Lall A, Sampson SR (1970b) Electron microscopic and electrophysiological studies on the carotid body following intracranial section of the glossopharyngeal nerve. J Physiol (Lond) 208: 133–152 Cárdenas H, Zapata P (1980) Dual effects of dopamine upon chemosensory responses to cyanide. Neurosci Lett 18: 317–322Google Scholar
  9. Chow CM, Winder C, Read DJC (1986) Influences of endogenous dopamine on carotid body discharge and ventilation. J Appl Physiol 60: 370–375PubMedGoogle Scholar
  10. Dearnaley DP, Fillenz M, Woods RI (1968) The identification of dopamine in the rabbit’s carotid body. Proc R Soc Lond [Biol] 170: 195–203CrossRefGoogle Scholar
  11. de Castro F (1926) Sur la structure et l’innervation de la glande intercarotidienne (glomus caroticum) de l’homme et des mammifères, et sur un nouveau système d’innervation autonome du nerf glossopharyngien. Trav Lab Rech Biol 24: 365–432Google Scholar
  12. de Castro F (1928) Sur la structure et l’innervation du sinus carotidien de l’homme et des mammiferes. Nouveaux faits sur l’innervation et la fonction du glomus caroticum. Études anatomiques et physiologiques. Trav Lab Rech Biol 25: 331–380Google Scholar
  13. Dejours P (1963) Control of respiration by arterial chemoreceptors. Ann NY Acad Sci 109: 682–693PubMedCrossRefGoogle Scholar
  14. Delpierre S, Fornais M, Guillot C, Grimaud C (1987) Increased ventilatory chemosensitivity induced by domperidone, a dopamine antagonist, in healthy humans. Bull Eur Physiopathol Respir 23: 31–35PubMedGoogle Scholar
  15. Dinger BG, Stensaas LJ, Fidone SJ (1984) Chemosensory end-organs reinervated by normal and foreign nerves. In: Pallot DJ (ed) The peripheral arterial chemoreceptors. Croom Helm, Beckenham, Kent, pp 225–234Google Scholar
  16. Eyzaguirre C, Fidone SJ (1980) Transduction mechanisms in carotid body: glomus cells, putative neurotransmitters, and nerve endings. Am J Physiol 239: C135–C152PubMedGoogle Scholar
  17. Eyzaguirre C, Zapata P (1984) Perspectives in carotid body research. J Appl Physiol 57: 931–957PubMedGoogle Scholar
  18. Fidone S, Gonzalez C (1982) Catecholamine synthesis in rabbit carotid body in vitro. J Physiol (Lond) 333: 69–79Google Scholar
  19. Fidone SJ, Zapata P, Stensaas LJ (1977) Axonal transport of labeled material into sensory nerve endings of cat carotid body. Brain Res 124: 9–28PubMedCrossRefGoogle Scholar
  20. Fidone S, Gonzalez C, Yoshizaki K (1982a) Effects of hypoxia on catecholamine synthesis in rabbit carotid body in vitro. J Physiol (Lond) 333: 81–91Google Scholar
  21. Fidone S, Gonzalez C, Yoshizaki K (1982b) Effects of low oxygen on the release of dopamine from the rabbit carotid body in vitro. J Physiol (Lond) 333: 93–110Google Scholar
  22. Fishman MC, Greene WL, Platika D (1985) Oxygen chemoreception by carotid body cells in culture. Proc Natl Acad Sci USA 82: 1448–1450PubMedCrossRefGoogle Scholar
  23. Fitzgerald RS, Garger P, Hauer MC, Raff H, Fechter L (1983) Effect of hypoxia and hypercapnia on catecholamine content in cat carotid body. J Appl Physiol 54: 1408–1413PubMedGoogle Scholar
  24. Hamburger B, Ritzén M, Wersall J (1966) Demonstration of catecholamines and 5-hydroxytryptamine in the human carotid body. J Pharmacol Exp Ther 152: 197–201Google Scholar
  25. Hanbauer I, Hellström S (1978) The regulation of dopamine and noradrenaline in the rat carotid body and its modification by denervation and hypoxia. J Physiol (Lond) 282: 21–34Google Scholar
  26. Haymet BT, McCloskey DI (1975) Baroreceptor and chemoreceptor influences on heart rate during the respiratory cycle in the dog. J Physiol (Lond) 245: 699–712Google Scholar
  27. Heymans C, Bouckhaert JJ, Dautrebande L (1930) Sinus carotidien et réflexes respiratoires. II. Influences respiratoires réflexes de l’acidose de l’alkalôse, de l’anhydride carbonique, de l’ion hydrogène et de l’anoxémie. Sinus carotidiens et echanges respiratoires dans les poumons et au delà des poumons. Arch Int Pharmacodyn Ther 39: 400–448Google Scholar
  28. Holton P, Wood JB (1965) The effects of bilateral removal of the carotid bodies and denervation of the carotid sinuses in two human subjects. J Physiol (Lond) 181: 365–378Google Scholar
  29. Honda Y (1985) Role of carotid chemoreceptors in control of breathing at rest and in exercise: studies on human subjects with bilateral carotid body resection. Japn J Physiol 35: 535–544CrossRefGoogle Scholar
  30. Lahiri S, Smatresk N, Pokorski M, Barnard P, Mokashi A (1983) Efferent inhibition of carotid body chemoreception in chronically hypoxic cats. Am J Physiol 245: R678–R683PubMedGoogle Scholar
  31. Lugliani R, Whipp BJ, Seard C, Wasserman K (1971) Effect of bilateral carotid body resection on ventilatory control at rest and during exercise in man. New Engl J Med 285: 1105–1111PubMedCrossRefGoogle Scholar
  32. Marshall JM (1987) Analysis of cardiovascular responses evoked following changes in peripheral chemoreceptor activity in the rat. J Physiol (Lond) 394: 393–414Google Scholar
  33. McQueen DS (1984) Effects of selective dopamine receptor agonists and antagonists on carotid body chemoreceptor activity. In: Pallot DJ (ed) The peripheral arterial chemoreceptors. Croom Helm, Beckenham, Kent, pp 325–333Google Scholar
  34. Mills E, Jöbsis FF (1972) Mitochondrial respiratory chain of carotid body and chemoreceptor response to changes in oxygen tension. J Neurophysiol 35: 405–428PubMedGoogle Scholar
  35. Mir AK, Al-Neamy K, Pallot DJ, Nahorski SR (1982) Catecholamines in the carotid body of several mammalian species: effects of surgical and chemical sympathectomy. Brain Res 252: 335–342PubMedCrossRefGoogle Scholar
  36. Mir AK, McQueen DS, Pallot DJ, Nahorski SR (1984) Direct biochemical and neuropharmacological indentification of dopamine D2-receptors in the rabbit carotid body. Brain Res 291: 273–283PubMedCrossRefGoogle Scholar
  37. Monti-Bloch L, Eyzaguirre C (1980) A comparative physiological and pharmacological study of cat and rabbit carotid body chemoreceptors. Brain Res 193: 449–470PubMedCrossRefGoogle Scholar
  38. Monti-Bloch L, Stensaas LJ, Eyzaguirre C (1983) Effects of ischaemia on the function and structure of the cat carotid body. Brain Res 270: 63–76PubMedCrossRefGoogle Scholar
  39. Monti-Bloch L, Stensaas LJ, Eyzaguirre C (1984) Induction of chemosensitivity in muscle nerve fibres by carotid body transplantation. In: Pallot DJ (ed) The peripheral arterial chemoreceptors. Croom Helm, Beckenham, Kent, pp 235–242Google Scholar
  40. Mulligan E, Lahiri S, Storey BT (1981) Carotid body 02 chemoreception and mitochondrial oxidative phosphorylation. J Appl Physiol 51: 438–446PubMedGoogle Scholar
  41. Murray PA, Lavallee M, Vatner SF (1984) α-Adrenergic-mediated reduction in coronary blood flow secondary to carotid chemoreceptor reflex activation in conscious dogs. Circ Res 54: 96–106PubMedGoogle Scholar
  42. Olson EB, Vidruk EH, McGimmon DR, Dempsey JA (1983) Monoamine neurotransmitter metabolism during acclimatization to hypoxia in rats. Respir Physiol 54: 79–96PubMedCrossRefGoogle Scholar
  43. Olson EB, Vidruk EH, Dempsey JA (1988) Carotid body excision significantly changes ventilatory control in awake cats. J Appl Physiol 64: 666–671PubMedCrossRefGoogle Scholar
  44. Olson NC, Robinson NE, Anderson DL, Scott JB (1982) Effect of carotid body hypoxia and/or hypercapnia on pulmonary vascular resistance. Proc Soc Exp Biol Med 170: 188–193PubMedGoogle Scholar
  45. O’Regan RG (1981) Responses of carotid body chemosensory activity and blood flow to stimulation of sympathetic nerves in the cat. J Physiol (Lond) 315: 81–98Google Scholar
  46. O’Regan RG, Majcherczyk S (1982) Role of peripheral chemoreceptors and central chemosensitivity in the regulation of respiration and circulation. J Exp Biol 100: 23–40PubMedGoogle Scholar
  47. Paintal AS (1968) Some considerations relating to studies on chemoreceptor responses. In: Torrance RW (ed) Proceedings of the Wates Foundation Symposium on arterial chemoreceptors. Blackwell, Edinburgh and Oxford, pp 253–261Google Scholar
  48. Pallot DJ (1987) The mammalian carotid body. Adv Anat Embryol Cell Biol 102: 1–91PubMedCrossRefGoogle Scholar
  49. Parker PE, Dabney JM, Scott JB, Haddy FJ (1975) Reflex vascular responses in kidney, ileum and forelimb to carotid body stimulation. Am J Physiol 228: 46–51PubMedGoogle Scholar
  50. Perrin DG, Chan W, Cutz E, Madapallimattam A, Cole MJ (1986) Serotonin in the human infant carotid body. Experientia 42: 562–564PubMedCrossRefGoogle Scholar
  51. Ponte J, Sadler CL (1989a) Interactions between hypoxia, acetylcholine and dopamine in the carotid body of the rabbit and cat. J Physiol (Lond) 410: 395–410Google Scholar
  52. Ponte J, Sadler CL (1989b) Studies on the regenerated carotid sinus nerve of the rabbit. J Physiol (Lond) 410: 411–424Google Scholar
  53. Starlinger H, Acker H (1986) The norepinephrine and dopamine content of the cat carotid body in vivo under normoxic and hypoxic conditions. Neurosci Lett 64: 65–68PubMedCrossRefGoogle Scholar
  54. Steele RH, Hinterberger J (1972) Catecholamines and 5-hydroxytryptamine in the carotid body in vascular, respiratory, and other diseases. J Lab Clin Med 80: 63–70PubMedGoogle Scholar
  55. Torrance RW (1968) Prolegomena. In: Torrance RW (ed) Proceedings of the Wates Foundation Symposium on arterial chemoreceptors. Blackwell, Edinburgh and Oxford, pp 1–40Google Scholar
  56. Verna A, Roumy M, Leitner LM (1975) Loss of chemoreceptive properties of the rabbit carotid body after destruction of the glomus cells. Brain Res 100: 13–23PubMedCrossRefGoogle Scholar
  57. Verna A, Barets A, Salat C (1984) Distribution of sympathetic nerve endings within the rabbit carotid body: a histochemical and ultrastructural study. J Neurocytol 13: 849–865PubMedCrossRefGoogle Scholar
  58. Welsh MJ, Heistad DD, Abboud FM (1978) Depression of ventilation by dopamine in man: evidence for an effect on the chemoreceptor reflex. J Clin Invest 61: 708–713PubMedCrossRefGoogle Scholar
  59. Zapata P, Torrealba F (1984) Blockade of dopamine-induced chemosensory inhibition by domperidone. Neurosci Lett 51: 359–364PubMedCrossRefGoogle Scholar
  60. Zapata P, Stensaas LJ, Eyzaguirre C (1976) Axon regeneration following a lesion of the carotid nerve: electrophysiological and ultrastructural observations. Brain Res 113: 235–253PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag London Limited 1992

Authors and Affiliations

  • Donald Heath
    • 1
  • Paul Smith
    • 2
  1. 1.Department of PathologyUniversity of Liverpool Royal Liverpool University HospitalLiverpoolUK
  2. 2.Department of PathologyLiverpoolUK

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