Effects of CA1 glutamatergic systems upon memory impairments in cholestatic rats

Behavioural Brain Research

Volumn 256, Issue , 2013, Pages 636-645

  Hosseini, Nasrin ^a   Nasehi, Mohammad ^b   Radahmadi, Maryam ^c   Zarrindast, Mohammad Reza ^a,d,e,f  

^a INSTITUTE FOR COGNITIVE SCIENCE STUDIES ICSS   (Iran)

^b ISLAMIC AZAD UNIVERSITY   (Iran)

^c ISFAHAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^d TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^e TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^f INSTITUTE FOR RESEARCH IN FUNDAMENTAL SCIENCES IPM   (Iran)

Author keywords

Cholestasis; D AP7; NMDA; Rat; Step through passive avoidance test

Indexed keywords

2 AMINO 7 PHOSPHONOHEPTANOIC ACID; N METHYL DEXTRO ASPARTIC ACID;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT LIGATION; CENTRAL NERVOUS SYSTEM; CHOLESTASIS; CONTROLLED STUDY; GLUTAMATERGIC SYSTEM; HIPPOCAMPAL CA1 REGION; LOCOMOTION; MALE; MEMORY CONSOLIDATION; NONHUMAN; PASSIVE AVOIDANCE; PRIORITY JOURNAL; RAT; RECALL;

CHOLESTASIS; D-AP7; NMDA; RAT; STEP-THROUGH PASSIVE AVOIDANCE TEST;

2-AMINO-5-PHOSPHONOVALERATE; ANIMALS; CA1 REGION, HIPPOCAMPAL; CHOLESTASIS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; MALE; MEMORY; MEMORY DISORDERS; MOTOR ACTIVITY; N-METHYLASPARTATE; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84884938704     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.08.018     Document Type: Article

References (110)

1. Forton D.M., Thomas H.C., Murphy C.A., Allsop J.M., Foster G.R., Main J., et al. Hepatitis C and cognitive impairment in a cohort of patients with mild liver disease. Hepatology 2002, 35:433-439.
2. Monfort P., Erceg S., Piedrafita B., Llansola M., Felipo V. Chronic liver failure in rats impairs glutamatergic synaptic transmission and long-term potentiation in hippocampus and learning ability. Eur J Neurosci 2007, 25:2103-2111.
3. Pantiga C., Rodrigo L.R., Cuesta M., Lopez L., Arias J.L. Cognitive deficits in patients with hepatic cirrhosis and in liver transplant recipients. J Neuropsych Clin Neurosci 2003, 15:84-89.
4. Weissenborn K., Heidenreich S., Giewekemeyer K., Rückert N., Hecker H. Memory function in early hepatic encephalopathy. J Hepatol 2003, 39:320-325.
5. Sheen J.M., Huang L.T., Hsieh C.S., Chen C.C., Wang J.Y., Tain Y.L. Bile duct ligation in developing rats: temporal progression of liver, kidney, and brain damage. J Pediatr Surg 2010, 45:1650-1658.
6. García-Ayllón M.S., Cauli O., Silveyra M.X., Rodrigo R., Candela A., Compañ A., et al. Brain cholinergic impairment in liver failure. Brain 2008, 131:2946-2956.
7. Huang L.T., Chen C.C., Sheen J.M., Chen Y.J., Hsieh C.S., Tain Y.L. The interaction between high ammonia diet and bile duct ligation in developing rats: assessment by spatial memory and asymmetric dimethylarginine. Int J Dev Neurosci 2010, 28:169-174.
8. Jover R., Rodrigo R., Felipo V., Insausti R., Sáez-Valero J., García-Ayllón M., et al. Brain edema and inflammatory activation in bile duct ligated rats with diet-induced hyperammonemia: A model of hepatic encephalopathy in cirrhosis. Hepatology 2006, 43:1257-1266.
9. Gartung C., Ananthanarayanan M., Rahman M., Schuele S., Nundy S., Soroka C., et al. Down-regulation of expression and function of the rat liver Na+/bile acid cotransporter in extrahepatic cholestasis. Gastroenterology 1996, 110:199-209.
10. Zarrindast M.R., Nasehi M., Hoseindoost S. Possible interaction between opioidergic and cholinergic systems of CA1 in cholestasis-induced amnesia in mice. Behav Brain Res 2011.
11. García-Moreno L.M., Ángeles Aller M., Conejo N.M., Gómez M.A., Martín F.R., Arias J., et al. Brain Ag-NOR activity in cholestatic rats with hepatic encephalopathy. Hepatol Res 2002, 24:275-281.
12. Blei A.T., Omary R., Butterworth R.F. Animal models of hepatic encephalopathies. Neuromethods 1992, 22:183.
13. Cauli O., Rodrigo R., Llansola M., Montoliu C., Monfort P., Piedrafita B., et al. Glutamatergic and gabaergic neurotransmission and neuronal circuits in hepatic encephalopathy. Metab Brain Dis 2009, 24:69-80.
14. Magen I., Avraham Y., Ackerman Z., Vorobiev L., Mechoulam R., Berry E. Cannabidiol ameliorates cognitive and motor impairments in bile-duct ligated mice via 5-HT1A receptor activation. Br J Pharmacol 2010, 159:950-957.
15. Márquez-Aguirre A., Canales-Aguirre A., Gómez-Pinedo U., Gálvez-Gastélum F. Molecular aspects of hepatic encephalopathy. Neurologia (Barcelona, Spain) 2010, 25:239-247.
16. Marrachelli V.G., Miranda F.J., Alabadí J.A., Lloréns S., Alborch E. Contribution of endothelin receptors and cyclooxygenase-derivatives to the altered response of the rabbit renal artery to endothelin-1 in diabetes. Eur J Pharmacol 2006, 534:178-186.
17. Palomero-Gallagher N., Bidmon H.J., Cremer M., Schleicher A., Kircheis G., Reifenberger G., et al. Neurotransmitter receptor imbalances in motor cortex and basal ganglia in hepatic encephalopathy. Cell Physiol Biochem 2009, 24:291-306.
18. Prado V.F., Martins-Silva C., de Castro B.M., Lima R.F., Barros D.M., Amaral E., et al. Mice deficient for the vesicular acetylcholine transporter are myasthenic and have deficits in object and social recognition. Neuron 2006, 51:601-612.
19. Jamali-Raeufy N., Nasehi M., Zarrindast M.R. Influence of N-methyl D-aspartate receptor mechanism on WIN55,212-2-induced amnesia in rat dorsal hippocampus. Behav Pharmacol 2011, 22:645-654.
20. Khakpai F., Nasehi M., Haeri-Rohani A., Eidi A., Zarrindast M.R. Scopolamine induced memory impairment; possible involvement of NMDA receptor mechanisms of dorsal hippocampus and/or septum. Behav Brain Res 2012, 231:1-10.
21. Bashir Z.I., Bortolotto Z.A., Davies C.H., Berretta N., Irving A.J., Seal A.J., et al. Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature 1993.
22. Boulton C., Southam E., Garthwaite J. Nitric oxide-dependent long-term potentiation is blocked by a specific inhibitor of soluble guanylyl cyclase. Neuroscience 1995, 69:699-703.
23. Harris E.W., Ganong A.H., Cotman C.W. Long-term potentiation in the hippocampus involves activation of N-methyl-{d}-aspartate receptors. Brain Res 1984.
24. Hermenegildo C., Montoliu C., Llansola M., Muñoz M.D., Gaztelu J.M., Miñana M.D., et al. Chronic hyperammonemia impairs the glutamate-nitric oxide-cyclic GMP pathway in cerebellar neurons in culture and in the rat in vivo. Eur J Neurosci 2001, 10:3201-3209.
25. Alvarez E., Banzan A. Ventral hippocampal glutamate receptors in the rat: possible involvement in learning mechanisms of an active avoidance response. J Neural Transm 1999, 106:987-1001.
26. Braak H., Braak E. Entorhinal-hippocampal interaction in mnestic disorders. Hippocampus 1993, 3:239.
27. Horel J. Some comments on the special cognitive functions claimed for the hippocampus. Cortex J Devoted Study Nervous Syst Behav 1994.
28. Ridley R., Baker H., Harder J., Pearson C. Effects of lesions of different parts of the septo-hippocampal system in primates on learning and retention of information acquired before or after surgery. Brain Res Bull 1996, 40:21-32.
29. Shen Y., Specht S.M., De Saint Ghislain I., Li R. The hippocampus: a biological model for studying learning and memory. Prog Neurobiol 1994, 44:485.
30. Squire L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 1992, 99:195.
31. Keller E.A., Borghese C.M., Carrer H.F., Ramirez O.A. The learning capacity of high or low performance rats is related to the hippocampus NMDA receptors. Brain Res 1992.
32. Davis S.F., Linn C.L. Activation of NMDA receptors linked to modulation of voltage-gated ion channels and functional implications. Am J Physiol Cell Physiol 2003, 284. C757-C68.
33. Kiyama Y., Manabe T., Sakimura K., Kawakami F., Mori H., Mishina M. Increased thresholds for long-term potentiation and contextual learning in mice lacking the NMDA-type glutamate receptor (1 subunit. J Neurosci 1998, 18:6704-6712.
34. Moghaddam B. Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J Neurochem 2006, 60:1650-1657.
35. Morris R. Synaptic plasticity and learning: selective impairment of learning rats and blockade of long-term potentiation in vivo by the N-methyl-D-aspartate receptor antagonist AP5. J Neurosci 1989, 9:3040-3057.
36. Morris R., Anderson E., Lynch G., Baudry M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 1986.
37. Richter-Levin G., Errington M., Maegawa H., Bliss T. Activation of metabotropic glutamate receptors is necessary for long-term potentiation in the dentate gyrus and for spatial learning. Neuropharmacology 1994, 33:853-857.
38. Hrabetova S., Sacktor T.C. Long-term potentiation and long-term depression are induced through pharmacologically distinct NMDA receptors. Neurosci Lett 1997, 226:107-110.
39. Pourmotabbed A., Motamedi F., Fathollahi Y., Mansouri F.A., Semnanian S. Involvement of NMDA receptors and voltage-dependent calcium channels on augmentation of long-term potentiation in hippocampal CA1 area of morphine dependent rats. Brain Res 1998, 804:125-134.
40. Xu X., Boshoven W., Lombardo B., Spranger J. Comparison of the amnestic effects on NMDA receptor antagonist MK-801 and nitric oxide synthase inhibitors: L-NAME and L-NOARG in goldfish. Behav Neurosci 1998, 112:892.
41. Rodrigo R., Cauli O., Gomez-Pinedo U., Agusti A., Hernandez-Rabaza V., Garcia-Verdugo J.M., et al. Hyperammonemia induces neuroinflammation that contributes to cognitive impairment in rats with hepatic encephalopathy. Gastroenterology 2010, 139:675-684.
42. Padovan C.M., Del Bel E.A., Guimarães F.S. Behavioral effects in the elevated plus maze of an NMDA antagonist injected into the dorsal hippocampus: influence of restraint stress. Pharmacol Biochem Behav 2000, 67:325-330.
43. van den Bos R. Charria Ortiz GA, Cools AR. Injections of the NMDA-antagonist D-2-amino-7-phosphonoheptanoic acid (AP-7) into the nucleus accumbens of rats enhance switching between cue-directed behaviours in a swimming test procedure. Behav Brain Res 1992, 48:165-170.
44. Car H., Wisniewski K. The effect of baclofen and AP-7 on selected behavior in rats. Pharmacol Biochem Behav 1998, 59:685-689.
45. Trullas R., Skolnick P. Functional antagonists at the NMDA receptor complex exhibit antidepressant actions. Eur J Pharmacol 1990, 185:1-10.
46. Felipo V. Contribution of altered signal transduction associated to glutamate receptors in brain to the neurological alterations of hepatic encephalopathy. World J Gastroenterol 2006, 12:7737.
47. Nasehi M., Amin Yavari S., Zarrindast M.R. Synergistic effects between CA1 mu opioid and dopamine D1-like receptors in impaired passive avoidance performance induced by hepatic encephalopathy in mice. Psychopharmacology (Berl) 2013, 227:553-566.
48. Zarrindast M.R., Hoseindoost S., Nasehi M. Possible interaction between opioidergic and cholinergic systems of CA1 in cholestasis-induced amnesia in mice. Behav Brain Res 2012, 228:116-124.
49. Shohami E., Novikov M., Bass R. Long-term effect of HU-211, a novel non-competitive NMDA antagonist, on motor and memory functions after closed head injury in the rat. Brain Res 1995, 674:55-62.
50. Ben-Eliyahu S., Marek P., Vaccarino A.L., Mogil J.S., Sternberg W.F., Liebeskind J.C. The NMDA receptor antagonist MK-801 prevents long-lasting non-associative morphine tolerance in the rat. Brain Res 1992, 575:304-308.
51. Laleman W., Omasta A., Van de Casteele M., Zeegers M., Vander Elst I., Van Landeghem L., et al. A role for asymmetric dimethylarginine in the pathophysiology of portal hypertension in rats with biliary cirrhosis. Hepatology 2005, 42:1382-1390.
52. Nacher J., Rosell D.R., Alonso-Llosa G., McEwen B.S. NMDA receptor antagonist treatment induces a long-lasting increase in the number of proliferating cells, PSA-NCAM-immunoreactive granule neurons and radial glia in the adult rat dentate gyrus. Eur J Neurosci 2001, 13:512-520.
53. Valeria Bergasa N., Alling D.W., Vergalla J., Anthony Jones E. Cholestasis in the male rat is associated with naloxone-reversible antinociception. J Hepatol 1994, 20:85-90.
54. Rastegar H., Homayoun H., Afifi M., Rezayat M., Dehpour A.R. Modulation of cholestasis-induced antinociception by CCK receptor agonists and antagonists. Eur Neuropsychopharmacol 2002, 12:111-118.
55. Jamali-Raeufy N., Nasehi M., Ebrahimi-Ghiri M., Zarrindast M.R. Cross state-dependency of learning between WIN55, 212-2 and scopolamine in rat dorsal hippocampus. Neurosci Lett 2011, 491:227-231.
56. Nasehi M., Sahebgharani M., Haeri-Rohani A., Zarrindast M.R. Effects of cannabinoids infused into the dorsal hippocampus upon memory formation in 3-days apomorphine-treated rats. Neurobiol Learn Mem 2009, 92:391-399.
57. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 2005, Academic Press.
58. Velíšková J., Liptáková S., Hussain S. The effects of N-methyl-d-aspartate antagonist 2-amino-7-phosphonoheptanoic acid microinfusions into the adult male rat substantia nigra pars reticulata are site-specific. Neurosci Lett 2001, 316:108-110.
59. Izquierdo I., Quillfeldt J., Zanatta M., Quevedo J., Schaeffer E., Schmitz P., et al. Sequential role of hippocampus and amygdala, entorhinal cortex and parietal cortex in formation and retrieval of memory for inhibitory avoidance in rats. Eur J Neurosci 2006, 9:786-793.
60. García-Moreno L., Conejo N., González-Pardo H., Aller M., Nava M., Arias J., et al. Evaluation of two experimental models of hepatic encephalopathy in rats. Braz J Med Biol Res 2005, 38:127-132.
61. Aronson D.C., Chamuleau R.A.F.M., Frederiks W.M., Gooszen H.G., Heijmans H.S.A., James J. Reversibility of cholestatic changes following experimental common bile duct obstruction: fact or fantasy. J Hepatol 1993, 18:85-95.
62. García-Ayllón M., Silveyra M.X., Candela A., Compañ A., Clària J., Jover R., et al. Changes in liver and plasma acetylcholinesterase in rats with cirrhosis induced by bile duct ligation. Hepatology 2006, 43:444-453.
63. Gieling R.G., Burt A.D., Mann D.A. Fibrosis and cirrhosis reversibility-molecular mechanisms. Clin Liver Dis 2008, 12:915-937.
64. Kountouras J., Billing B.H., Scheuer P.J. Prolonged bile duct obstruction: a new experimental model for cirrhosis in the rat. Br J Exp Pathol 1984, 65:305.
65. Ferenci P., Lockwood A., Mullen K., Tarter R., Weissenborn K., Blei A.T. Hepatic encephalopathy-definition, nomenclature, diagnosis, and quantification: final report of the working party at the 11th World Congresses of Gastroenterology, Vienna, 1998. Hepatology 2002, 35:716-721.
66. Michalak A., Rose C., Butterworth J., Butterworth R.F. Neuroactive amino acids and glutamate (NMDA) receptors in frontal cortex of rats with experimental acute liver failure. Hepatology 2003, 24:908-913.
67. Romero-Gómez M., Córdoba J., Jover R., del Olmo J.A., Ramírez M., Rey R., et al. Value of the critical flicker frequency in patients with minimal hepatic encephalopathy. Hepatology 2007, 45:879-885.
68. Tarter R.E., Arria A.M., Carra J., Van Thiel D.H. Memory impairments concomitant with nonalcoholic cirrhosis. Int J Neurosci 1987, 32:853-859.
69. Butterworth R.F. The neurobiology of hepatic encephalopathy. Semin Liver Dis 1996, 235.
70. Lozeva V., Montgomery J.A., Tuomisto L., Rocheleau B., Pannunzio M., Huet P.M., et al. Increased brain serotonin turnover correlates with the degree of shunting and hyperammonemia in rats following variable portal vein stenosis. J Hepatol 2004, 40:742-748.
71. Bearn J., Allain T., Coskeran P., Munro N., Butler J., McGregor A., et al. Neuroendocrine responses to d-fenfluramine and insulin-induced hypoglycemia in chronic fatigue syndrome. Biol Psychiatry 1995, 37:245-252.
72. Burak K.W., Le T., Swain M.G. Increased sensitivity to the locomotor-activating effects of corticotropin-releasing hormone in cholestatic rats. Gastroenterology 2002, 122:681-688.
73. Swain M.G., Patchev V., Vergalla J., Chrousos G., Jones E.A. Suppression of hypothalamic-pituitary-adrenal axis responsiveness to stress in a rat model of acute cholestasis. J Clin Invest 1993, 91:1903.
74. Forton D., Patel N., Prince M., Oatridge A., Hamilton G., Goldblatt J., et al. Fatigue and primary biliary cirrhosis: association of globus pallidus magnetisation transfer ratio measurements with fatigue severity and blood manganese levels. Gut 2004, 53:587-592.
75. Carrier E.J., Auchampach J.A., Hillard C.J. Inhibition of an equilibrative nucleoside transporter by cannabidiol: a mechanism of cannabinoid immunosuppression. Sci Signal 2006, 103:7895.
76. Butterworth R.F. Hepatic encephalopathy and brain edema in acute hepatic failure: does glutamate play a role. Hepatology 2003, 25:1032-1034.
77. Monfort P., Munoz M.D., Felipo V. Hyperammonemia impairs long-term potentiation in hippocampus by altering the modulation of cGMP-degrading phosphodiesterase by protein kinase G. Neurobiol Dis 2004, 15:1.
78. Bartanusz V., Aubry J.M., Pagliusi S., Jezova D., Baffi J., Kiss J.Z. Stress-induced changes in messenger RNA levels of N-methyl-d-aspartate and AMPA receptor subunits in selected regions of the rat hippocampus and hypothalamus. Neuroscience 1995, 66:247-252.
79. Monfort P., Muñoz M.D., ElAyadi A., Kosenko E., Felipo V. Effects of hyperammonemia and liver failure on glutamatergic neurotransmission. Metab Brain Dis 2002, 17:237-250.
80. Ambrogi Lorenzini C.G., Baldi E., Bucherelli C., Sacchetti B., Tassoni G. Role of ventral hippocampus in acquisition, consolidation and retrieval of rat's passive avoidance response memory trace. Brain Res 1997, 768:242-248.
81. Bouton M.E., Moody E.W. Memory processes in classical conditioning. Neurosci Biobehav Rev 2004, 28:663-674.
82. Broadbent N.J., Squire L.R., Clark R.E. Spatial memory, recognition memory, and the hippocampus. Proc Natl Acad Sci USA 2004, 101:14515-14520.
83. Lorenzini C.A., Baldi E., Bucherelli C., Sacchetti B., Tassoni G. Role of dorsal hippocampus in acquisition, consolidation and retrieval of rat's passive avoidance response: a tetrodotoxin functional inactivation study. Brain Res 1996, 730:32-39.
84. Lynch M. Long-term potentiation and memory. Physiol Rev 2004, 84:87-136.
85. Shors T.J., Matzel L.D. Long-term potentiation: what's learning got to do with it. Behav Brain Sci 1997, 20:597-614.
86. Bernabeu R., Schroder N., Quevedo J., Cammarota M., Izquierdo I., Medina J.H. Further evidence for the involvement of a hippocampal cGMP/cGMP-dependent protein kinase cascade in memory consolidation. Neuroreport 1997, 8:2221.
87. Martinez J.L., Derrick B.E. Long-term potentiation and learning. Annu Rev Psychol 1996, 47:173-203.
88. Wiœniewski K. Behavioral effects of D-AP7 in rats subjected to experimental hypoxia. Pol J Pharmacol 2003, 55:337-344.
89. Bliss T.V.P., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
90. Riedel G., Reymann K. Metabotropic glutamate receptors in hippocampal long-term potentiation and learning and memory. Acta Physiol Scand 2003, 157:1-19.
91. Rodrigo R., Erceg S., Rodriguez-Diaz J., Saez-Valero J., Piedrafita B., Suarez I., et al. Glutamate-induced activation of nitric oxide synthase is impaired in cerebral cortex in vivo in rats with chronic liver failure. J Neurochem 2007, 102:51-64.
92. Bekkers J.M., Stevens C.F. NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus. Nature 1989.
93. Campeau S., Miserendino M.J., Davis M. Intra-amygdala infusion of the N-methyl-D-aspartate receptor antagonist AP5 blocks acquisition but not expression of fear-potentiated startle to an auditory conditioned stimulus. Behav Neurosci 1992, 106:569.
94. Gorter J.A., de Bruin J.P.C. Chronic neonatal MK-801 treatment results in an impairment of spatial learning in the adult rat. Brain Res 1992, 580:12-17.
95. Rickard N., Poot A., Gibbs M., Ng K. Both non-NMDA and NMDA glutamate receptors are necessary for memory consolidation in the day-old chick. Behav Neural Biol 1994, 62:33-40.
96. Lavoie J., Giguère J.F., Layrargues G.P., Butterworth R.F. Amino acid changes in autopsied brain tissue from cirrhotic patients with hepatic encephalopathy. J Neurochem 2006, 49:692-697.
97. Record C., Buxton B., Chase R., Curzon G., Murray-Lyon I., Plasma Williams R. brain amino acids in fulminant hepatic failure and their relationship to hepatic encephalopathy. Eur J Clin Invest 2008, 6:387-394.
98. Butterworth R.F., Le O., Lavoie J., Szerb J.C. Effect of portacaval anastomosis on electrically stimulated release of glutamate from rat hippocampal slices. J Neurochem 2006, 56:1481-1484.
99. Peterson C., Giguere J.F., Cotman C.W., Butterworth R.F. Selective loss of NMDA Sensitive [3H] Glutamate binding sites in rat brain following portacaval anastomosis. J Neurochem 2006, 55:386-390.
100. Felipo V., Butterworth R.F. Neurobiology of ammonia. Prog Neurobiol 2002, 67:259-279.
101. Miñana M.D., Llansola M., Hermenegildo C., Cucarella C., Montoliu C., Kosenko E., et al. Glutamate and muscarinic receptors in the molecular mechanisms of acute ammonia toxicity and of its prevention. Adv Exp Med Biol 1997, 420:45.
102. Fan P., Lavoie J., Le N., Szerb J., Butterworth R. Neurochemical and electrophysiological studies on the inhibitory effect of ammonium ions on synaptic transmission in slices of rat hippocampus: evidence for a postsynaptic action. Neuroscience 1990, 37:327-334.
103. Fan P., Szerb J. Effects of ammonium ions on synaptic transmission and on responses to quisqualate and N-methyl-d-aspartate in hippocampal CA1 pyramidal neurons in vitro. Brain Res 1993, 632:225-231.
104. Yamada K., Hiramatsu M., Noda Y., Mamiya T., Murai M., Kameyama T., et al. Role of nitric oxide and cyclic GMP in the dizocilpine-induced impairment of spontaneous alternation behavior in mice. Neuroscience 1996, 74:365-374.
105. Albrecht J. Roles of neuroactive amino acids in ammonia neurotoxicity. J Neurosci Res 1998, 51:133-138.
106. Monfort P., Corbalán R., Martinez L., López-Talavera J.C., Córdoba J., Felipo V. Altered content and modulation of soluble guanylate cyclase in the cerebellum of rats with portacaval anastomosis. Neuroscience 2001, 104:1119-1125.
107. Erceg S., Monfort P., Hernández-Viadel M., Rodrigo R., Montoliu C., Felipo V. Oral administration of sildenafil restores learning ability in rats with hyperammonemia and with portacaval shunts. Hepatology 2005, 41:299-306.
108. Huang L.T., Tiao M.M., Tain Y.L., Chen C.C., Hsieh C.S. Melatonin ameliorates bile duct ligation-induced systemic oxidative stress and spatial memory deficits in developing rats. Pediatr Res 2009, 65:176-180.
109. Keller J.N., Guo Q., Holtsberg F., Bruce-Keller A., Mattson M.P. Increased sensitivity to mitochondrial toxin-induced apoptosis in neural cells expressing mutant presenilin-1 is linked to perturbed calcium homeostasis and enhanced oxyradical production. J Neurosci 1998, 18:4439-4450.
110. Keller J.N., Mattson M.P. Roles of lipid peroxidation in modulation of cellular signaling pathways, cell dysfunction, and death in the nervous system. Rev Neurosci 1998, 9:105-116.