About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 893506, 18 pages
http://dx.doi.org/10.1155/2013/893506
Review Article

Evaluating the Importance of the Carotid Chemoreceptors in Controlling Breathing during Exercise in Man

School of Sport, Exercise & Rehabilitation Sciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK

Received 25 April 2013; Accepted 8 July 2013

Academic Editor: Maxime Cannesson

Copyright © 2013 M. J. Parkes. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. F. De Castro, “Towards the sensory nature of the carotid body: Hering, De Castro and Heymans,” Frontiers in Neuroanatomy, vol. 3, pp. 1–11, 2009.
  2. C. Heymans, “Pharmacology in old and modern medicine,” Annual Review of Pharmacology, vol. 7, pp. 1–15, 1967. View at Scopus
  3. J. H. Comroe, “The hypernea of muscular exercise,” Physiological Reviews, vol. 24, pp. 319–339, 1944.
  4. T. G. Waldrop, F. L. Eldridge, G. A. Iwamoto, and J. H. Mitchell, “Central neural control of respiration and circulation during exercise,” in Handbook of Physiology, Section 12. Exercise: Regulation and Integration of Multiple Systems, L. B. Rowell and J. T. Shepherd, Eds., pp. 353–380, Oxford University Press, New York, NY, USA, 1996.
  5. S. A. Ward, “Assessment of peripheral chemoreflex contributions to exercise hyperpnea in humans,” Medicine and Science in Sports and Exercise, vol. 26, no. 3, pp. 303–310, 1994. View at Scopus
  6. N. R. Prabhakar and Y.-J. Peng, “Peripheral chemoreceptors in health and disease,” Journal of Applied Physiology, vol. 96, no. 1, pp. 359–366, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. P. Dejours, “Control of respiration in muscular exercise,” in Handbook of Physiology, Respiration, Section 1, W. O. Fenn and H. Rahn, Eds., pp. 631–648, American Physiological Society, Washington, DC, USA, 1964.
  8. J. H. Comroe, Physiology of Respiration, An Introductory Text, Year Book, Chicago, Ill, USA, 2nd edition, 1974.
  9. J. A. Dempsey and B. J. Whipp, “The respiratory system,” in Exercise Physiology, People and Ideas, C. M. Tipton, Ed., pp. 138–187, American Physiological Society, Bethesda, Md, USA, 2003.
  10. G. S. Dawes and J. H. Comroe Jr., “Chemoreflexes from the heart and lungs,” Physiological reviews, vol. 34, no. 2, pp. 167–201, 1954. View at Scopus
  11. K. Wasserman, B. J. Whipp, and R. Casaburi, “Respiratory control during exercise,” in Handbook of Physiology, Section 3 the Respiratory System II, the Control of Breathing, pp. 595–619, American Physiological Society, Bethesda, Md, USA, 1986.
  12. B. J. Whipp, “The control of exercise hyperpnea,” in Regulation of Breathing Part II, T. F. Hornbein, Ed., pp. 1069–1139, Marcel Dekker, New York, NY, USA, 1981.
  13. B. J. Whipp, “Ventilatory control during exercise in humans,” Annual Review of Physiology, vol. 45, pp. 393–413, 1983. View at Scopus
  14. B. J. Whipp and J. A. Davis, “Peripheral chemoreceptors and exercise hyperpnea,” Medicine and Science in Sports and Exercise, vol. 11, no. 2, pp. 204–212, 1979. View at Scopus
  15. P. Kumar and N. R. Prabhakar, “Peripheral chemoreceptors: function and plasticity of the carotid body,” Comprehensive Physiology, vol. 2, pp. 141–219, 2012.
  16. H. V. Forster, P. Haouzi, and J. A. Dempsey, “Control of breathing during exercise,” Comprehensive Physiology, vol. 2, pp. 743–777, 2012.
  17. J. Bronowski, The Ascent of Man, BBC, London, UK, 1973.
  18. H. V. Forster and L. G. Pan, “Control of breathing during exercise,” in The Lung, R. G. Crystal, J. B. West, E. R. Weibel, and P. J. Barnes, Eds., pp. 2001–2010, Lippincott-Raven, Philadelphia, Pa, USA, 2nd edition, 1997.
  19. E. Nattie, “Why do we have both peripheral and central chemoreceptors?” Journal of Applied Physiology, vol. 100, no. 1, pp. 9–10, 2006. View at Publisher · View at Google Scholar · View at Scopus
  20. C. Bernard, An Introduction to the Study of Experimental Medicine, Dover Publications, New York, NY, USA, 1865.
  21. J. S. Mill, A System of Logic, Ratiocinative and Inductive, Being a Connected View of the Principles of Evidence and the Methods of Scientific Investigation, Longmans, London, UK, 9th edition, 1875.
  22. M. I. Cohen and S. C. Wang, “Respiratory neuronal activity in pons of cat,” Journal of Neurophysiology, vol. 22, no. 1, pp. 33–50, 1959. View at Scopus
  23. M. J. Parkes, “Endocrine factors in fetal growth,” in Fetal and Neonatal Growth, F. Cockburn, Ed., pp. 33–48, John Wiley & Sons, Chichester, UK, 1988.
  24. J. F. Stein, An Introduction to Neurophysiology, Blackwells, Oxford, UK, 1982.
  25. J. F. Stein and C. J. Stoodley, Neuroscience, an Introduction, John Wiley & Sons, Chichester, UK, 2006.
  26. F. M. R. Walshe, “On the interpretation of experimental studies of cortical motor function: with special reference to the “operational view” of experimental procedures,” Brain, vol. 74, no. 3, pp. 249–266, 1951. View at Publisher · View at Google Scholar · View at Scopus
  27. H. Galbo, M. Kjaer, and N. H. Secher, “Cardiovascular, ventilatory and catecholamine responses to maximal dynamic exercise in partially curarized man,” Journal of Physiology, vol. 389, pp. 557–568, 1987. View at Scopus
  28. B. K. Hutt, S. M. Horvath, and G. B. Spurr, “Influence of varying degrees of passive limb movements on respiration,” Journal of Applied Physiology, vol. 12, no. 2, pp. 297–300, 1958. View at Scopus
  29. Y. Honda, S. Myojo, S. Hasegawa, T. Hasegawa, and J. W. Severinghaus, “Decreased exercise hyperpnea in patients with bilateral carotid chemoreceptor resection,” Journal of Applied Physiology Respiratory Environmental and Exercise Physiology, vol. 46, no. 5, pp. 908–912, 1979. View at Scopus
  30. K. Wasserman, B. J. Whipp, S. N. Koyal, and M. G. Cleary, “Effect of carotid body resection on ventilatory and acid base control during exercise,” Journal of Applied Physiology, vol. 39, no. 3, pp. 354–358, 1975. View at Scopus
  31. J. A. Dempsey and P. D. Wagner, “Exercise-induced arterial hypoxemia,” Journal of Applied Physiology, vol. 87, no. 6, pp. 1997–2006, 1999. View at Scopus
  32. D. M. Band, C. B. Wolff, J. Ward, G. M. Cochrane, and J. Prior, “Respiratory oscillations in arterial carbon dioxide tension as a control signal in exercise,” Nature, vol. 283, no. 5742, pp. 84–85, 1980. View at Scopus
  33. K. Murphy, R. P. Stidwill, B. A. Cross et al., “Is hypercapnia necessary for the ventilatory response to exercise in man?” Clinical Science, vol. 73, no. 6, pp. 617–625, 1987. View at Scopus
  34. C. S. Poon and C. Tin, “Mechanism of augmented exercise hyperpnea in chronic heart failure and dead space loading,” Respiratory Physiology & Neurobiology, vol. 186, pp. 114–130, 2013.
  35. E. Strange-Petersen, B. J. Whipp, D. B. Drysdale, and D. J. Cunningham, “Carotid arterial blood gas oscillations and the phase of the respiratory cycle during exercise in man: testing a model,” Advances in Experimental Medicine and Biology, vol. 99, pp. 335–342, 1978. View at Scopus
  36. J. H. Mateika and J. Duffin, “A review of the control of breathing during exercise,” European Journal of Applied Physiology and Occupational Physiology, vol. 71, no. 1, pp. 1–27, 1995. View at Publisher · View at Google Scholar · View at Scopus
  37. T. J. Clark and S. Godfrey, “The effect of CO2 on ventilation and breath-holding during exercise and while breathing through an added resistance,” Journal of Physiology, vol. 201, no. 3, pp. 551–566, 1969. View at Scopus
  38. A. R. C. Cummin, J. Alison, M. S. Jacobi, V. I. Iyawe, and K. B. Saunders, “Ventilatory sensitivity to inhaled carbon dioxide around the control point during exercise,” Clinical Science, vol. 71, no. 1, pp. 17–22, 1986. View at Scopus
  39. J. Duffin and G. V. McAvoy, “The peripheral-chemoreceptor threshold to carbon dioxide in man,” Journal of Physiology, vol. 406, pp. 15–26, 1988. View at Scopus
  40. M. Miyamura, H. Folgering, R. A. Binkhorst, F. D. J. Smolders, and F. Kreuzer, “Ventilatory response to CO2 at rest and during positive and negative work in normoxia and hyperoxia,” Pflugers Archiv European Journal of Physiology, vol. 364, no. 1, pp. 7–15, 1976. View at Scopus
  41. C. S. Poon and J. G. Greene, “Control of exercise hyperpnea during hypercapnia in humans,” Journal of Applied Physiology, vol. 59, no. 3, pp. 792–797, 1985. View at Scopus
  42. A. K. Datta, S. A. Shea, R. L. Horner, and A. Guz, “The influence of induced hypocapnia and sleep on the endogenous respiratory rhythm in humans,” Journal of Physiology, vol. 440, pp. 17–33, 1991. View at Scopus
  43. D. J. Paterson, P. A. Robbins, and J. Conway, “Changes in arterial plasma potassium and ventilation during exercise in man,” Respiration Physiology, vol. 78, no. 3, pp. 323–330, 1989. View at Publisher · View at Google Scholar · View at Scopus
  44. D. J. Paterson, J. S. Friedland, D. O. Oliver, and P. A. Robbins, “The ventilatory response to lowering potassium with dextrose and insulin in subjects with hyperkalaemia,” Respiration Physiology, vol. 76, no. 3, pp. 393–398, 1989. View at Scopus
  45. D. J. Paterson, K. L. Dorrington, D. H. Bergel et al., “Effect of potassium on ventilation in the rhesus monkey,” Experimental Physiology, vol. 77, no. 1, pp. 217–220, 1992. View at Scopus
  46. M. M. Warner and G. S. Mitchell, “Ventilatory responses to hyperkalemia and exercise in normoxic and hypoxic goats,” Respiration Physiology, vol. 82, no. 2, pp. 239–250, 1990. View at Publisher · View at Google Scholar · View at Scopus
  47. H. E. Cooper, T. H. Clutton-Brock, and M. J. Parkes, “Contribution of the respiratory rhythm to sinus arrhythmia in normal unanesthetized subjects during positive-pressure mechanical hyperventilation,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 286, no. 1, pp. H402–H411, 2004. View at Scopus
  48. S. Corne, K. Webster, and M. Younes, “Hypoxic respiratory response during acute stable hypocapnia,” American Journal of Respiratory and Critical Care Medicine, vol. 167, no. 9, pp. 1193–1199, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. R. Mohan and J. Duffin, “The effect of hypoxia on the ventilatory response to carbon dioxide in man,” Respiration Physiology, vol. 108, no. 2, pp. 101–115, 1997. View at Publisher · View at Google Scholar · View at Scopus
  50. P. Bock, The Paraganglia, Springer, Heidelberg, Germany, 1982.
  51. A. Dahan, D. Nieuwenhuijs, and L. Teppema, “Plasticity of central chemoreceptors: effect of bilateral carotid body resection on central CO2 sensitivity,” PLoS Medicine, vol. 4, no. 7, article e239, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. M. Fatemian, D. J. F. Nieuwenhuijs, L. J. Teppema et al., “The respiratory response to carbon dioxide in humans with unilateral and bilateral resections of the carotid bodies,” Journal of Physiology, vol. 549, no. 3, pp. 965–973, 2003. View at Publisher · View at Google Scholar · View at Scopus
  53. Y. Honda, S. Watanabe, I. Hashizume, et al., “Hypoxic chemosensitivity in asthmatic patients two decades after carotid body resection,” Journal of Applied Physiology Respiratory Environmental and Exercise Physiology, vol. 46, no. 4, pp. 632–638, 1979. View at Scopus
  54. R. Lugliani, B. J. Whipp, C. Seard, and K. Wasserman, “Effect of bilateral carotid-body resection on ventilatory control at rest and during exercise in man,” The New England Journal of Medicine, vol. 285, no. 20, pp. 1105–1111, 1971. View at Scopus
  55. J. G. Wade, C. P. Larson Jr., R. F. Hickey, W. K. Ehrenfeld, and J. W. Severinghaus, “Effect of carotid endarterectomy on carotid chemoreceptor and baroreceptor function in man,” The New England Journal of Medicine, vol. 282, no. 15, pp. 823–829, 1970. View at Scopus
  56. A. Guz, M. I. M. Noble, J. G. Widdicombe, D. Trenchard, and W. W. Mushin, “Peripheral chemoreceptor block in man,” Respiration Physiology, vol. 1, no. 1, pp. 38–40, 1966. View at Scopus
  57. B. J. Whipp, S. A. Ward, V. C. Baum, and B. Winter, “The influence of hyperoxia on ventilatory kinetics during moderate exercise in carotid-body-resected humans,” Journal of Physiology, vol. 475, article 20, 1994.
  58. J. W. Severinghaus, “Carotid body resection for COPD?” Chest, vol. 95, no. 5, pp. 1128–1129, 1989. View at Scopus
  59. M. S. Stulbarg and W. R. Winn, “Bilateral carotid body resection for the relief of dyspnea in severe chronic obstructive pulmonary disease: physiologic and clinical observations in three patients,” Chest, vol. 95, no. 5, pp. 1123–1128, 1989. View at Scopus
  60. S. A. Shea and A. Guz, “Personnalite ventilatoire—an overview,” Respiration Physiology, vol. 87, no. 3, pp. 275–291, 1992. View at Publisher · View at Google Scholar · View at Scopus
  61. J. J. Rutherford, T. H. Clutton-Brock, and M. J. Parkes, “Hypocapnia reduces the T wave of the electrocardiogram in normal human subjects,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 289, no. 1, pp. R148–R155, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. J. W. Bellville, B. J. Whipp, R. D. Kaufman, G. D. Swanson, K. A. Aqleh, and D. M. Wiberg, “Central and peripheral chemoreflex loop gain in normal and carotid body-resected subjects,” Journal of Applied Physiology Respiratory Environmental and Exercise Physiology, vol. 46, no. 4, pp. 843–853, 1979. View at Scopus
  63. J. A. Dempsey, H. V. Forster, and D. M. Ainsworth, “Regulation of hyperpnea, hyperventilation, and respiratory muscle recruitment during exercise,” in Regulation of Breathing, J. A. Dempsey and A. I. Pack, Eds., pp. 1065–1132, Marcel Dekker, New York, NY, USA, 1995.
  64. J. A. Dempsey, E. H. Vidruk, and G. S. Mitchell, “Pulmonary control systems in exercise: update,” Federation Proceedings, vol. 44, no. 7, pp. 2260–2270, 1985. View at Scopus
  65. J. M. Hagberg, E. F. Coyle, J. E. Carroll, J. M. Miller, W. H. Martin, and M. H. Brooke, “Exercise hyperventilation in patients with McArdle's disease,” Journal of Applied Physiology Respiratory Environmental and Exercise Physiology, vol. 52, no. 4, pp. 991–994, 1982. View at Scopus
  66. R. Jeyaranjan, R. Goode, and J. Duffin, “The effect of metabolic acid-base changes on the ventilatory changes at the end of heavy exercise,” European Journal of Applied Physiology and Occupational Physiology, vol. 58, no. 4, pp. 405–410, 1989. View at Scopus
  67. S. M. Rausch, B. J. Whipp, K. Wasserman, and A. Huszczuk, “Role of the carotid bodies in the respiratory compensation for the metabolic acidosis of exercise in humans,” Journal of Physiology, vol. 444, pp. 567–578, 1991. View at Scopus
  68. W. Stringer, R. Casaburi, and K. Wasserman, “Acid-base regulation during exercise and recovery in humans,” Journal of Applied Physiology, vol. 72, no. 3, pp. 954–961, 1992. View at Scopus
  69. R. G. G. Hanson, “Respiratory heat loss at increased core temperature,” Journal of Applied Physiology, vol. 37, no. 1, pp. 103–107, 1974. View at Scopus
  70. P. Chappuis, P. Pittet, and E. Jequier, “Heat storage regulation in exercise during thermal transients,” Journal of Applied Physiology, vol. 40, no. 3, pp. 384–392, 1976. View at Scopus
  71. J. D. MacDougall, W. G. Reddan, C. R. Layton, and J. A. Dempsey, “Effects of metabolic hyperthermia on performance during heavy prolonged exercise,” Journal of Applied Physiology, vol. 36, no. 5, pp. 538–544, 1974. View at Scopus
  72. P. F. Iampietro, M. Mager, and E. B. Green, “Some physiological changes accompanying tetany induced by exposure to hot, wet conditions,” Journal of Applied Physiology, vol. 16, pp. 409–412, 1961. View at Scopus
  73. J. A. Dempsey, J. M. Thomson, S. C. Alexander, H. V. Forster, and L. W. Chosy, “Respiratory influences on acid-base status and their effects on O2 transport during prolonged muscular work,” in Metabolic Adaptation to Prolonged Physical Exercise, H. Howard and J. R. Poortmans, Eds., pp. 56–64, Birkhäuser, Basel, Switzerland, 1975.
  74. K. Wasserman, W. L. Beaver, X.-G. Sun, and W. W. Stringer, “Arterial H+ regulation during exercise in humans,” Respiratory Physiology & Neurobiology, vol. 178, no. 2, pp. 191–195, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. X.-G. Sun, J. E. Hansen, W. W. Stringer, H. Ting, and K. Wasserman, “Carbon dioxide pressure-concentration relationship in arterial and mixed venous blood during exercise,” Journal of Applied Physiology, vol. 90, no. 5, pp. 1798–1810, 2001. View at Scopus
  76. D. J. C. Cunningham, “Studies on arterial chemoreceptors in man,” Journal of Physiology, vol. 384, pp. 1–26, 1987. View at Scopus
  77. S. Lahiri, “Physiologic responses: peripheral chemoreflexes,” in The Lung: Scientific Foundations, R. G. Crystal and J. B. West, Eds., pp. 1333–1340, Raven Press, New York, NY, USA, 1991.
  78. T. L. Griffiths, L. C. Henson, and B. J. Whipp, “Influence of inspired oxygen concentration on the dynamics of the exercise hypernoea in man,” Journal of Physiology, vol. 380, pp. 387–403, 1986. View at Scopus
  79. J. V. Weil and G. D. Swanson, “Peripheral chemoreceptors and the control of breathing,” in Exercise Pulmonary Physiology and Pathophysiology, B. J. Whipp and K. Wasserman, Eds., pp. 371–403, Marcel Dekker, New York, NY, USA, 1991.
  80. R. Jeyaranjan, R. Goode, S. Beamish, and J. Duffin, “The contribution of peripheral chemoreceptors to ventilation during heavy exercise,” Respiration Physiology, vol. 68, no. 2, pp. 203–213, 1987. View at Scopus
  81. K. Wasserman, “Testing regulation of ventilation with exercise,” Chest, vol. 70, no. 1, pp. 173–178, 1976. View at Scopus
  82. G. G. Somjen, “The missing error signal—regulation beyond negative feedback,” News in Physiological Sciences, vol. 7, pp. 184–185, 1992.
  83. H. E. Wood, M. Fatemian, and P. A. Robbins, “A learned component of the ventilatory response to exercise in man,” Journal of Physiology, vol. 553, no. 3, pp. 967–974, 2003. View at Publisher · View at Google Scholar · View at Scopus
  84. G. M. Blain, C. A. Smith, K. S. Henderson, and J. A. Dempsey, “Contribution of the carotid body chemoreceptors to eupneic ventilation in the intact, unanesthetized dog,” Journal of Applied Physiology, vol. 106, no. 5, pp. 1564–1573, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. G. M. Blain, C. A. Smith, K. S. Henderson, and J. A. Dempsey, “Peripheral chemoreceptors determine the respiratory sensitivity of central chemoreceptors to CO2,” Journal of Physiology, vol. 588, no. 13, pp. 2455–2471, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. M. Daly and A. Ungar, “Comparison of the reflex responses elicited by stimulation of the separately perfused carotid and aortic body chemoreceptors in the dog,” Journal of Physiology, vol. 182, no. 2, pp. 379–403, 1966. View at Scopus
  87. R. D. Dripps and J. H. Comroe, “The effect of the inhalation of high and low oxygen concentrations on respiration, pulse rate, ballistocardiogram and arterial oxygen saturation (oximeter) of normal individuals,” American Journal of Physiology, vol. 149, pp. 277–291, 1947.
  88. C. J. Lambertsen, R. H. Kough, D. Y. Cooper, G. L. Emmel, H. H. Loeschcke, and C. F. Schmidt, “Comparison of relationship of respiratory minute volume to pCO2 and pH or arterial blood and internal jugular blood in normal Man during hyperventilation produced by low concentrations of CO2 at 1 atmosphere and by O2 at 3.0 atmospheres,” Journal of Applied Physiology, vol. 5, pp. 255–263, 1953.
  89. K. Wasserman, B. J. Whipp, S. N. Koyal, and W. L. Beaver, “Anaerobic threshold and respiratory gas exchange during exercise,” Journal of Applied Physiology, vol. 35, no. 2, pp. 236–243, 1973. View at Scopus