Hyperbaric hyperoxia and normobaric reoxygenation increase excitability and activate oxygen-induced potentiation in CA1 hippocampal neurons

Journal of Applied Physiology

Volumn 109, Issue 3, 2010, Pages 804-819

  Garcia III, Alfredo J ^a   Putnam, Robert W ^b   Dean, Jay B ^c  

^a SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

^b WRIGHT STATE UNIVERSITY   (United States)

^c UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

Hyperbaric oxygen; Neural plasticity; Oxidative stress; Oxygen toxicity

Indexed keywords

OXYGEN;

ACTION POTENTIAL; ANIMAL; ARTICLE; HIPPOCAMPAL CA1 REGION; HYPERBARIC OXYGEN; HYPEROXIA; IN VITRO STUDY; INSTRUMENTATION; ION SELECTIVE ELECTRODE; MALE; METABOLISM; NERVE CELL; NERVE CELL PLASTICITY; PATHOPHYSIOLOGY; POLAROGRAPHY; PRESSURE; RAT; SPRAGUE DAWLEY RAT; TIME;

ACTION POTENTIALS; ANIMALS; CA1 REGION, HIPPOCAMPAL; HYPERBARIC OXYGENATION; HYPEROXIA; ION-SELECTIVE ELECTRODES; MALE; NEURONAL PLASTICITY; NEURONS; OXYGEN; POLAROGRAPHY; PRESSURE; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 77957147471     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.91429.2008     Document Type: Article

References (88)

1. Aitken PG, Breese GR, Dudek FF, Edwards F, Espanol MT, Larkman PM, Lipton P, Newman GC, Nowak T S J, Panizzon KL. Preparative methods for brain slices: a discussion. J Neurosci Methods 59:139-149. 1995.
2. Alger BE, Dhanjal SS, Dingledine R, Garthwaite J, Henderson G, King GL, Lipton P, North A, Schwartzkronin PA, Sears TA, Segal M, Whittingham TS, Williams J. Appendix, brain slice methods. In: Brain Slices, edited by Dingledine R. New York: Plenum, 1984, p. 381-437.
3. 2 toxicity in the rat. Eur J Appl Physiol 75:182-187, 1997.
4. Atkins CM, Sweatt JD. Reactive oxygen species mediate activity-dependent neuron-glia signaling in output fibers of the hippocampus. J Neurosci 19:7241-7248, 1999.
5. 2 underlies glutamate-dependent inhibition of striatal dopamine release. Proc Natl Acad Sci USA 100:11729-11734, 2003.
6. Avshalumov MV, Rice ME. NMDA receptor activation mediates hydrogen peroxide-induced pathophysiology in rat hippocampal slices. J Neurophysiol 87:2896-2903, 2002.
7. Balentine JD. Pathology of Oxygen Toxicity. New York: Academic, 1982.
8. Bennett P, Papahadjopoulos D, Bangham A. The effect of raised pressure of inert gases on phospholipid membranes. Life Sci 6:2527-2533, 1967.
9. o2 profiles in hippocampal slices of the guinea pig. Exp Brain Res 48:89-96, 1982.
10. Brahma B, Forman RE, Stewart E, Rice ME. Ascorbate inhibits edema in brain slices. J Neurochem 74:1263-1270, 2000.
11. Brauer RW, Hogan PM, Hugon M, Macdonald AG, Miller KW. Patterns of interaction of effects of light metabolically inert gases with those of hydrostatic pressure as such-a review. Undersea Biomed Res 9:353-396, 1982.
12. Butterfield DA, Koppal T, Howard B, Subramaniam R, Hall N, Hensley K, Yatin S, Allen K, Aksenov M, Aksenova M, Carney J. Structural and functional changes in proteins induced by free radicalmediated oxidative stress and protective action of the antioxidants N-tertbutyl-alpha-phenylnitrone and vitamin E. Ann NY Acad Sci 854:448-462, 1998.
13. Buzsaki G, Freund TF, Bayardo F, Somogyi P. Ischemia-induced changes in the electrical activity of the hippocampus. Exp Brain Res 78:268-278, 1989.
14. Cater D, Garattini S, Marina F, Silver I. Changes of oxygen tension in brain and somatic tissues induced by vasodilator and vasoconstrictor drugs. Proc R Soc Land B Biol Sci 155:136-157, 1961.
15. Chang HS, Sasaki T, Kassell NF. Hippocampal unit activity after transient cerebral ischemia in rats. Stroke 20:1051-1058, 1989.
16. Cragg PA, Drysdale DB, Hamilton JH. Ventilation in intact and glossopharyngeal nerve sectioned anaesthetized rats exposed to oxygen at high pressure. J Physiol 370:489-499, 1986.
17. Crepel V, Hammond C, Chinestra P, Diabira D, Ben-Ari Y. A selective LTP of NMDA receptor-mediated currents induced by anoxia in CA1 hippocampal neurons. J Neurophysiol 70:2045-2055, 1993.
18. Crepel V, Hammond C, Krnjevic K, Chinestra P, Ben-Ari Y. Anoxiainduced LTP of isolated NMDA receptor-mediated synaptic responses. J Neurophysiol 69:1774-1778, 1993.
19. D'Agostino DP, Colomb DG, Dean JB. Effects of hyperbaric gases on membrane nanostructure and function in neurons. J Appl Physiol 106:996-1003, 2009.
20. D'Agostino DP, Olson JE, Dean JB. Acute hyperoxia increases lipid peroxidation and induces plasma membrane blebbing in human U87 glioblastoma cells. Neuroscience 159:1011-1022, 2009.
21. -) production in CA1 neurons of rat hippocampal slices exposed to graded levels of oxygen. J Neurophysiol 98:1030-1041, 2007.
22. Dean JB, D'Agostino DP. Pressure effects on human physiology. In: Physiology and Medicine of Hyperbaric Oxygen Therapy, edited by Newman T and Thorn S. Philadelphia, PA: Elsevier, 2008, p. 189-202.
23. Dean JB, D'Agostino DP, Landon C, Matott M, Hartzler LK, Putnam RW. Superoxide production increases in nucleus tractus solitarius (NTS) neurons in rat brain slices during acute normobaric hyperoxia and hypoxia. Soc Neurosci Abstr. Program No. 481.20, 2008.
24. Dean JB, Mulkey DK. Continuous intracellular recording from mammalian neurons exposed to hyperbaric helium, oxygen, or air. J Appl Physiol 89:807-822, 2000.
25. Dean JB, Mulkey DK, Garcia III AJ, Putnam RW, Henderson III RA. Neuronal sensitivity to hyperoxia, hypercapnia and inert gases at hyperbaric pressures. J Appl Physiol 95:883-909, 2003.
26. Dean JB, Mulkey DK, Arehart JD. Details on building a hyperbaric chamber for intracellular recording in brain tissue slices. J Appl Physiol 89:807-822, 2000. [Supplemental Material for Ref. 24]
27. Demchenko IT, Boso AE, Whorton AR, Piantadosi CA. Nitric oxide production is enhanced in rat brain before oxygen-induced convulsions. Brain Res 917:253-261, 2001.
28. Dingledine R, Dodd J, Kelly JS. The in vitro brain slice as a useful neurophysiological preparation for intracellular recording. J Neurosci Methods 2:323-362, 1980.
29. DiScenna P. Method and myth in maintaining brain slices. Brain Slices: Fundamentals, Applications, and Implications, edited by Schurr A. Louisville, KY: Karger, 1987, p. 10-21.
30. Fagni L, Soumireu-Mourat B, Carlier E, Hugon M. A study of spontaneous and evoked activity in the rat hippocampus under heliumoxygen high pressure. Electroencephalogr Clin Neurophysiol 60:267-275, 1985.
31. Fagni L, Zinebi F, Hugon M. Helium pressure potentiates the N-methyl-D-aspartate-and D, L-homocysteate-induced decreases of field potentials in the rat hippocampal slice preparation. Neurosci Lett 81:285-290, 1987.
32. Fessel J, Arbeson WC, Winder D, Roberts LJ. Standard brain slice protocols result in oxidative injury in hippocampal brain slices (Abstract). Free Radic Biol Med 33: S433, 2002.
33. Fowler JC. Changes in extracellular adenosine levels and population spike amplitude during graded hypoxia in the rat hippocampal slice. Naunyn Schmiedebergs Arch Pharmacol 347:73-78, 1993.
34. Fowler JC, Gervitz LM, Hamilton ME, Walker JA. Systemic hypoxia and the depression of synaptic transmission in rat hippocampus after carotid artery occlusion. J Physiol 550:961-972, 2003.
35. Freiberger JJ, Suliman HB, Sheng H, McAdoo J, Piantadosi CA, Warner DS. A comparison of hyperbaric oxygen versus hypoxic cerebral preconditioning in neonatal rats. Brain Res 1075:213-222, 2006.
36. Friedman JE, Haddad GG. Anoxia induces an increase in intracellular sodium in rat central neurons in vitro. Brain Res 663:329-334, 1994.
37. +-dependent mechanisms. Brain Res 762:97-102, 1997.
38. Furukawa K, Yamana K, Kogure K. Postischemic alterations of spontaneous activities in rat hippocampal CA1 neurons. Brain Res 530:257-260, 1990.
39. Gao TM, Xu ZC. In vivo intracellular demonstration of an ischemiainduced postsynaptic potential from CA1 pyramidal neurons in rat hippocampus. Neuroscience 75:665-669, 1996.
40. Garcia AJ III, Putnam RW, Dean JB. Hyperoxic stimulation of synchronous orthodromic activity and induction of neural plasticity does not require changes in excitatory synaptic transmission. J Appl Physiol (June 17, 2010). doi:10.1152/japplphysiol.91430.2008.
41. Gennser M, Blogg SL. Oxygen or carbogen breathing before simulated submarine escape. J Appl Physiol 104:50-56, 2008.
42. Graulick J, Hoffmann U, Maier RF, Ruscher K, Pomper JK, Ko HK, Gabriel S, Obladen M, Heinemann U. Acute neuronal injury after hypoxia is influenced by the reoxygenation mode in juvenile hippocampal slice cultures. Dev Brain Res 137:35-42, 2002.
43. Hajos N, Ellender TJ, Zemankovics R, Mann EO, Exley R, Cragg SJ, Freund TF, Paulsen O. Maintaining network activity in submerged hippocampal slices: importance of oxygen supply. Eur J Neurosci 29:319-327, 2009.
44. Hoffmann U, Pomper J, Graulich J, Zeller M, Schuchmann S, Gabriel S, Maier RF, Heinemann U. Changes of neuronal activity in areas CA1 and CA3 during anoxia and normoxic or hyperoxic reoxygenation in juvenile rat organotypic hippocampal slice cultures. Brain Res 1069:207-215, 2006.
45. Hunt R, Blackburn J, Ogilvie R, Balentine D. Oxygen tension in the globus pallidus and neostriatum of unanesthetized rats during exposure to hyperbaric oxygen. Exp Neurol 62:698-707, 1978. (Pubitemid 9083376)
46. Imon H, Mitani A, Andou Y, Arai T, Kataoka K. Delayed neuronal death is induced without postischemic hyperexcitability: continuous multiple-unit recording from ischemic CA1 neurons. J Cereb Blood Flow Metab 11:819-823, 1991.
47. Jamieson D, Van den Brenk A. Measurement of oxygen tensions in cerebral tissues of rats exposed to high pressures of oxygen. J Appl Physiol 18:869-876, 1963.
48. Jensen MS, Azouz R, Yaari Y. Variant firing patterns in rat hippocampal pyramidal cells modulated by extracellular potassium. J Neurophysiol 71:831-839, 1994.
49. Jensen MS, Yaari Y. Role of intrinsic burst firing, potassium accumulation, and electrical coupling in the elevated minpotassium model of hippocampal epilepsy. J Neurophysiol 77:1224-1233, 1997.
50. King GL, Parmentier JL. Oxygen toxicity of hippocampal tissue in vitro. Brain Res 260:139-142, 1983.
51. Klann E, Roberson E, Knapp L, Sweatt J. A role for superoxide in protein kinase C activation and induction of long-term potentiation. J Biol Chem 273:4516-4522, 1998.
52. Krnjevic K. Electrophysiology of cerebral ischemia. Neuropharmacology 55:319-333, 2008.
53. + activity accompanying hippocampal discharges. Can J Physiol Pharmacol 58:579-582, 1980.
54. Krnjevic K, Xu Y. Mechanisms underlying anoxic hyperpolarization of hippocampal neurons. Can J Physiol Pharmacol 68:1609-1613, 1990.
55. Le Fevre ME. Calibration of Clark oxygen electrode for use in aqueous solutions. J Appl Physiol 26:844-846, 1969.
56. Lei SZ, Pan ZH, Aggarwal SK, Chen HS, Hartman J, Sucher NJ, Lipton SA. Effect of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex. Neuron 8:1087-1099, 1992.
57. Lipton P. Ischemic cell death in brain neurons. Physiol Rev 79:1431-1568, 1999.
58. Lynch MA. Long-term potentiation and memory. Physiol Rev 84:87-136, 2004.
59. MacDonald AG. Hydrostatic pressure as an environmental factor in life processes. Comp Biochem Physiol 116 A: 291-297, 1997.
60. MacDonald AG, Fraser PJ. The transduction of very small hydrostatic pressures. Comp Biochem Physiol 122 A 13-36, 1999.
61. Mahon RT, Dainer HM, Gibellato MG, SES. Short oxygen pre-breathe periods reduce or prevent severe decompression sickness in a 70kg swine saturation model. J Appl Physiol 106:1459-1463, 2009.
62. Mor A, Grossman Y. High pressure modulation of NMDA receptor dependent excitability. Eur J Neurosci 25:2045-2052, 2007.
63. Mor A, Grossman Y. Modulation of isolated N-methyl-D-aspartate receptor response under hyperbaric conditions. Eur J Neurosci 24:3453-3462, 2006.
64. Mulkey DK, Henderson RA, Olson JE, Putnam RW, Dean JB. Oxygen measurements in brain stem slices exposed to normobaric hyperoxia and hyperbaric oxygen. J Appl Physiol 90:1887-1899, 2001.
65. +-sensitive neurons in rat brain stem slices. J Appl Physiol 95:910-921, 2003.
66. Mulkey DK, Henderson RA, Putnam RW, JBD. Pressure (<4 ATA) increases membrane conductance and firing rate in the rat solitary complex. J Appl Physiol 95:922-930, 2003.
67. Noda Y, McGeer PL, McGeer EG. Lipid peroxide distribution in brain and the effect of hyperbaric oxygen. J Neurochem 4:1329-1332, 1983.
68. Offenhauser N, Thomsen K, Caesar K, Lauritzen M. Activity-induced tissue oxygenation changes in rat cerebellar cortex: interplay of postsynaptic activation and blood flow. J Physiol 565:279-294, 2005.
69. o2. Physiol Meas 25:1413-1423, 2004.
70. Pittenger C, Kandel ER. In search of general mechanisms for longlasting plasticity: aplysia and the hippocampus. Philos Trans R Soc Land B Biol Sci 358:757-763, 2003.
71. Rice ME. Use of ascorbate in the preparation and maintenance of brain slices. Methods 18:144-149, 1999.
72. Rutecki PA, Lebeda F J D J. Epileptiform activity induced by changes in extracellular potassium in hippocampus. J Neurophysiol 54:1363-1374, 1985.
73. Schiff SJ, Somjen GG. Hyperexcitability following moderate hypoxia in hippocampal tissue slices. Brain Res 337:337-340, 1985.
74. Sick TJ, Solow EL, Roberts E L J. Extracellular potassium ion activity and electrophysiology in the hippocampal slice: paradoxical recovery of synaptic transmission during anoxia. Brain Res 418:227-234, 1987.
75. Simon AJ, Torbati D. Effects of hyperbaric oxygen on heart, brain and lung functions in rat. Undersea Biomed Res 9:263-275, 1982.
76. Somjen GG, Aitken PG, Czeh G, Jing J, Young JN. Cellular physiology of hypoxia of the mammalian central nervous system. Res Publ Assoc Res Nerv Ment Dis 71:51-65, 1993.
77. Southan AP, Wann KT. Effects of high helium pressure on intracellular and field potential responses in the CA1 region of the in vitro rat hippocampus. Eur J Neurosci 8:2571-2581, 1996.
78. Southan AP, Wann KT. Methods for intracellular recording from hippocampal brain slices under high helium pressure. J Appl Physiol 71:365-371, 1991.
79. Suzuki R, Yamaguchi T, Li CL, Klatzo I. The effects of 5-minute ischemia in Mongolian gerbils. II. Changes of spontaneous neuronal activity in cerebral cortex and CA1 sector of hippocampus. Acta Neuropathol 60:217-222, 1983.
80. Swartz HM, Dunn JF. Measurements of oxygen in tissues: overview and perspectives on methods. Adv Exp Med Biol 530:1-12, 2003.
81. Taylor MD, Millert TK, Parmentier JL, Lynne EJ. Pharmacological protection of reoxygenation damage to in vitro brain slice tissue. Brain Res 347:286-273, 1985.
82. Tibbies PM, Edelsberg JS. Hyperbaric-oxygen therapy. N Engl J Med 334:1642-1648, 1996.
83. Torbati D, Mokashi A, Lahiri S. Effects of acute hyperbaric oxygenation on respiratory control in cats. J Appl Physiol 67:2351-2356, 1989.
84. Tryba AK, Peña F, Lieske SP, Viemari JC, Thoby-Brisson M, Ramirez JM. Differential modulation of neural network and pacemaker activity underlying eupnea and sigh-breathing activities. J Neurophysiol 99:2114-2125, 2008.
85. Vanderkooi JM, Ereccinska M, Silver IA. Oxygen in mammalian tissue: methods of measurement and affinities of various reactions. Am J Physiol Cell Physiol 260: C1130-C1150, 1991.
86. Wann KT, Southan AP. The action of anaesthetics and high pressure on neuronal discharge patterns. Gen Pharmacol 23:993-1004, 1992.
87. Watson PL, Weiner JL, Carlen PL. Effects of variations in hippocampal slice preparation protocol on the electrophysiological stability, epileptogenicity and graded hypoxia responses of CA1 neurons. Brain Res 115:134-143, 1997.
88. Xu ZC, Gao TM, Ren Y. Neurophysiological changes associated with selective neuronal damage in hippocampus following transient forebrain ischemia. Biol Signals Recept 8:294-308, 1999.