Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Peripheral Chemoreceptors and Their Sensory Neurons in Chronic States of Hypo‐ and Hyperoxygenation

Sukhamay Lahiri

10.1002/cphy.cp040251

Source: Supplement 14: Handbook of Physiology, Environmental Physiology

Originally published: 1996

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Overview: Peripheral Chemoreceptors and Sensory Neurons
2 Oxygen Continuum and Optimum
3 pHo‐pHi Relationship and CO2‐H+ Stimulus Interaction with Hypoxia: Role of Carbonic Anhydrase
3.1 CO2–H+ and Interaction with Hypoxia
3.2 Catecholamine Release and Chemosensory Nerve Discharge
4 Oxygen Delivery
4.1 Po2 vs. O2 Content
4.2 Arterial Perfusion Pressure
4.3 Carotid Body Blood Volume and Flow
5 Integrated Carotid Body and Glomus Cell
6 Oxygen and Chemoreceptive Pigments
6.1 Carbon Monoxide/Oxygen
6.2 Nitric Oxide/Oxygen
7 Chronic Hypoxia Vs. Hyperoxia
7.1 Structure
7.2 Neurotransmitters and Gene Expression
7.3 Chemosensory Nerve Function
8 Chronic Cell Depolarization
9 Efferent Control
9.1 Petrosal and Nodose Ganglia
9.2 Sympathetic Ganglia
9.3 Cyclic GMP, Vascular Smooth Muscle, Glomus Cells, Petrosal Ganglion Processes, and Innervation of Carotid Body Elements
9.4 Cobalt, Other Transition Metals, and Ca2+
10 Lifelong Hypoxia and Developmental Aspects
11 Peripheral Chemoreceptors in Cardiopulmonary and Vascular Diseases
11.1 Cardiopulmonary and Vascular Diseases
11.2 Diseases of the Glomoids
11.3 Baroreceptor vs. Peripheral Chemoreceptors
12 Perspectives
Figure 1. Figure 1.

Effects of CO2 hydration and pHo on chemosensory discharge of cat carotid body. (A) Acidic hypercapnia stimulated discharge with gradual adaptation. The same hypercapnia without changing pHo showed a similar response pattern but its magnitude was less. This means that acid pHo contributed to the response, and hypercapnia itself was a stimulus, which at least in part was due to fast intracellular hydration mediated by carbonic anhydrase. (B) To examine the idea, the foregoing tests were repeated after treating the carotid body with methazolamide (40 μM). Methazolamide reduced baseline activity, eliminated the fast initial response, and delayed and dimished the magnitude of the responses to both acidic and isohydric hypercapnia. Thus intracellular carbonic anhydrase is critical for fast response to CO2. Without fast CO2 hydration the response to isohydric hypercapnia, developed slowly, but acidic hypercapnia produced a faster and larger response, indicating a significant effect of pHo.
Figure 2. Figure 2.

Time course of effects of high Pco on the chemosensory response to hypoxia. Hypoxia of 50 torr stimulated discharge in the absence of bright light. At point a the perfusate was changed to the same hypoxia plus 300 torr Pco. The immediate effect was a depression of the activity (b), followed by excitation. The excitation was eliminated by bright light (c) (photodissociation of the CO complex) even though the same hypoxia was present. Clearly, hypoxia did not cause the usual stimulation in the presence of CO. However, undissociated CO complex elicited chemoreception.
Figure 3. Figure 3.

(A) Control cat carotid body (150 torr of inspired oxygen pressure). Two glomus cells are in view. ER, endoplasmic reticulum; M, mitochondria. There are numerous dense‐core granules and an average number of mitochondria. Bar indicates 1 μm magnification. (B) Carotid body of a chronically hypoxic cat (28 days of 70 torr inspired oxygen pressure). Parts of several glomus (G) cells and a nerve ending (N) are seen. Overabundance of mitochondria (M) in the cells and nerve ending, are apparent. Bar indicates 1 μm magnification.
Figure 4. Figure 4.

(A) Neuroglomus junction in a normal cat carotid body (150 torr of inspired oxygen pressure). Nerve ending (N) on the glomus cell (G) with a cleft between is seen. Clear‐core granules in the nerve ending are of various sizes. They are particularly concentrated at the synaptic condensations. Some of the dense‐core vesicles in the glomus cell appear to have lost their contents and are less dense. Bar indicates 0.2 μm magnification.

(B) Neuroglomus junction in a carotid body of a chronically hypoxic cat (28 days of 70 torr inspired oxygen pressure). Along the length of the synaptic junction the clear‐core vesicles (V) is arranged in concentric rings. Three such arrangements can be identified (arrows). These vesicles are gravitated toward the synapse. The dense‐core vesicles in the glomus (G) are also concentrated near one end of the synapse. Bar indicates 0.2 μm magnification.
Figure 5. Figure 5.

Effects of chronic hyperoxia on cat carotid body ultrastructure (63 h of 700 torr inspired oxygen pressure). Numerous endoplasmic reticulum (ER/er) are seen in all glomus cells. Dense‐core vesicles are preponderant, and mitochondria in glomus cells manifest low levels of cristae, unlike in another structure near the blood vessel at top. Bar indicates 1 μm magnification.
Figure 6. Figure 6.

Carotid body of a chronically hyperoxic cat at a higher magnification than Figure 5 (63 h of 700 torr inspired oxygen pressure). Membranous structures in and around glomus cells are numerous. A nerve ending (N) on a glomus (G) cell appears normal, but clear‐core vesicles are only few. Dense‐core vesicles are quite abundant but appear to be fusing in many instances. Mitochondria (M) in glomus cells show fewer cristae. There is a lipofuscin body (*) in a glomus cell. This structure appears to be a repository of some of the dense‐core vesicles. Another glomus cell shows a cilium (C). Bar indicates 1 μm magnification.
Figure 7. Figure 7.

Relationship between inspired Po2 at high altitudes and alveolar/arterial Pco2, indicating high respiratory drive in the low‐altitude native (LAN) and low respiratory drive in the high‐altitude native (HAN).

(Reprinted with permission from Santolaya et al., Respir. Physiol. 77: 253–262, 1989, see ref. 134.)


Figure 1.

Effects of CO2 hydration and pHo on chemosensory discharge of cat carotid body. (A) Acidic hypercapnia stimulated discharge with gradual adaptation. The same hypercapnia without changing pHo showed a similar response pattern but its magnitude was less. This means that acid pHo contributed to the response, and hypercapnia itself was a stimulus, which at least in part was due to fast intracellular hydration mediated by carbonic anhydrase. (B) To examine the idea, the foregoing tests were repeated after treating the carotid body with methazolamide (40 μM). Methazolamide reduced baseline activity, eliminated the fast initial response, and delayed and dimished the magnitude of the responses to both acidic and isohydric hypercapnia. Thus intracellular carbonic anhydrase is critical for fast response to CO2. Without fast CO2 hydration the response to isohydric hypercapnia, developed slowly, but acidic hypercapnia produced a faster and larger response, indicating a significant effect of pHo.



Figure 2.

Time course of effects of high Pco on the chemosensory response to hypoxia. Hypoxia of 50 torr stimulated discharge in the absence of bright light. At point a the perfusate was changed to the same hypoxia plus 300 torr Pco. The immediate effect was a depression of the activity (b), followed by excitation. The excitation was eliminated by bright light (c) (photodissociation of the CO complex) even though the same hypoxia was present. Clearly, hypoxia did not cause the usual stimulation in the presence of CO. However, undissociated CO complex elicited chemoreception.



Figure 3.

(A) Control cat carotid body (150 torr of inspired oxygen pressure). Two glomus cells are in view. ER, endoplasmic reticulum; M, mitochondria. There are numerous dense‐core granules and an average number of mitochondria. Bar indicates 1 μm magnification. (B) Carotid body of a chronically hypoxic cat (28 days of 70 torr inspired oxygen pressure). Parts of several glomus (G) cells and a nerve ending (N) are seen. Overabundance of mitochondria (M) in the cells and nerve ending, are apparent. Bar indicates 1 μm magnification.



Figure 4.

(A) Neuroglomus junction in a normal cat carotid body (150 torr of inspired oxygen pressure). Nerve ending (N) on the glomus cell (G) with a cleft between is seen. Clear‐core granules in the nerve ending are of various sizes. They are particularly concentrated at the synaptic condensations. Some of the dense‐core vesicles in the glomus cell appear to have lost their contents and are less dense. Bar indicates 0.2 μm magnification.

(B) Neuroglomus junction in a carotid body of a chronically hypoxic cat (28 days of 70 torr inspired oxygen pressure). Along the length of the synaptic junction the clear‐core vesicles (V) is arranged in concentric rings. Three such arrangements can be identified (arrows). These vesicles are gravitated toward the synapse. The dense‐core vesicles in the glomus (G) are also concentrated near one end of the synapse. Bar indicates 0.2 μm magnification.



Figure 5.

Effects of chronic hyperoxia on cat carotid body ultrastructure (63 h of 700 torr inspired oxygen pressure). Numerous endoplasmic reticulum (ER/er) are seen in all glomus cells. Dense‐core vesicles are preponderant, and mitochondria in glomus cells manifest low levels of cristae, unlike in another structure near the blood vessel at top. Bar indicates 1 μm magnification.



Figure 6.

Carotid body of a chronically hyperoxic cat at a higher magnification than Figure 5 (63 h of 700 torr inspired oxygen pressure). Membranous structures in and around glomus cells are numerous. A nerve ending (N) on a glomus (G) cell appears normal, but clear‐core vesicles are only few. Dense‐core vesicles are quite abundant but appear to be fusing in many instances. Mitochondria (M) in glomus cells show fewer cristae. There is a lipofuscin body (*) in a glomus cell. This structure appears to be a repository of some of the dense‐core vesicles. Another glomus cell shows a cilium (C). Bar indicates 1 μm magnification.



Figure 7.

Relationship between inspired Po2 at high altitudes and alveolar/arterial Pco2, indicating high respiratory drive in the low‐altitude native (LAN) and low respiratory drive in the high‐altitude native (HAN).

(Reprinted with permission from Santolaya et al., Respir. Physiol. 77: 253–262, 1989, see ref. 134.)
References
 1. Acker, H. Po2 chemoreception in arterial chemoreceptors. Annu. Rev. Physiol. 51: 835–844, 1989.
 2. Anand, A., and A. S. Paintal. Oxygen sensing by arterial chemoreceptors. In: Response and Adaptation to Hypoxia: Organ to organelle, edited by S. Lahiri, N. S. Cherniack, and R. S. Fitzgerald. New York: Oxford University Press, 1991, p. 81–94.
 3. Barnard, P. S., S. Andronikou, M. Pokorski, N. J. Smatresk, and A. Mokashi. Time‐dependent effect of hypoxia on carotid body chemosensory function. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 63: 685–691, 1987.
 4. Bartfai, T., G. Fidone, and G. Laugel. Galanin and galanin antagonists: molecular and biochemical perspectives. TIPS 13: 312–317, 1992.
 5. Bauer, C., P. Ratcliffe, and K.‐U. Eckhardt. Hypoxia, erythropoietin gene expression, and erythropoiesis. In: Handbook of Physiology. Environmental, Physiology edited by M. J. Fregly and C. M. Blatteis. Bethesda, MD: Am. Physiol. Soc.
 6. Bee, D., D. J. Pallot, and G. R. Barer. Division of type 1 and epithelial cells in the hypoxic rat carotid body. Acta Anat. (Basel) 126: 226–229, 1986.
 7. Biscoe, T. J., and M. R. Duchen. Cellular basis of transduction in carotid chemoreceptors. Am. J. Physiol. 258 (Gastrointest. Liver Physiol. 21): G271–G278, 1990.
 8. Biscoe, T. J., and M. R. Duchen. Monitoring Po2 by the carotid chemoreceptors. NIPS 5: 229–233, 1990.
 9. Biscoe, T. J., and M. R. Duchen. Responses of type I cells dissociated from the rabbit carotid body to hypoxia. J. Physiol. (Lond.) 428: 39–59, 1990.
 10. Bisgard, G. E., M. A. Busch, and H. V. Forster. Ventilatory acclimatization to hypoxia is not dependent on cerebral hypocapnic alkalosis. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 60: 1011–1015, 1986.
 11. Bisgard, G. E., and H. Forster. Ventilatory responses to acute and chronic hypoxia. In: Handbook of Physiology. Environmental, Physiology edited by M. J. Fregly and C. M. Blatteis. New York: Oxford University Press, for the American Physiological Society, 1995, p. 1207–1239.
 12. Bisgard, G. E., A. Nielsen, E. Vidruk, L. Daristotle, M. Engwall, and H. V. Forster. Mechanisms of ventilatory acclimatization to hypoxia in goats. In: Chemoreceptors and Reflexes in Breathing: Cellular and Molecular Aspects, edited by S. Lahiri, R. Forster II, R. O. Davies, and A. I. Pack. New York: Oxford University Press, 1989, p. 208–215.
 13. Black, A. M., D. I. McCloskey, and R. W. Torrance. The responses of carotid body chemoreceptors in the cat to sudden changes of hypercapnic and hypoxic stimuli. Respir. Physiol. 13: 36–49, 1971.
 14. Black, I. B., D. M. Chikaraishi, and E. J. Lewis. Trans‐synaptic increase in RNA coding for tyrosine hydroxylase in rat sympathetic ganglion. Brain Res. 339: 151–153, 1985.
 15. Blanco, E. E., G. S. Dawes, M. A. Hanson, and H. B. McCook. The response to hypoxia of arterial chemoreceptors in fetal sheep and newborn lambs. J. Physiol. (Lond.) 351: 25–37, 1984.
 16. Blesa, M., S. Lahiri, W. Rashkind, and A. P. Fishman. Normalization of the blended ventilatory response to acute hypoxia in congenital cyanotic heart disease. N. Engl. J. Med. 296: 237–241, 1977.
 17. Bredt, D. S., and S. H. Synder. Nitric oxide as a neuronal molecular messenger. Neuron 8: 3–11, 1992.
 18. Brown, S. D., and C. D. Piantadosi. In vivo binding of carbon monoxide to cytochrome c oxidase in rat brain. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 68: 604–610, 1990.
 19. Buckler, K. J., R. D. Vaughan‐Jones, C. Peers, D. Lagadic‐Gossman, and P. C. G. Nye. Effects of extracellular pH, Pco2 and HCO3‐ on intracellular pH in isolated type‐1 cells of the neonatal rat carotid body. J. Physiol. (Lond.) 444: 703–721, 1991.
 20. Buckler, K. J., R. D. Vaughan Jones, C. Peers, and P. C. Nye. Intracellular pH and its regulation in isolated type I carotid body cells of the neonatal rat. J. Physiol. (Lond.) 436: 107–129, 1991.
 21. Buerk, D., S. Lahiri, D. K. Chugh, and A. Mokashi. Electrochemical detection of rapid dopamine release kinetics during hypoxia in perfused/superfused cat carotid bodies. J. Appl. Physiol. (in press), 1995.
 22. Buerk‐Wolin, T. M., and M. S. Wolin. H2O2 and cGMP may function as an O2 sensor in the pulmonary artery. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 66: 107–170, 1989.
 23. Chance, B., M. Erechinska, and M. Wagner. Mitochondrial responses to carbon monoxide toxicity. Ann. N. Y. Acad. Sci. 174: 193–204, 1970.
 24. Cherry, P. D., H. A. Omar, K. A. Farrell, J. Stuart, and M. S. Wolin. Superoxide anion inhibits cGMP‐associated bovine pulmonary arterial relaxation. Am. J. Physiol. 259 (Heat Circ. Physiol 28): H1056–1062, 1990.
 25. Chug, D., M. Katayama, A. Mokashi, and S. Lahiri. Nitric oxide–related inhibition of carotid chemosensory nerve activity in the cat. Respir. Physiol. 97: 147–156, 1994.
 26. Coburn, R. F., E. R. Allen, S. Ayres, D. Bartlett, Jr., S. M. Horvath, L. H. Kuller, V. Laties, L. D. Longo, and E. P. Radford, Jr. Carbon Monoxide. Washington, DC: Natl. Acad. Sci., 1977.
 27. Coburn, R. F., and H. Forman. Carbon monoxide toxicity. In: Handbook of Physiology. The Respiratory System, edited by L. E. Farhi and S. M. Tenney. Bethesda, MD: Am. Physiol. Soc., 1986, vol. IV p. 439–458.
 28. Comroe, J. H., Jr., and C. F. Schmidt. The part played by reflexes from the carotid body in the chemical regulation of respiration in the dog. Am. J. Physiol. 121: 75–96, 1938.
 29. Cruz, J. C., J. T. Reeves, R. F. Grover, J. T. Maher, R. E. McCullough, A. Cymerman, and J. C. Denniston. Ventilatory acclimatization to high altitude is prevented by CO2 breathing. Respiration 39: 121–130, 1980.
 30. Czyzyk‐Krzeska, M. F., D. A. Bayliss, E. E. Lawson, and D. E. Milhorn. Regulation of tyrosine hydroxylase gene expression in the rat carotid body by hypoxia. J. Neurochem. 58: 1538–1546, 1992.
 31. Data, P. G., C. Di Giulio, A. Mokashi, W.‐X. Huang, A. K. Sherpa, D. G. Penney, K. Albertine, and S. Lahiri. Mechanisms and site of effect of chronic erythropoietic stimuli on carotid body. In: Arterial Chemoreception, edited by C. Eyzaguirre, S. J. Fidone, R. S. Fitzgerald, S. Lahiri, and D. McDonald. New York: Springer‐Verlag, 1990, p. 323–329.
 32. DeCastro, F., and M. Rubio. The anatomy and innervation of the blood vessels of the carotid body and the role of chemoreceptive reactions in the autoregulation of the blood flow. In: Arterial Chemoreceptors, edited by R. W. Torrance. Oxford: Blackwell, 1968, p. 267–277.
 33. Delpiano, M. A., and J. Heschler. Evidence for a Po2 sensitive K+ channel in the type‐1 cell of the rabbit carotid body. FEBS Lett. 249: 195–198, 1989.
 34. Dhillon, D. P., G. R. Barer, and M. Walsh. The enlarged carotid body of the chronically hypoxic and chronically hypercapnic rat: a morphometric analysis. Q. J. Exp. Physiol. 69: 301–317, 1984.
 35. Di Giulio, C., P. G. Data, and S. Lahiri. Chronic cobalt causes of hypertrophy of glomus cells in the rat carotid body. Am. J. Physiol. 261 (Cell Physiol. 30): C102–C105, 1991.
 36. Di Giulio, C., W.‐X. Huang, S. Lahiri, A. Mokashi, and D. B. Buerk. Cobalt stimulates carotid body chemoreceptors. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 68: 1844–1849, 1990.
 37. Donnelley, D. F. Electrochemical detection of catecholamine release from rat carotid body in vitro. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 74: 2330–2337, 1993.
 38. Donnelly, D. F., and T. P. Doyle. Developmental changes in hypoxia‐induced catecholamine release from rat carotid body, in vitro. J. Physiol. (Lond.) 475: 267–275, 1994.
 39. Donnelley, D. F., and K. Kholwadwala. Hypoxia decreases intracellular calcium in adult rat carotid body glomus cells. J. Neurophysiol. 67: 1543–1551, 1992.
 40. Duchen, M. R., and T. J. Biscoe. Mitochondrial function in type I cells isolated from rabbit arterial chemoreceptors. J. Physiol. (Lond.) 450: 13–31, 1992.
 41. Duchen, M. R., and T. J. Biscoe. Relative mitochondrial membrane potential and [Ca2+]i in type I cells isolated from the rabbit carotid body. J. Physiol. (Lond.) 450: 33–61, 1992.
 42. Edelman, N. H., J. E. Melton, and J. A. Neubauer. Central adaptation to hypoxia. In: Response and Adaptation to Hypoxia: Organ to Organelle, edited by S. Lahiri, N. S. Cherniack, and R. S. Fitzgerald. New York: Oxford University Press, 1991, p. 235–244.
 43. Erhan, B., E. Mulligan, and S. Lahiri. Metabolic regulation of aortic chemoreception responses to CO2. Neurosci. Lett. 24: 143–147, 1981.
 44. Eyzaguirre, C., R. S. Fitzgerald, S. Lahiri, and P. Zapata. Arterial chemoreceptors. In: Handbook of Physiology. The Cardiovascular System, edited by J. T. Shepherd and F. M. Abboud. Washington, DC: Am. Physiol. Soc., 1983, vol. III, p. 557–621.
 45. Fidone, S. J., C. Gonzalez, B. Dinger, A. Gomez‐Niño, A. Obeso, and K. Yoshizaki. Cellular aspects of peripheral chemoreceptor function. In: The Lung, edited by R. G. Crystal, J. B. West, P. J. Barnes, N. S. Cherniack, and E. R. Weibel. New York: Raven, 1991, p. 1319–1332.
 46. Fidone, S. J., C. Gonzalez, A. Obeso, A. Gomez‐Niño, and B. Durger. Biogenic amine and neuropeptide transmitters in carotid body chemotransmission: experimental findings and perspectives. In: Hypoxia: The Adaptations, edited by J. R. Sutton, G. Coates, and J. E. Remmors. Toronto: Decker, 1990, p. 116–126.
 47. Finley, J. C. W., J. Polak, and D. M. Katz. Transmitter diversity in carotid body afferent neurons: dopaminergic and peptidergic phenotypes. Neuroscience 51: 973–987, 1992.
 48. Fisher, J. W. Pharmacologic modulation of erythropoietin production. Annu. Rev. Pharmacol. Toxicol. 28: 101–122, 1988.
 49. Fitzgerald, R. S., P. Garger, M. C. Hauer, H. Raff, and L. Fechter. Effect of hypoxia and hypercapnia on catecholamine content in cat carotid body. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 54: 1408–1413, 1983.
 50. Fitzgerald, R. S., and S. Lahiri. Reflex responses to chemoreceptor stimulation. In: Handbook of Physiology. The Respiratory System, edited by N. S. Cherniack and J. G. Widdicombe. Washington, DC: Am. Physiol. Soc., 1986, p. 313–362.
 51. Fitzgerald, R. S., E. M. Rogus, and A. Deghani. Catecholamines and 3',5′ cyclic AMP in carotid body chemoreception in the cat. In: Tissue Hypoxia and Ischemia, edited by M. Reivich, R. F. Coburn, S. Lahiri, and B. Chance. New York: Plenum, 1977, p. 245–260.
 52. Fridovitch, I. The biology of oxygen radicals: general concepts. In: Oxygen Radicals and Tissue Injury, edited by B. Halliwell. Bethesda, MD: FASEB, 1988, p. 1–3.
 53. Furchgot, R. F., W. Martin, P. D. Cherry, D. Jothianandan, and G. Villani. Endothelium‐dependent relaxation and cyclic GMP. In: Vascular Neuroeffector Mechanisms, edited by J. A. Bevan, T. Godfriend, R. A. Maxwell, J. C. Stodet, and M. Worcel. Amsterdam: Elsevier, p. 105–114.
 54. Gallego, R., I. Ivorra, and A. Morales. Effects of central or peripheral anatomy on membrane properties of sensory neurons in the petrosal ganglion of the cat. J. Physiol. (Lond.) 391: 39–56, 1987.
 55. Gilbert, D. L. Evolutionary aspects of atmospheric oxygen and organisms. In: Handbook of Physiology. Environmental Physiology, edited by M. J. Fregly and C. M. Blatteis. New York: Oxford University Press, for the American Physiological Society, 1995, p. 1059–1094.
 56. Goldberg, M. A., S. P. Dunning, and H. F. Bunn. Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein. Science 242: 1412–1414, 1988.
 57. Gonzalez, C., L. Almaraz, A. Obeso, and R. Rigual. Oxygen and acid chemoreception in the carotid body chemoreceptors. TIPS 15: 146–153, 1992.
 58. Gray, B. A. Response of the perfused carotid body to changes in pH and Pco2. Respir. Physiol. 4: 229–245, 1968.
 59. Grimes, P., S. Lahiri, R. Stone, A. Mokashi, and D. Chug. Nitric oxide synthase occurs in neurons and nerve fibers of the cat carotid body. In: Arterial Chemoreceptors: Cell to System. New York: Plenum, 1994, p. 221–224.
 60. Hackett, P. Mountain Sickness: Prevention, Recognition and Treatment. New York: American Alpine Club, 1980.
 61. Hanbauer, I., F. Karoum, S. Hellstrom, and S. Lahiri. Effects of long‐term hypoxia on the catecholamine content in rat carotid. Neuroscience 6: 81–86, 1981.
 62. Hanson, M. A., G. J. Eden, J. G. Nighuis, and P. J. Moore. Peripheral chemoreceptors and other oxygen sensors in the fetus and newborn. In: Chemoreceptors and Reflexes in Breathing: Cellular and Molecular Aspects, edited by S. Lahiri, R. E. Forster, R. O. Davies, and A. I. Pack. New York: Oxford University Press, 1989, p. 113–120.
 63. Hayashi, Y., S. Miwa, K. Lee, K. Koshimura, K. Hamahata, H. Hasegawa, M. Gujiwara, and J. Watanabe. Enhancement of in vivo tyrosine hydroxylation in the rat adrenal gland under hypoxic conditions. J. Neurochem. 54: 1115–1121, 1990.
 64. He, S.‐F., J.‐Y. Wei, and C. Eyzaguirre. Effects of relative hypoxia and hypercapnia on intracellular pH and membrane potential of cultured carotid body glomus cells. Brain Res. 556: 333–338, 1991.
 65. Heath, D., and P. Smith. Diseases of the Human Carotid Body. London: Springer‐Verlag, 1992.
 66. Hertzberg, T. Postnatal Adaptation of Peripheral Arterial Chemoreceptors. Stockholm: Nobel Institute for Neurophysiology, 1990.
 67. Hochachka, P. W. Metabolic defense adaptations to hypobaric hypoxia in man. In: Handbook of Physiology. Environmental Physiology, edited by M. J. Fregly and C. M. Blatteis. New York: Oxford University Press, for the American Physiological Society, 1995, p. 1115–1123.
 68. Howe, A., and E. Neil. Arterial chemoreceptors. In: Handbook of Sensory Physiology: Entereceptors, edited by E. Neil. Berlin: Springer‐Verlag, 1972, p. 47–80.
 69. Hoyt, R., and A. Honig. Energy metabolism and fluid balance at high altitude. In: Handbook of Physiology. Environmental Physiology, edited by M. J. Fregly and C. M. Blatteis. Bethesda, MD: Am. Physiol. Soc. 1994.
 70. Iturriaga, R., and S. Lahiri. Carotid body chemoreception in the absence and presence of CO2–HCO3‐. Brain Res. 568: 253–260, 1991.
 71. Iturriaga, R., A. Mokashi, and S. Lahiri. Dynamics of carotid body responses in the presence and absence of CO2–HCO3‐: role of carbonic anhydrase. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 75: 1587–1594, 1993.
 72. Iturriaga, R., W. L. Rumsey, S. Lahiri, D. Spergel, and D. F. Wilson. Intracellular pH and oxygen chemoreception in the cat carotid body in vitro. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 72: 2259–2266, 1992.
 73. Jamieson, D. Oxygen toxicity and reactive oxygen metabolites in mammals. Free Radical Biol. Med. 7: 87–108, 1989.
 74. Joels, N., and E. Niel. The action of high tensions of carbon monoxide on the carotid chemoreceptors. Arch. Int. Pharmacodyn. Ther. 138: 528–534, 1962.
 75. Joenje, H., J. J. P. Gille, A. B. Oostra, and P. Van de Valk. Some characteristics of hyperoxia‐adapted Hela cells. Lab. Invest. 52: 420–428, 1985.
 76. Katsuoka, Y., B. Beckman, W. J. George, and J. W. Fisher. Increased level of erythropoietin in kidney extracts of rats treated with and hypoxia. J. Physiol. (Lond.) 244: 129–133, 1983.
 77. Katz, D. M. Molecular mechanisms of carotid body afferent neuron development. In: Response and Adaptation to Hypoxia: Organ to Organelle, edited by S. Lahiri, N. S. Cherniack, and R. S. Fitzgerald. New York: Oxford University Press, 1991, p. 133–142.
 78. Katz, D. M., and M. J. Erb. Developmental regulation of tyrosine hydroxylase expression in primary sensory neurons of the rat. Dev. Biol. 137: 233–242, 1990.
 79. 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. USA 80: 3526–3530, 1986.
 80. Keilin, D. The History of Cell Respiration and Cytochrome. Cambridge: Cambridge University Press, 1970.
 81. Klausner, R. D., J. G. Donaldson, J. Lippincott‐Schwatz, and A. Brefeldin. Insights in the control of membrane traffic and organelle structure. J. Cell. Biol. 116: 1071–1080, 1992.
 82. Kummer, W. Three types of neurochemically defined autonomic fibers innervate the carotid baroreceptor and chemoreceptor regions in the guinea‐pig. Anat. Embryol. 181: 477–489, 1990.
 83. Kummer, W., and K. Addicks. Quantitative studies of the aortic bodies of the cat. 1. Point‐counting analysis of tissue components. Acta Anat. (Basel) 126: 48–53, 1986.
 84. Kummer, W., and J.‐O. Habeck. Light and electronmicroscopical and immunohistochemical investigation of the innervation of the human carotid body. In: Neurobiology and Cell Physiology of Chemoreception, edited by P. G. Data, H. Acker, and S. Lahiri. London: Plenum, 1993, p. 67–71.
 85. Lahiri, S. Peripheral chemoreflex. In: The Lung, edited by R. G. Crystal, J. B. West, P. J. Barnes, N. S. Cherniack, and E. R. Weibel. New York: Raven, 1991, p. 1333–1340.
 86. Lahiri, S. Respiration in chronic hypoxia and hyperoxia: role of peripheral chemoreceptors. In: Control of Breathing and Its Modelling Perspective, edited by Y. Honda, Y. Miamoto, K. Kono, and J. G. Widdicombe. New York: Plenum, 1992, p. 433–440.
 87. Lahiri, S. Chromophores in O2 chemoreception: the carotid body model. NIPS 9: 162–165, 1994.
 88. Lahiri, S., J. S. Brody, T. Velasquez, E. K. Motoyama, M. Simpser, R. G. Delaney, and G. Polgar. Pulmonary adaptation to high altitude: genetic vs. environment. Nature 261: 133–135, 1976.
 89. Lahiri, S., N. S. Cherniack, and R. S. Fitzgerald (Eds). Response and Adaptation to Hypoxia: Organ to Organelle. New York: Oxford University Press, 1991.
 90. Lahiri, S., and R. G. Delaney. Stimulus interaction in the responses of carotid body chemoreceptor single afferent fibres. Respir. Physiol. 24: 249–266, 1975.
 91. Lahiri, S., and R. G. Gelfand. Mechanisms of acute ventilatory responses. In: Regulation of Breathing, edited by T. F. Hornbein. New York: Dekker, 1981, p. 773–843.
 92. Lahiri, S., R. Iturriaga, and A. Mokashi. CO reveals dual mechanisms of O2 chemoreception in the cat carotid body. Respir. Physiol. 94: 227–240, 1993.
 93. Lahiri, S., K. Maret, and M. G. Sherpa. Dependence of high altitude sleep apnea on ventilatory sensitivity to hypoxia. Respir. Physiol. 52: 281–301, 1983.
 94. Lahiri, S., A. Mokashi, C. Di Giulio, A. K. Sherpa, W.‐X. Huang, and P. G. Data. Carotid body adaptation. In: Hypoxia—The Adaptations, edited by J. R. Sutton, G. Coates, and J. E. Remmers. Toronto: Dekker, 1990, p. 127–130.
 95. Lahiri, S., A. Mokashi, M. Shirahata, and S. Andronikou. Chemical respiratory control in chronically hyperoxic cats. Respir. Physiol. 82: 201–216, 1990.
 96. Lahiri, S., E. Mulligan, S. Andronikou, M. Shirahata, and A. Mokashi. Carotid body chemosensory function in prolonged normobaric hyperoxia in the cat. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 62: 1924–1931, 1987.
 97. Lahiri, S., E. Mulligan, T. Nishino, A. Mokashi, and R. O. Davies. Relative responses of aortic body and carotid body chemoreceptors to carboxyhemoglobinemia. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 50: 580–586, 1981.
 98. Lahiri, S., E. Mulligan, N. J. Smatresk, P. Barnard, A. Mokashi, D. Torbati, M. Pokorski, R. Zhang, P. G. Data, and K. Albertine. Mechanisms of carotid body responses to chronic low and high oxygen pressures. In: Chemoreceptors and Reflexes in Breathing: Cellular and Molecular Aspects, edited by S. Lahiri, R. E. Forster, R. O. Davies, and A. I. Pack. New York: Oxford University Press, 1989, p. 215–227.
 99. Lahiri, S., D. G. Penney, A. Mokashi, and K. H. Albertine. Chronic CO inhalation and carotid body catecholamines: testing of hypotheses. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 67: 239–242, 1989.
 100. Lahiri, S., W. L. Rumsey, D. F. Wilson, and R. Iturriaga. Contribution of in vivo microvascular Po2 in the cat carotid body chemotransduction. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 75: 1035–1043, 1993.
 101. Lahiri, S., N. J. Smatresk, and E. Mulligan. Responses of peripheral chemoreceptors to natural stimuli. In: Physiology of the Peripheral Arterial Chemoreceptors, edited by R. G. O'Regan and H. Acker. Amsterdam: Elsevier, 1983, p. 221–256.
 102. Lahiri, S., N. J. Smatresk, M. Pokorski, P. Barnard, and A. Mokashi. Efferent inhibition of carotid body chemoreception in chronically hypoxic cats. Am. J. Physiol. 245 (Regulatory Integrative Comp. Physiol. 14): R678–R683, 1983.
 103. Lahiri, S., N. J. Smatresk, M. Pokorski, P. Barnard, A. Mokashi, and K. H. McGregor. Dopaminergic inhibition of carotid body chemoreceptors in chronically hypoxic cats. Am. J. Physiol. 247 (Regulatory Integrative Comp. Physiol. 17): R24–R28, 1984.
 104. Lauweryns, J. M., and A. V. Lommel. Morphometric analysis of hypoxia‐induced synaptic activity in intrapulmonary neuroepithelial bodies. Cell Tissue Res. 226: 201–214, 1982.
 105. Liberzon, I. R., R. Arieli, and D. Kerem. Attenuation of hypoxic ventilation by hypobaric O2: effects of pressure and exposure time. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 66: 851–856, 1989.
 106. Lloyd, B. B., D. J. C. Cunningham, and R. C. Goode. Depression of hypoxic hyperventilation in man by sudden inspiration of carbon monoxide. In: Arterial Chemoreceptors, edited by R. W. Torrance. Oxford: Blackwell, 1968, p. 145–147.
 107. Lopez‐Barneo, J., J. R. Lopez‐Lopez, J. Urena, and C. Gonzalez. Chemotransduction in the carotid body: K+ current modulated by Po2 in type I chemoreceptor cells. Science 241: 580–582, 1988.
 108. Lopez‐Lopez, J. R., and C. Gonzalez. Time course of K+ current inhibition by low oxygen in the chemoreceptor cells of adult rabbit carotid body. FEBS Lett. 299: 251–254, 1992.
 109. Lutz, P. L. Mechanisms for anoxic survival in the vertebrate brain. Annu. Rev. Physiol. 54: 601–618, 1992.
 110. Marchal, F., A. Bairam, P. Hauzi, J. P. Crance, C. Di Giulio, P. Vert, and S. Lahiri. Carotid chemoreceptor response to natural stimuli in the newborn kitten. Respir. Physiol. 87: 183–193, 1992.
 111. Marchal, R., A. Bairam, P. Hauzi, J. M. Hascoet, J. P. Crance, P. Vert, and S. Lahiri. Dual responses of carotid chemosensory afferents to dopamine in the newborn kitten. Respir. Physiol. 90: 173–183, 1992.
 112. Marks, G. S., J. F. Brien, K. Nakatsu, and B. E. McLaughlin. Does carbon monoxide have a physiological functions? TIPS 12: 185–188, 1991.
 113. McDonald, D. Peripheral chemoreceptors. In: Regulation of Breathing, edited by T. F. Hornbein. New York: Dekker, 1981, p. 105–319.
 114. McGregor, K. H., J. Gil, and S. Lahiri. A morphometric study of the carotid body in chronically hypoxic rat. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 57: 1430–1438, 1984.
 115. McQueen, D. S. Pharmacological aspects of putative transmitters in the carotid body. In: Physiology of the Peripheral Arterial Chemoreceptors, edited by H. Acker and R. G. O'Regan. Amsterdam: Elsevier, 1983, p. 149–196.
 116. Mitchell, R. A., A. K. Sinha, and D. M. McDonald. Chemoreceptive properties of regenerated endings of the carotid sinus nerve. Brain Res. 43: 680–685, 1972.
 117. Mokashi, A., C. DiGuilio, L. Morelli, and S. Lahiri. Chronic hyperoxic effects on cat carotid body structure and catecholamines. Respir. Physiol. 97: 25–32, 1994.
 118. Mokashi, A., and S. Lahiri. Aortic and carotid body chemoreception in prolonged hyperoxia in the cat. Respir. Physiol. 86: 233–243, 1991.
 119. Moncada, R. M., J. Palmer, and E. A. Higgs. Nitric oxide: physiology, pathophysiology and pharmacology. Pharmacol. Rev. 43: 109–142, 1991.
 120. Mulligan, E. Discharge properties of carotid bodies: developmental aspects. In: Development Neurobiology of Breathing, edited by G. G. Haddard and J. P. Farber. New York: Dekker, p. 321–340.
 121. Mulligan, E., S. Lahiri, and B. T. Storey. Carotid body O2 chemoreception and mitochondrial oxidative phosphorylation. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 51: 438–446, 1981.
 122. Nurse, C. A., and C. Vollmer. Effects of hypoxia on cultured chemoreceptors of the rat carotid body: DNA synthesis and mitotic activity in glomus cells. In: Neurobiology and Cell Physiology of Chemoreception, edited by P. G. Data, H. Acker, and S. Lahiri. London: Plenum, 1993, p. 79–84.
 123. Obeso, A., A. Rocher, S. Fidone, and C. Gonzalez. The role of dihydrophyridine‐sensitive Ca2+ channels in stimulus‐evoked catecholamine release from chemoreceptor cells of the carotid body. Neuroscience 47: 463–472, 1992.
 124. O'Regan, R. G., and S. Majcherczyk. Control of peripheral chemoreceptors by efferent nerves. In: Physiology of the Peripheral Arterial Chemoreceptors, edited by H. Acker and R. G. O'Regan. Amsterdam: Elsevier, 1983, p. 257–298.
 125. O'Sullivan, A. J., and R. D. Burgoyne. Cyclic GMP regulates nicotine‐induced secretion from cultured bovine adrenal chromaffin cells: effects of 8‐bromo‐cyclic GMP, atrial natriuretic peptide and nitroprusside (nitric oxide). J. Neurochem. 54: 1805–1908, 1990.
 126. Peers, C., and J. O'Donnell. Potassium currents recorded in type I carotid body cells from the neonatal rat and their modulation by chemoexcitatory agents. Brain Res. 522: 259–266, 1990.
 127. Pequignot, J. M., J. M. Cottet‐Emard, Y. Dalmaz, and L. Peyrin. Dopamine and norepinephrine dynamics in rat carotid body during long‐term hypoxia. J. Auton. Nerv. Syst. 21: 9–14, 1987.
 128. Pequignot, J. M., S. Hellström, and T. Hertzberg. Long‐term hypoxia and hypercapnia in the cat carotid body: a review. In: Arterial Chemoreception, edited by C. Eyzaguirre, S. J. Fidone, R. S. Fitzgerald, S. Lahiri, and P. Zapata. New York: Springer‐Verlag, 1990, p. 100–114.
 129. Perez‐Garcia, M. T., L. Alvaraz, and C. Gonzalez. Effects of different types of stimulation on cyclic AMP content in the rabbit carotid body: functional significance. J. Neurochem. 55: 1287–1293, 1990.
 130. Pokorski, M., and S. Lahiri. Endogenous opiates and ventilatory acclimatization to chronic hypoxia in the cat. Respir. Physiol. 83: 211–222, 1991.
 131. Prabhakar, N. R., G. K. Kumar, C. H. Chang, F. H. Agani, and M. A. Haxhiru. Nitric oxide in the sensory function of the carotid body. Brain Res. 625: 10–22, 1993.
 132. Prabhakar, N. R., S. C. Landis, G. K. Kumar, D. Mullikin‐Kilpatrick, N. S. Cherniack, and S. Leeman. Substance P and neurokinin A in the cat carotid body: localization, exogenous effects and changes in content in response to arterial Po2. Brain Res. 481: 205–214, 1989.
 133. Ray, D. K., A. Mokashi, M. Katayama, F. Botré, and S. Lahiri. Lack of parallelism between the effects of hypoxia on the glomus cell pHi and carotid chemosensory response. Neurosci. Abstr. 19: 1407, 1993.
 134. Rigual, R., J. R. Lopez‐Lopez, and C. Gonzalez. Release of dopamine and chemoreceptor discharge induced by low pH and high Pco2 stimulation of the cat carotid body. J. Physiol. (Lond.) 433: 519–531, 1991.
 135. Roumy, M., C. Armengand, and L.‐M. Leitner. Catecholamines in the carotid body. In: Arterial Chemoreception, edited by C. Eyzaguirre, S. J. Fidone, R. S. Fitzgerald, S. Lahiri, and D. McDonald. New York: Springer‐Verlag, 1990, p. 115–123.
 136. Rumsey, W. L., R. Iturriaga, D. Spergel, S. Lahiri, and D. F. Wilson. Optical measurements of the dependence of chemoreception on oxygen pressure in the cat carotid body. Am. J. Physiol. 261 (Cell Physiol. 30): C614–C622, 1991.
 137. Santolaya, R. B., S. Lahiri, R. T. Alfaro, and R. B. Schoene. Respiration adaptation in the highest inhabitants and highest Sherpa mountaineers. Respir. Physiol. 77: 253–262, 1989.
 138. Sato, M., K. Ikeda, K. Yoshizaki, and H. Koyano. Response of cytosolic calcium to anoxia and cyanide in cultured glomus cells of newborn rabbit carotid body. Brain Res. 551: 527–530, 1991.
 139. Schoonen, W. G. E. J., A. H. Wanamarta, J. M. Van der Kleivan Moorsel, C. Jakobs, and H. Joenje. Respiration failure and stimulation of glycolysis in Chinese hamster ovary cells exposed to normobaric hyperoxia. J. Biol. Chem. 265: 11118–11124, 1990.
 140. Schulz, S., M. Chinkers, and D. L. Garbers. The guanylate cyclase/receptor family of proteins. FASEB J. 3: 2026–2035, 1989.
 141. Sherpa, A. K., K. H. Albertine, D. G. Penney, B. Thompkins, and S. Lahiri. Chronic CO exposure stimulates erythropoiesis but not glomus cell growth. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 67: 1383–1387, 1989.
 142. Shirahata, M., and R. S. Fitzgerald. Dependency of hypoxic chemotransduction in cat carotid body on voltage‐gated calcium channels. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 71: 1062–1069, 1991.
 143. Shirahata, M., and R. S. Fitzgerald. The presence of CO2/HCO3‐ is essential for hypoxic chemotransduction in the in vivo perfused carotid body. Brain Res. 545: 297–300, 1991.
 144. Smith, J. B., C. D. Dwyer, and L. Smith. Cadmium evokes inositol polyphosphate formation and calcium mobilization. J. Biol. Chem. 264: 7115–7118, 1989.
 145. Snyder, S. H. Nitric oxide: first in a new class of neurotransmitters? Science 257: 494–496, 1992.
 146. Stea, A., A. Jackson, and C. A. Nurse. Hypoxia and N6,O2‐dibutyryladenosine 3'5'‐cyclic monophosphate, but not nerve growth factor, induce Na+ channels and hypertrophy in chromaffin‐like arterial chemoreceptors. Proc. Natl. Acad. Sci. U.S.A. 89: 9469–9473, 1992.
 147. Sutton, J. R., C. S. Houston, A. L. Mansell, M. McFadden, P. Hackett, and A. C. Powles. Effects of acetazolamide on hypoxemia during sleep at high altitude. N. Engl. J. Med. 301: 1329–1331, 1979.
 148. Tatsumi, K., C. K. Pickett, and J. V. Weil. Attenuated carotid body hypoxic sensitivity after prolonged hypoxic exposure. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 70: 748–755, 1991.
 149. Tenney, S. M., and L. C. Ou. Hypoxic ventilatory response of cats at high altitude: an interpretation of blunting. Respir. Physiol. 30: 185–199, 1977.
 150. Teppema, L. J., F. Rocheffe, and M. Demedts. Ventilatory effects of acetazolamide in cats during hypoxemia. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 72: 1717–1723, 1992.
 151. Torbati, D., A. K. Sherpa, S. Lahiri, A. Mokashi, K. H. Albertine, and C. Di Giulio. Hyperbaric oxygenation alters carotid body ultrastructure and function. Respir. Physiol. 92: 183–196, 1993.
 152. Vanderkooi, J. M., M. Erecinska, and I. A. Silver. Oxygen in mammalian tissue: methods of measurement and affinities of various reactions. Am. J. Physiol. 260 (Cell Physiol. 29): C1131–C1150, 1991.
 153. Verna, A., D. J. Hirsch, C. E. Glatt, G. V. Ronnett, and S. H. Snyder. Carbon monoxide: a putative neural messenger. Science 259: 381–384, 1993.
 154. Verna, A., A. Scharnel and J.‐M. Pequignot. Long‐term hypoxia increases the number of norepinephrine‐containing glomus cells in the rat carotid body: a correlative immunocytochemical and biochemical study. J. Auton. Nerve Syst. 44: 171–177, 1993.
 155. Vizek, M., C. K. Pickett, and J. V. Weil. Increased carotid body hypoxic sensitivity during acclimatization to hypobaric hypoxia. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 63: 2403–2410, 1987.
 156. Voelkel, N. F. Mechanisms of hypoxic pulmonary vasoconstriction. Am. Rev. Respir. Dis. 133: 1186–1195, 1986.
 157. Wang, W.‐J., G.‐F. Chen, B. G. Dinger, and S. J. Fidone. Effects of hypoxia on cyclic nucleotide‐formation in rabbit carotid body in vitro. Neurosci. Lett. 105: 164–168, 1989.
 158. Wang, Z.‐Z., D. S. Bredt, S. J. Fidone, and L. J. Stensaas. Neurons synthesizing nitric oxide innervate the mammalian carotid body. J. Comp. Neurol. 336: 419–432, 1993.
 159. Wang, Z.‐Z., L. He, L. J. Stensaas, B. G. Dinger, and S. J. Fidone. Localization and in vitro actions of atrial natriuretic peptide in the cat carotid body. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 70: 942–946, 1991.
 160. Wang, Z.‐Z., L. J. Stensaas, W.‐J. Wang, B. G. Dinger, J. De Vente, and S. J. Fidone. Atrial natriuretic peptide increases cyclic guanosine monophosphate immunoreactivity in the carotid body. Neuroscience 49: 479–486, 1992.
 161. Weil, J. V. Ventilatory control at high altitude. In: Handbook of Physiology. The Respiratory System, edited by N. S. Cherniack and J. G. Widdicombe. Washington, DC: Am. Physiol. Soc., 1986, vol. II, p. 703–727.
 162. West, J. B. Life at extreme altitude. In: Handbook of Physiology. Environmental Physiology, edited by M. J. Fregly and C. M. Blatteis. Bethesda, MD: Am. Physiol. Soc., 1994.
 163. Wilding, T. J., B. Cheng, and A. Roos. pH regulation in adult rat carotid body glomus cells: importance of extracellular pH, sodium and potassium. J. Gen. Physiol. 100: 593–608, 1992.
 164. Wilson, D. F., W. L. Rumsey, T. J. Green, and J. M. Vanderkooi. The oxygen dependence of mitochondrial oxidative phosphorylation measured by a new optical method for measuring oxygen concentration. J. Biol. Chem. 263: 2712–2718, 1988.
 165. Wilson, D. F., A. Mokashi, D. Chugh, S. Vinogradov, S. Osanai, and S. Lahiri. The primary oxygen sensor of the cat carotid body is cytochrome a3 of the mitochondrial respiratory chain. FEBS Lett. 351: 370–374, 1994.
 166. Winquist, R. J., E. P. Faison, S. A. Waldman, K. Schwartz, F. Murad, and R. M. Rapport. Atrial natriuretic factor elicits an endothelium independent relaxation and activates particulate guanylate cyclase in vascular smooth muscle. Proc. Natl. Acad. Sci. U.S.A. 81: 7661–7664, 1984.
 167. Winslow, R. M., and C. Monge. Hypoxia, Polycythemia and Chronic Mountain Sickness. Baltimore: Johns Hopkins University Press, 1987.
 168. Wolin, M. S., and T. M. Burke. Hydrogen peroxide elicits activation of bovine pulmonary arterial soluble guanylate cyclase by a mechanism associated with its metabolism by catalase. Biochem. Biophys. Res. Commun. 143: 20–25, 1987.
 169. Wyatt, C. N., C. Wright, D. Bell, and C. Peers. O2‐sensitive K+ currents in carotid body chemoreceptor cells from normoxic and chronically hypoxic rats and their roles in hypoxic chemotransduction. Proc. Natl. Acad. Sci. USA 92: 295–299, 1995.
 170. Zak, F. G., and W. Lawson. The Paraganglionic Chemoreceptor System. New York: Springer‐Verlag, 1982.
 171. Zigmond, R. E., and C. W. Bowers. Influence of nerve activity on the macromolecular content of neurons and their effector organs. Annu. Re. Physiol. 43: 673–687, 1981.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Peripheral Chemoreceptors and Their Sensory Neurons in Chronic States of Hypo‐ and Hyperoxygenation
 

How to Cite

Sukhamay Lahiri. Peripheral Chemoreceptors and Their Sensory Neurons in Chronic States of Hypo‐ and Hyperoxygenation. Compr Physiol 2011, Supplement 14: Handbook of Physiology, Environmental Physiology: 1183-1206. First published in print 1996. doi: 10.1002/cphy.cp040251