Abstract
In rats, a single exposure to 3 MPa nitrogen induces change in motor processes, a sedative action and a decrease in dopamine release in the striatum. These changes due to a narcotic effect of nitrogen have been attributed to a decrease in glutamatergic control and the facilitation of GABAergic neurotransmission involving NMDA and GABAA receptors, respectively. After repeated exposure to nitrogen narcosis, a second exposure to 3 MPa increased dopamine levels suggesting a change in the control of the dopaminergic pathway. We investigated the role of the nigral NMDA and GABAA receptors in changes in the striatal dopamine levels. Dopamine-sensitive electrodes were implanted into the striatum under general anesthesia, together with a guide-cannula for drug injections into the SNc. Dopamine level was monitored by in vivo voltammetry. The effects of NMDA/GABAA receptor agonists (NMDA/muscimol) and antagonists (AP7/gabazine) on dopamine levels were investigated. Rats were exposed to 3 MPa nitrogen before and after five daily exposures to 1 MPa. After these exposures to nitrogen narcosis, gabazine, NMDA and AP7 had no effect on the nitrogen-induced increase in dopamine levels. By contrast, muscimol strongly enhanced the increase in dopamine level induced by nitrogen. Our findings suggest that repeated nitrogen exposure disrupted NMDA receptor function and decreased GABAergic input by modifying GABAA receptor sensitivity. These findings demonstrated a change in the mechanism of action of nitrogen at pressure.
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Abbreviations
- AP7:
-
D-2-amino-7-phosphonoheptonoic acid
- DA:
-
Dopamine
- GABA:
-
Gamma-amino-butyric acid
- MPa:
-
Megapascal (106 Pascal international pressure unit)
- NMDA:
-
N-methyl-d-aspartate
- SNc:
-
Substantia nigra pars compacta
References
Bennett PB, Rostain JC (2003) Inert gas narcosis. In: Brubakk AO, Neuman TS (eds) Bennett and Elliott’s physiology and medecine of diving. Saunders Company Ltd, London, pp 300–322
Rostain JC, Risso JJ, Abraini JH (2006) Toxicité des gaz inertes. I La narcose aux gaz inertes. In: Broussolle B, Méliet JL (eds). Physiologie et Médecine de la Plongée. Ellipse Paris, pp 313–329
Barthelemy-Requin M, Semelin P, Risso JJ (1994) Effect of nitrogen narcosis on extracellular levels of dopamine and its metabolites in the rat striatum, using intracerebral microdialysis. Brain Res 667:1–5
Balon N, Kriem B, Weiss M, Rostain JC (2002) Opposing effects of narcotic gases and pressure on the striatal dopamine release in rats. Brain Res 947:218–224
Dedieu D, Balon N, Weiss M, Risso JJ, Kinkead R, Rostain JC (2004) Microdialysis study of striatal dopaminergic dysfunctions induced by 3 MPa of nitrogen- and helium-oxygen breathing mixtures in freely moving rats. Brain Res 998:202–207
Lavoute C, Weiss M, Rostain JC (2005) Effects of repeated hyperbaric nitrogen-oxygen exposures on the striatal dopamine release and on motor disturbances in rats. Brain Res 1056:36–42
Lavoute C, Weiss M, Rostain JC (2007) The role of NMDA and GABAA receptors in the inhibiting effect of 3 MPa nitrogen on striatal dopamine level. Brain Res 1176:37–44
Wedzony K, Czepiel K, Figal K (2001) Immunohistochemical evidence for localization of NMDAR1 receptor subunit on dopaminergic neurons of rat substantia nigra pars compacta. Pol J Pharmacol 345:523–529
Westerink BH, Santiago M, De Vries JB (1992) The release of dopamine from nerve terminals and dendrites of nigrostriatal neurons induced by excitatory amino acids in conscious rat. Naunyn Schmiedbergs Arch Pharmacol 345:523–529
Christoffersen CL, Meltzer LT (1995) Evidence for N-methyl-d-aspartate and AMPA subtypes of the glutamate receptor on substantia nigra dopamine neurons: possible preferential role for N-methyl-d-aspartate receptors. Neuroscience 67:373–381
Balon N, Dupenloup L, Blanc F, Weiss M, Rostain JC (2003) Nitrous oxide reverses the increase in the striatal dopamine release produced by N-methyl-d-aspartate infusion in the substantia nigra pars compacta in rats. Neurosci Lett 343:174–179
Bolam JP, Smith Y (1990) The GABA and substance P input to dopaminergic neurons in the substantia nigra of the rat. Brain Res 529:57–78
Paladini G, Celada P, Tepper JM (1999) Striatal, pallidal and pars reticulata evoked inhibition of nigrostriatal dopaminergic neurons is mediated by GABA(A) receptors in vivo. Neuroscience 89:799–812
Tepper JM, Martin LP, Anderson DR (1995) GABAA receptor-mediated inhibition of rat substantia nigra dopaminergic neurons by pars reticulate projection neurons. J Neurosci 15:3092–3103
Balon N, Kriem B, Dousset E, Weiss M, Rostain JC (2002) GABA(A) receptors in the pars compacta and GABA(B) receptors in the pars reticulata of rat substantia nigra modulate the striatal dopamine release. Neurochem Res 27:373–379
Little HJ (1996) How has molecular pharmacology contributed to our understanding of the mechanism(s) of general anesthesia? Pharmacol Ther 69:37–58
Lavoute C, Weiss M, Rostain JC (2008) Alterations in nigral NMDA and GABAA receptor control of the striatal dopamine level after repetitive exposures to nitrogen narcosis. Exp Neurol 212(1):63–70
Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates. Academic Press, New York
Forni C (1982) Realization of a new multifiber electrochemical device allowing continuous in vivo measurements of neuromediators. J Neurosci Methods 5:167–171
El Ganouni S, Forni C, Nieoullon A (1987) In vitro and in vivo characterization of the properties of a multifiber carbon electrode allowing long-term electrochemical detection of dopamine in freely moving animals. Brain Res 404:239–256
Rostain JC, Forni C (1995) Effects of high pressures of various gas mixtures on rat striatal dopamine detected in vivo by voltammetry. J Appl Physiol 78:1179–1187
Abraini JH, Rostain JC, Kriem B (1998) Sigmoidal compression rate-dependence of inert gas narcotic potency in rats: implication for lipid vs. protein theories of inert gas action in the central nervous system. Brain Res 19:300–304
Hill L, Davis RH, Selby RP, Pridham A, Malone AE (1933) Deep diving and ordinary diving. In: report of a Committee Appointed by the British Admiralty
Rostain JC, Lavoute C (2010) Inert gas narcosis. In: Sebert P (ed) Comparative high pressure biology. Sciences Publishers, Enfield NH, USA, pp 413–429
Vallée N, Rostain JC, Boussuges A, Risso JJ (2009) Comparison of nitrogen narcosis and helium pressure effects on striatal amino acids: a microdialysis study in rats. Neurochem Res 34(5):835–844
Vallée N, Rostain JC, Risso JJ (2009) How can an inert gas counterbalance a NMDA-induced glutamate release? J Appl Physiol 107:1951–1958
Vallée N, Rostain JC, Risso JJ (2010) A pressurized nitrogen counterbalance to cortical glutamatergic pathway stimulation. Neurochem Res 35:718–726
Lavoute C, Weiss M, Rostain JC (2006) Effects of NMDA administration in the substantia nigra pars compacta on the striatal dopamine release before and after repetitive exposures to nitrogen narcosis in rats. Undersea Hyperb Med 33(3):175–179
Rostain JC, Lavoute C, Risso JJ, Vallée N, Weiss M (2011) A review of recent neurochemical data on inert gas narcosis. Undersea Hyperb Med 38(1):49–59
Meltzer LT, Christoffersen CL, Serpa KA (1997) Modulation of dopamine neuronal activity by glutamate receptor subtypes. Neurosci Biobehav Rev 21:511–518
Hebb MO, Robertson HA (2000) Identification a population of substantia nigra pars compacta gamma-aminobutyric acid neurons that is regulated by basal ganglia activity. J Comp Neurol 416:30–44
Seutin V, Engel D (2009) Difference in NA+ conductance density and Na+ channel functional properties between dopamine and GABA neurons in the rat substantia nigra. J Neurophysiol 193:3009–3014
Daniels S, Grossman Y (2003) Biological effects of pressure. In: Brubakk AO, Neuman TS (eds) Bennett and Elliott’s Physiology and Medecine of Diving. Saunders Compagny Ltd, London, pp 265–299
Yamakura T, Harris RA (2000) Effects of gaseous anesthetics nitrous oxide and xenon on ligand-gated ion channels Comparison with isoflurane and ethanol. Anesthesiol 93:1095–1101
Franks NP, Lieb WR (1994) Molecular and cellular mechanisms of general anesthesia. Nature 367:607–617
Colloc’h N, Sopkova-de Oliveira Santos J, Retailleau P, Vivarès D, Bonneté F, Langlois d’Estainto B, Gallois B, Brisson A, Risso JJ, Lemaire M, Prangé T, Abraini JH (2007) Protein crystallography under xenon and nitrous oxide pressure: comparison with in vivo pharmacology studies and implications for the mechanism of inhaled anesthetic action. Biophys J 92(1):217–224
Santiago M, Westerink BH (1992) The role of GABA receptors in the control of nigrostriatal dopaminergic neurons: dual-probe microdialysis study in awake rats. Eur J Pharmacol 219(2):175–181
Yamauchi T, Hori T, Takahashi T (2000) Presynaptic inhibition by muscimol through GABAB receptors. Eur J Neurosci 12(9):3433–3436
Girard E, Marchal S, Perez J, Finet S, Kahn R, Fourme R, Marassio G, Dhaussy AC, Prangé T, Giffard M, Dulin F, Bonneté F, Lange R, Abraini JH, Mezouar M, Colloc’h N (2010) Structure-function perturbation and dissociation of tetrameric urate oxidase by high hydrostatic pressure. Biophys J 98(10):2365–2373
Marassio G, Prangé T, David HN, Sopkova-de Oliveira Santos J, Gabison L, Delcroix N, Abraini JH, Colloc’h N (2011) Pressure-response analysis of anesthetic gases xenon and nitrous oxide on urate oxidase: a crystallographic study. FASEB J 25(7):2266–2275
Devaud LL, Fritschy JM, Sieghart W, Morrow AL (1997) Bidirectional alterations of GABA(A) receptor subunit peptide levels in rat cortex during chronic ethanol consumption and withdrawal. J Neurochem 69:126–130
Mhatre MC, Pane G, Sieghart W, Ticku MK (1993) Antibodies specific for GABAA receptor alpha subunits reveal that chronic alcohol treatment down-regulates alpha-subunit expression in rat brain regions. J Neurochem 61:1620–1625
Cagetti E, Liang J, Spigelman I, Olsen RW (2003) Withdrawal from chronic intermittent ethanol treatment changes subunit composition, reduces synaptic function, and decreases behavioral responses to positive allosteric modulators of GABAA receptors. Mol Pharmacol 63:53–64
Biggio G, Dazzi L, Biggio F, Mancuso L, Talani G, Busonero F, Mostallino MC, Sanna E, Follesa P (2003) Molecular mechanisms of tolerance to and withdrawal of GABAA receptor modulators. Eur Neuropsychopharmacol 13:411–413
Ortiz J, Fitzgerald LW, Charlton M, Lane S, Trevisan L, Guitart X, Shoemaker W, Duman RS, Nestler EJ (1995) Biochemical actions of chronic ethanol exposure in the mesolimbic dopamine system. Synapse 21:289–298
Liang J, Cagetti E, Olsen RW, Spigelman I (2004) Altered pharmacology of synaptic and extrasynaptic GABAA receptors on CA1 hippocampal neurons is consistent with subunit changes in a model of alcohol withdrawal and dependence. J Pharmacol Exp Ther 310:1234–1345
Hamilton K, Laliberté MF, Fowler B (1995) Dissociation of the behavioral and subjective components of nitrogen narcosis and diver adaptation. Undersea Hyperb Med 22:41–49
Acknowledgments
This study was supported by a research grant from the Direction Générale de l’Armement, Paris, France. PEA no. 010809/06Co024.
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Lavoute, C., Weiss, M., Risso, JJ. et al. Mechanism of Action of Nitrogen Pressure in Controlling Striatal Dopamine Level of Freely Moving Rats is Changed by Recurrent Exposures to Nitrogen Narcosis. Neurochem Res 37, 655–664 (2012). https://doi.org/10.1007/s11064-011-0657-1
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DOI: https://doi.org/10.1007/s11064-011-0657-1