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Dopamine, Neurochemical Processes, and Oxygen Toxicity at Pressure

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ABSTRACT

All mammals, including man, exposed to breathing gas mixtures at high pressures exhibit central nervous system disturbances, which differ according to the gas used. With the use of compressed air, the increased oxygen partial pressure induces hyperoxic disturbances that consist of epileptic seizures that occur, on average, after 30 min exposure to 2.8 ATA in man or to 5 ATA in rats. Increased oxygen partial pressure induces reactive oxygen species and reactive nitrogen species production that could be related to neurotransmitter changes reported for the preepileptic phase or at pressures that produce epileptic seizures. In rats, oxygen pressures lower than 5 ATA induce a decrease of dopamine release in the stratum that could be due to disturbances of neurotransmitter regulatory processes that are different from those implicated for hyperbaric oxygen‐induced epileptic seizures. © 2016 American Physiological Society. Compr Physiol 6:1339‐1344, 2016.

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Figure 1. Figure 1. Relationships between depth of sea water, absolute pressure, relative pressure, and oxygen or nitrogen partial pressure.
Figure 2. Figure 2. Consequences of the increase of pressure and partial pressure of breathing gas mixtures on biological and physiological systems.
Figure 3. Figure 3. Maximal decrease in DA level recorded in striatum of rats by differential pulse voltametry during different exposures at 1, 2, 3, and 4 ATA. Results are expressed in percentage difference from control value.
Figure 4. Figure 4. Changes in striatal DA level during exposure to 5 ATA oxygen before and after hyperoxic epileptic seizure comparatively to control values. Results are expressed in percentage difference from control value.


Figure 1. Relationships between depth of sea water, absolute pressure, relative pressure, and oxygen or nitrogen partial pressure.


Figure 2. Consequences of the increase of pressure and partial pressure of breathing gas mixtures on biological and physiological systems.


Figure 3. Maximal decrease in DA level recorded in striatum of rats by differential pulse voltametry during different exposures at 1, 2, 3, and 4 ATA. Results are expressed in percentage difference from control value.


Figure 4. Changes in striatal DA level during exposure to 5 ATA oxygen before and after hyperoxic epileptic seizure comparatively to control values. Results are expressed in percentage difference from control value.
References
 1.Adachi YU, Watanabe K, Higuchi H, Satoh T, Vizi ES. Oxygen inhalation enhances striatal dopamine metabolism and monoamineoxidase enzyme inhibition prevents it: A microdialysis study. Eur J Pharmacol 422: 61‐68, 2001.
 2.Ames BN, Shigenage MK, Hagen TM. Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci U S A 90: 7915‐7922, 1993.
 3.Bean JW. Reserpine, chlorpromazine and the hypothalamus in reactions to oxygen at high pressure. Am J Physiol 187: 389‐394, 1956.
 4.Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 271(5 Pt 1): C1424‐C1437, 1996.
 5.Bitterrman N. CNS oxygen toxicity. Undersea Hyperbaric Med 31(1): 63‐72, 2004.
 6.Brennan ML, Wu W, Fu X, Shen Z, Song W, Frost H, Vadseth C, Narine L, Lenkiewicz E, Borchers MT, Lusis AJ, Lee JJ, Lee NA, Abu‐Soud HM, Ischiropoulos H, Hazen SL. A tale of two controversies: Defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase‐deficient mice, and the nature of peroxidase‐generated reactive nitrogen species. J Biol Chem. 277(20): 17415‐17427, 2002.
 7.Bruzzese L, Rostain JC, Née L, Condo J, Mottola G, Adjriou N, Mercier L, Bergé‐Lefranc JL, Fromonot J, Kipson N, Lucciano M, Durand‐Gorde JM, Jammes Y, Guieu R, Ruf J, Fenouillet E. Effect of hyperoxic and hyperbaric conditions on the adenosinergic pathway and CD26‐expression in rat. J Appl Physiol 119: 140‐147, 2015.
 8.Clark JM, Thom SR. Oxygen under pressure. In: Brubback AO, Neuman TS, editors. Bennett and Elliott's Physiology and Medicine of Diving. New York: Saunders, Elsevier, 2003, pp. 358‐418.
 9.Cohn R, Gersh I. Changes in brain potentials during convulsions induced by oxygen under pressure. J Neurophysiol 8: 155‐160, 1945.
 10.Colton CA, Colton JS. Blockade of hyperbaric oxygen induced seizures by excitatory amino acid antagonists. Can J Physiol Pharmacol 63: 519‐521, 1985.
 11.Colton CA, Colton JS. The action of oxygen and oxygen at high pressure on inhibitory transmission. Brain Res 364: 151‐158, 1986.
 12.Courtiere A, Reybaud J, Camilla C, Lobert P, Drouet J, Jadot G. Oxygen‐induced modifications of benzodiazepine receptors and D2 dopamine receptors in rat under hyperoxia. Free Radic Res Commun 15: 29‐34, 1991.
 13.Cox BA, Johnson SW. Nitric oxide facilitates N‐methyl‐D‐aspartate‐induced burst firing in dopamine neurons from rat midbrain slices. Neurosci Lett 255: 131‐134, 1998.
 14.D'Agostino DP, Putnam RW, Dean JB. Superoxyde (*O2−) production in CA1 neurons of rat hippocampal slices exposed to graded levels of oxygen. J Neurophysiol 98: 1030‐1041, 2007. doi:10.1152/jn010003.2006.
 15.Davies KJ. Oxidative stress: the paradox of aerobic life. Biochem Soc Symp 61: 1‐31, 1995.
 16.Davis HC, Davis RE. Biochemical aspects of oxygen poisoning. In: Fenn WO, Rahn H, editors. Handbook of Physiology. Respiration. Bethesda, MD: Am. Physiol. Soc., 1965, Sec. 3, Vol. 2, pp. 1047‐1058.
 17.Dawson VL, Dawson TM, London ED, Bredt DS, Snyder SH. Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc Natl Acad Sci U S A. 88(14): 6368‐6371, 1991.
 18.Dean JB, Mulkey DK, Henderson RA III, Potter SJ, Putnam RW. Hyperoxia, reactive oxygen species, and hyperventilation: Oxygen sensitivity of brain stem neurons. J Appl Physiol 96: 784‐791, 2004. doi:10.1152/japplphysiol.00892.2003.
 19.Demchenko IT, Atochin DN, Boso AE, Astern J, Huang PL, Piantadosi CA. Oxygen seizure latency and peroxynitrite formation in mice lacking neuronal or endothelial nitric oxide syntheses. Neurosci Lett 344: 53‐56, 2003.
 20.Demchenko IT, Boso AE, O'Neill TJ, Bennett PB, Piantadosi CA. Nitric oxide and cerebral blood flow responses to hyperbaric oxygen. J Appl Physiol 88: 1381‐1389, 2000.
 21.Demchenko IT, Boso AE, Whorton AR, Piantadosi CA. Nitric oxide production is enhanced in rat brain before oxygen induced convulsions. Brain Res 17: 253‐261, 2001.
 22.Demchenko IT, Piantadosi CA. Nitric oxide amplifies the excitatory to inhibitory neurotransmitter imbalance accelerating oxygen seizure. Undersea Hyperb Med 33(3): 169‐174, 2006.
 23.Diaz PM, Ngai SH, Costa E. Effect of oxygen on brain serotonin metabolism in rats. Am J Physiol 214: 591‐594, 1968.
 24.Dröge W. Free radicals in the physiological control of cell function. Physiol Rev 82: 47‐95, 2002.
 25.During MJ, Spencer DD. Extracellular hippocampal glutamate and spontaneous seizure in the conscious human brain. Lancet 6(341): 1607‐1610, 1993.
 26.Elayan JM, Axley MJ, Prassad PV, Ahlers ST, Auker CR. Effect of hyperbaric oxygen treatment on nitric oxide and oxygen free radicals in rat brain. J Neurophysiol 83: 2022‐2029, 2000.
 27.Eyring H, Woodbury JW, D'Arrigo J. A molecular mechanism of general anesthesia. Anesthesiology 38: 415‐424, 1973.
 28.Faiman MD, Hable A, Mehl RG. Hyperbaric oxygenation and brain norepinephrine and 5‐hydroxytryptamine: Oxygen pressure interactions. Life Sci 8(21): 1163‐1178, 1969.
 29.Faiman MD, Mehl RG, Myers MB. Brain norepinephrine and serotonin in central oxygen toxicity. Life Sci 10(1): 21‐34, 1971.
 30.Faiman MD, Nolan RJ, Baxter CF, Dodd DE. Brain gamma‐aminobutyric acid, glutamic acid decarboxylase, glutamate, and ammonia in mice during hyperbaric oxygenation. J Neurochem 28: 861‐865, 1977.
 31.Forni C, Rostain JC. Effect of helium‐oxygen pressure on dopamine detected in vivo in the striatum of hamsters. J Appl Physiol 67: 1617‐1622, 1989.
 32.Gibbs FA, Davis H, Lennox WG. The electroencephalogram in epilepsy and in conditions of impaired consciousness. Arch Neurol Psychiatr 34: 1133‐1148, 1935.
 33.Globus MY, Prado R, Sanchez‐Ramos J, Zhao W, Dietrich WD, Busto R, Ginsberg MD. A dual role for nitric oxide in NMDA‐mediated toxicity in vivo. J Cereb Blood Flow Metab. 15(6): 904‐913, 1995.
 34.Gosset A. Traitement par l'hyperbarie des embolies gazeuses cérébrales chez le singe Papio papio. Medical Doctor Thesis. Aix‐Marseille II, Marseille. 1966, p. 161.
 35.Hagioka S, Takeda Y, Zhang S, Sato T, Morita K. Effects of 7‐nitroindazole and N‐nitro‐I‐arginine methyl ester on changes in cerebral blood flow and nitric oxide production preceding development of hyperbaric oxygen‐induced seizures in rats. Neurosci Lett 382: 206‐210, 2005.
 36.Halliwell B. Oxidative stress and neurodegeneration: Where are we now? Review. J Neurochem 97(6): 1634‐1658, 2006.
 37.Harel D, Kerem J, Lavy S. The influence of high oxygen pressure on the electrical activity of the brain. Electroencephalogr Clin Neurophysiol 27(2): 219, 1969.
 38.Haugaard N. Cellular mechanisms of oxygen toxicity. Physiol Rev 48:11‐373, 1968.
 39.Huggins AK, Nelson DR. The effects of hyperbaric oxygenation on the levels of 5‐hydroxytryptamine, noradrenaline, dopamine and free amino acids in whole mouse brain. J Neurochem 25: 117‐121, 1975.
 40.Jamieson D, Chance B, Cadenas E, Boveris A. The relation of free radical production to hyperoxia. Annu Rev Physiol 48:703‐719, 1986.
 41.Kovachich GB, Haugaard N. Biochemical aspects of oxygen toxicity in the metazoa. In: Gilbert DL, editor. Oxygen and Living Processes: An Interdisciplinary Approach. New York, Springer, 1981, pp. 210‐234.
 42.Lakshmi VM, Nauseef WM, Zenser TV. Myeloperoxidase potentiates nitric oxide‐mediated nitrosation. J Biol Chem 280(3): 1746‐1753, 2005.
 43.Lambertsen CJ. Effects of oxygen at high partial pressure. In: Fenn WO, Rahn H, editors. Handbook of Physiology, Respiration, Sec. 3, Vol. II. Washington DC, American Physiological Society, 1965, pp. 1027‐1046.
 44.Lavoute C, Weiss M, Risso JJ, Rostain JC. Preliminary results about GABAergic neurotransmission involvement in dopaminergic changes under hyperoxia in pre‐epileptic phase in freely moving rats. Undersea Hyperbaric Med 36(4): 268, 2009.
 45.Lavoute C, Weiss M, Risso JJ, Rostain JC. Alteration of striatal dopamine levels under various partial pressure of oxygen in pre‐convulsive and convulsive phases in freely‐moving rats. Neurochem Res 39(2): 287‐294, 2014. doi: 10.1007/s11064‐013‐1220‐z.
 46.Li Q, Guo M, Xu X, Xiao X, Xu W, Sun X, Tao H, Li R. Rapid decrease of GAD 67 content before the convulsion induced by hyperbaric oxygen exposure. Neurochem Res 33(1): 185‐193, 2008.
 47.Mailly F, Marin P, Israël M, Glowinski J, Prémont J. Increase in external glutamate and NMDA receptor activation contribute to H2O2‐induced neuronal apoptosis. J Neurochem 73(3): 1181‐1188, 1999.
 48.Mialon P, Joanny P, Gibey R, Cann‐Moisan C, Caroff J, Steinberg J, Barthélémy L. Amino acids and ammonia in the cerebral cortex, the corpus striatum and the brain stem of the mouse prior to the onset and after a seizure induced by hyperbaric oxygen. Brain Res 676: 352‐357, 1995.
 49.Miyazaki I, Asanuma M. Dopaminergic neuron‐specific oxidative stress caused by dopamine itself. Acta Med Okayama 62: 141‐150, 2008.
 50.Omoi NO, Arai M, Saito M, Takatsu H, Shibata A, Fukuzawa K, Sato K, Abe K, Fukui K, Urano S. Influence of oxidative stress on fusion of pre‐synaptic plasma membranes of the rat brain with phosphatidyl choline liposomes, and protective effect of vitamin E. J Nutr Sci Vitaminol (Tokyo) 52: 248‐255, 2006.
 51.Radomski MW, Watson WJ. Effect of lithium on acute oxygen toxicity and associated changes in brain gamma‐aminobutyric acid. Aerosp Med 44(4): 387‐392, 1973.
 52.Rogawski MA. The NMDA receptor, NMDA antagonists and epilepsy therapy. A status report. Drugs 44(3): 279‐292, 1992.
 53.Rostain JC, Montmayeur A, Louge P, Robinet C, Meliet JM. Comparative studies of EEG changes of two diver populations during a long period of oxygen breathing. Undersea and Hyperbaric Med 28(Suppl.): 41, 2001.
 54.Rucci FS, Giretti ML, La Rocca M. Changes in electrical activity of the cerebral cortex and of some subcortical centers in hyperbaric oxygen. Electroencephalogr Clin Neurophysiol 22(3): 231‐238, 1967.
 55.Sampson JB, Ye Y, Rosen H, Beckman JS. Myeloperoxidase and horseradish peroxidase catalyze tyrosine nitration in proteins from nitrite and hydrogen peroxide. Arch Biochem Biophys 356(2): 207‐213, 1998.
 56.Sato T, Takeda Y, Hagioka S, Zhang S, Hirakawa M. Changes in nitric oxide production and cerebral blood flow before development of hyperbaric oxygen‐induced seizures in rats. Brain Res 918: 131‐140, 2001.
 57.Sies H. Oxidative stress: Introduction. In: Sies H, editor. Oxidative Stress: Oxidants and Antioxidants. London: Academic Press, 1991, p. 650.
 58.Smith WL. Cyclooxygenases, peroxide tone and the allure offish oil. Curr Opin Cell Biol 17, 174‐182, 2005.
 59.Thom SR. Hyperbaric oxygen therapy. In: Sebert P, editor. Comparative High Pressure Biology. Enfield NH USA: Science Publishers, 2010, pp. 465‐501.
 60.Thom SR, Bhopale V, Fisher D, Manevich Y, Huang PL, Buerk DG. Stimulation of nitric oxide synthase in cerebral cortex due to elevated partial pressures of oxygen: an oxidative stress response. J Neurobiol 51(2): 85‐100, 2002.
 61.Torbati D, Simon AJ, Ranade A. Frequency analysis of EEG in rats during the preconvulsive period of O2 poisoning. Aviat Space Environ Med 52: 598‐603, 1981.
 62.Tunnicliff G, Urton M, Wood JD. Susceptibility of chick brain L‐glutamic acid decaboxylase and other neurotransmitter enzymes to hyperbaric oxygen in vitro. Biochem Pharmacol 22: 501‐505, 1973.
 63.Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39(1): 44‐84, 2007.
 64.Vallée N, Rostain JC, Boussuges A, Risso JJ. Comparison of nitrogen narcosis and helium pressure effects on striatal amino acids: A microdialysis study in rats. Neurochem Res 34(5): 835‐844, 2009. doi: 10.1007/s11064‐008‐9827‐1.
 65.West AR, Galloway MP. Nitric oxide and potassium chloride‐facilitated striatal dopamine efflux in vivo: Role of calcium‐dependant release mechanisms. Neurochem Int 33: 493‐501, 1998.
 66.Wood JD, Watson WJ. Gamma‐aminobutyric acid levels in the brain of rats exposed to oxygen at high pressures. Can J Biochem Physiol 41: 1907‐1913, 1963.
 67.Wood JD, Watson WJ, Murray GW. Correlation between decrease in brain γ‐aminobutyric acid levels and susceptibility to convulsions induced by hyperbaric oxygen. J Neurochem 16: 281‐287, 1969.
 68.Zhang J, Su Y, Oury TD, Piantadosi CA. Cerebral amino acid, norepinephrine and nitric oxide metabolism in CNS oxygen toxicity. Brain Res 606: 56‐62, 1993.
 69.Zhilyaev SY1, Moskvin AN, Platonova TF, Gutsaeva DR, Churilina IV, Demchenko IT. Hyperoxic vasoconstriction in the brain is mediated by inactivation of nitric oxide by superoxide anions. Neurosci Behav Physiol 33(8): 783‐787, 2003.
 70.Zirkle LG, Mengel CE, Horton BD, Duffy EJ. Studies of oxygen toxicity in the central nervous system. Aerosp Med 36:1027‐1032, 1965.

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How to Cite

Jean‐Claude Rostain, Cécile Lavoute. Dopamine, Neurochemical Processes, and Oxygen Toxicity at Pressure. Compr Physiol 2016, 6: 1339-1344. doi: 10.1002/cphy.c140025