Basal and learning task-related brain oxidative metabolism in cirrhotic rats

Brain Research Bulletin

Volumn 78, Issue 4-5, 2009, Pages 195-201

  Méndez, Marta ^a   Méndez López, Magdalena ^a   López, Laudino ^a   Aller, María Ángeles ^b   Arias, Jaime ^b   Arias, Jorge L ^a  

^a UNIVERSITY OF OVIEDO   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Cirrhosis; Cytochrome c oxidase; Hepatic encephalopathy; Spatial working memory; Thioacetamide; Wistar rat

Indexed keywords

CYTOCHROME C OXIDASE; THIOACETAMIDE;

AEROBIC METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN REGION; CONTROLLED STUDY; ENZYME ACTIVITY; LEARNING; LIVER CIRRHOSIS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL MEMORY; TASK PERFORMANCE; WORKING MEMORY;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT COMPLEX IV; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LIVER CIRRHOSIS; MALE; MAMILLARY BODIES; MAZE LEARNING; MEMORY; NEURONS; RATS; RATS, WISTAR; SPACE PERCEPTION; SPATIAL BEHAVIOR; THALAMUS; THIOACETAMIDE;

EID: 58749086396     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2008.10.008     Document Type: Article

References (70)

1. Abraldes J.G., Pasarín M., and García-Pagán J.C. Animal models of portal hypertension. World J. Gastroeneterol. 12 (2006) 6577-6584
2. Aggleton J.P., and Brown M.W. Episodic memory amnesia, and the hippocampal thalamic axis. Behav. Brain Sci. 22 (1999) 425-444
3. Albrecht J., and Jones E.A. Hepatic encephalopathy: molecular mechanisms underlying the clinical syndrome. J. Neurol. Sci. 170 (1999) 138-146
4. Audet R.M., and Butterworth R.F. Portacaval anastomosis results in more widespread alterations of cerebral metabolism in old versus young adult rats: implications for post-shunt encephalopathy. Metab. Brain Dis. 13 (1998) 69-78
5. Bahceci F., Yildirim B., Karincaoglu M., Dogan I., and Sipahi B. Memory impairment in patients with cirrhosis. J. Natl. Med. Assoc. 97 (2005) 213-216
6. Blei A.T., Omary R., and Butterworth R.F. Animal models of hepatic encephalopathies. In: Bouton A., Baker B., and Butterworth R.F. (Eds). Animal Models of Neurological Disease vol. 2 (1992), The Humana Press, Clifton, NJ 183-222
7. Butterworth R.F. Hepatic encephalopathy: a neuropsychiatric disorder involving multiple neurotransmitter systems. Curr. Opin. Neurol. 13 (2000) 721-727
8. Butterworth R.F. Pathophysiology of hepatic encephalopathy: a new look at ammonia. Metab. Brain Dis. 17 (2002) 221-227
9. Cada A., de la Torre J.C., and Gonzalez-Lima F. Chronic cerebrovascular ischemia in aged rats: effects on brain metabolic capacity and behavior. Neurobiol. Aging 21 (2000) 225-233
10. Conejo N.M., Gonzalez-Pardo H., Vallejo G., and Arias J.L. Changes in brain oxidative metabolism induced by water maze training. Neuroscience 145 (2007) 403-412
11. Cruz N.F., and Duffy T.E. Local cerebral glucose metabolism in rats with chronic portacaval shunts. J. Cerebr. Blood Flow Metab. 3 (1983) 311-320
12. Dashti H., Jeppsson B., Hagerstrand I., Hultberg B., Srinivas U., Abdulla M., and Bengmark S. Thioacetamide- and carbon tetrachloride-induced liver cirrhosis. Eur. Surg. Res. 21 (1989) 83-91
13. DeJoseph M.R., and Hawkins R.A. Glucose consumption decreases throughout the brain only hours after portacaval shunting. Am. J. Physiol. 260 (1991) 613-619
14. de la Torre J.C., Cada A., Nelson N., Davis G., Sutherland R.J., and Gonzalez-Lima F. Reduced cytochrome oxidase and memory dysfunction after chronic brain ischemia in aged rats. Neurosci. Lett. 223 (1997) 165-168
15. Diéguez B., Aller M.A., Nava M.P., Palma M.D., Arias J.L., López L., and Arias J. Chronic portal hypertension in the rat by triple-portal stenosing ligation. J. Invest. Surg. 15 (2002) 329-336
16. Ferenci P., Lockwood A., Mullen K., Tarter R., Weissenborn K., and Blei A.T. Hepatic encephalopathy-definition, nomenclature, diagnosis, and quantification: final report of the working party at the 11th World Congresses of Gastroenterology, Viena, 1998. Hepatology 35 (2002) 716-721
17. Filipponi F., and Mosca F. Animal models of fulminate hepatic failure: need to test liver support devices. Digest. Liver Dis. 33 (2001) 607-613
18. Geiger A., and Magnes J. The isolation of the cerebral circulation and perfusion of the brain in the living cat. Am. J. Physiol. 149 (1947) 517-537
19. Gonzalez-Lima F., and Cada A. Cytochrome oxidase activity in the auditory system of the mouse: a qualitative and quantitative histochemical study. Neuroscience 63 (1994) 559-578
20. Gonzalez-Lima F., and Jones D. Quantitative mapping of cytochrome oxidase activity in the central auditory system of the gerbil: a study with calibrated activity standards and metal-intensified histochemistry. Brain Res. 660 (1994) 34-49
21. Gonzalo-Ruiz A., Morte L., and Sanz J.M. Glutamate/aspartate and leu-enkephalin immunoreactivity in mammillothalamic projection neurons of the rat. Brain Res. Bull. 47 (1998) 565-574
22. Groeneweg M., Quero J.C., De Bruin I., Hartmann I.J., Essink-bot M.L., Hop W.C., and Schalm S.W. Subclinical hepatic encephalopathy impairs daily functioning. Hepatology 28 (1998) 45-49
23. Hazell A., and Butterworth R.F. Hepatic encephalopathy: an update of pathophysiologic mechanisms. PSEBM 222 (1999) 99-112
24. Hernandez R., Martinez-Lara E., Del Moral M.L., Blanco S., Cañuelo A., Siles E., Esteban F.J., Pedrosa J.A., and Peinado M.A. Upregulation of endothelial nitric oxide synthase maintains nitric oxide production in the cerebellum of thioacetamide cirrhotic rats. Neuroscience 126 (2004) 879-887
25. Hilgier W., Benveniste H., Diemer N.H., and Albrecht J. Decreased glucose utilization in discrete brain regions of rat in thioacetamide-induced hepatic encephalopathy as measured with [3H]-deoxyglucose. Acta Neurol. Scand. 83 (1991) 353-355
26. Jeansok J.K., and Yoon K.S. Stress: metaplastic effects in the hippocampus. Trends Neurosci. 21 (1998) 505-509
27. Jessy J., DeJoseph M.R., and Hawkins R.A. Hyperammonemia depresses glucose consumption throughout the brain. Biochem. J. 277 (1991) 693-696
28. Kesner R.P. Behavioral functions of the CA3 subregion of the hippocampus. Learn. Memory 14 (2007) 771-781
29. Kirk I.J. Frequency modulation of hippocampal theta by the supramammillary nucleus, and other hypothalamo-hippocampal interactions: mechanisms and functional implications. Neurosci. Biobehav. Rev. 22 (1998) 291-302
30. Kocsis B., and Vertes R.P. Characterization of neurons of the supramammillary nucleus and mammillary body that discharge rhythmically with hippocampal theta in the rat. J. Neurosci. 14 (1994) 7040-7052
31. Kountouras J., Billing B.H., and Scheuer P.J. Prolonged bile duct obstruction: a new experimental model for cirrhosis in the rat. Br. J. Exp. Pathol. 65 (1984) 305-311
32. Laleman W., Elst I.V., Zeegers M., Servaes R., Libbrecht L., Roskams T., Fevery J., and Nevens F. A stable model of cirrhotic portal hypertension in the rat: thioacetamide revisited. Eur. J. Clin. Invest. 36 (2006) 242-249
33. Lockwood A.H., Ginsberg M.D., Rhoades H.M., and Gutierrez M.T. Cerebral glucose metabolism after portacaval shunting in the rat. Patterns of metabolism and implications for the pathogenesis of hepatic encephalopathy. J. Clin. Invest. 78 (1986) 86-95
34. Lockwood A.H., Murphy B.W., Donnelly K.Z., Mahl T.C., and Perini S. Positron emission tomographic localization of abnormalities of brain metabolism in patients with minimal hepatic encephalopathy. Hepatology 18 (1993) 1061-1068
35. Lockwood A.H., Weissenborn K., Bokemeyer M., Tietge U., and Burchert W. Correlations between cerebral glucose metabolism and neuropsychological test performance in non-alcoholic cirrhotics. Metab. Brain Dis. 17 (2002) 29-40
36. Lopez L., Cimadevilla J.M., Aller M.A., Arias J., Nava M.P., and Arias J.L. Diurnal locomotor activity and oxidative metabolism of the suprachiasmatic nucleus in two models of hepatic insufficiency. J. Neurol. Sci. 212 (2003) 93-97
37. Méndez M., Méndez-López M., López L., Aller M.A., Arias J., and Arias J.L. Working memory impairment and reduced hippocampal and prefrontal cortex c-Fos expression in a rat model of cirrhosis. Physiol. Behav. 95 (2008) 302-307
38. Méndez M., Méndez-López M., López L., Aller M.A., Arias J., and Arias J.L. Mammillary body alterations and spatial memory impairment in Wistar rats with thioacetamide-induced cirrhosis. Brain Res. 1233 (2008) 185-195
39. Mendez M., Mendez-Lopez M., Lopez L., Aller M.A., Arias J., Cimadevilla J.M., and Arias J.L. Spatial memory alterations in three models of hepatic encephalopathy. Behav. Brain Res. 188 (2008) 32-40
40. Méndez-López M., Méndez M., López L., Aller M.A., González-Pardo H., Nava M.P., Sánchez-Patán F., Arias J., and Arias J.L. Increased cytochrome oxidase activity in adrenal glands of thioacetamide-cirrhotic rats. Neuro. Endocrinol. Lett. 26 (2005) 719-723
41. Mendez-Lopez M., Mendez M., Sanchez-Patan F., Casado I., Aller M.A., Lopez L., Corcuera M.T., Alonso M.J., Nava M.P., Arias J., and Arias J.L. Partial portal vein ligation plus thioacetamide: a method to obtain a new model of cirrhosis and chronic portal hypertension in the rat. J. Gastrointest. Surg. 11 (2007) 187-194
42. Morris R.G.M. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11 (1984) 47-60
43. Norenberg M.D. Astrocytic-ammonia interactions in hepatic encephalopathy. Semin. Liver Dis. 16 (1996) 245-253
44. Norenberg M.D., Jayakumar A.R., and Rama Rao K.V. Oxidative stress in the pathogenesis of hepatic encephalopathy. Metab. Brain Dis. 19 (2004) 313-329
45. Ortiz M., Córdoba J., Jacas C., Flavià M., Esteban R., and Guardia J. Neuropsychological abnormalities in cirrhosis include learning impairment. J. Hepatol. 44 (2006) 104-110
46. Papenberg J., Lanzinger B., Kommerell B., and Hoyer S. Comparative studies of the electroencephalogram and the cerebral oxidative metabolism in patients with liver cirrhosis. Klin. Wschr. 53 (1975) 1107-1113
47. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates-The New Coronal Set. 5th ed. (2005), Elsevier Academic Press, London
48. Poordad F.F. Review article: the burden of hepatic encephalopathy. Aliment. Pharmacol. Ther. 25 (2006) 3-9
49. Poremba A., Jones D., and Gonzalez-Lima F. Classical conditioning modifies cytochrome oxidase activity in the auditory system. Eur. J. Neurosci. 10 (1998) 3035-3043
50. Rama Rao K.V., Mawal Y.R., and Qureshi I.A. Progressive decrease of cerebral cytochrome C oxidase activity in sparse-fur mice: role of acetyl-l-carnitine in restoring the ammonia-induced cerebral energy depletion. Neurosci. Lett. 224 (1997) 83-86
51. Rao V.L., Audet R.M., and Butterworth R.F. Increased neuronal nitric oxide synthase expression in brain following portacaval anastomosis. Brain Res. 765 (1997) 169-172
52. Santín L.J., Rubio S., Begega A., and Arias J.L. Effects of mammillary body lesions on spatial referente and working memory tasks. Behav. Brain Res. 102 (1999) 137-150
53. Sathyasaikumar K.V., Swapna I., Reddy P.V.B., Murthy Ch.R., Dutta Gupta A., Senthilkumaran B., and Reddanna P. Fulminant hepatic failure in rats induces oxidative stress differentially in cerebral cortex, cerebellum and pons medulla. Neurochem. Res. 32 (2007) 517-524
54. Stewart V.C., Sharpe M.A., Clark J.B., and Heales S.J. Astrocyte-derived nitric oxide causes both reversible and irreversible damage to the neuronal mitochondrial respiratory chain. J. Neurochem. 75 (2000) 694-700
55. Swapna I., SathyaSaikumar K.V., Murthy Ch.R., Dutta-Gupta A., and Senthilkumaran B. Changes in cerebral membrane lipid composition and fluidity during thioacetamide-induced hepatic encephalopathy. J. Neurochem. 98 (2006) 1899-1907
56. Terblanche J., and Hickman R. Animal models of fulminant hepatic failure. Digest. Dis. Sci. 36 (1991) 770-774
57. Tyce G.M., Flock E.V., and Owen C.A. Metabolism of glucose in brain after hepatectomy. Exp. Biol. Med. 4 (1971) 92-103
58. Vann S.D. Transient spatial deficit associated with bilateral lesions of the lateral mammillary nuclei. Eur. J. Neurosci. 21 (2005) 820-824
59. Vann S.D., and Aggleton J.P. Evidence of a spatial encoding deficit in rats with lesions of the mammillary bodies or mammillothalamic tract. J. Neurosci. 23 (2003) 3506-3514
60. Vann S.D., and Aggleton J.P. The mammillary bodies: two memory systems in one?. Nat. Rev. Neurosci. 5 (2004) 35-44
61. Vann S.D., Honey R.C., and Aggleton J.P. Lesions of the mammillothalamic tract impair the acquisition of spatial but not nonspatial contextual conditional discriminations. Eur. J. Neurosci. 18 (2003) 2413-2416
62. Vaquero J., Chung C., Cahill M.E., and Blei A.T. Pathogenesis of hepatic encephalopathy in acute liver failure. Semin. Liver Dis. 23 (2003) 259-269
63. Vizi E.S., and Kiss J.P. Neurochemistry and pharmacology of the major hippocampal transmitter systems: synaptic and nonsynaptic interactions. Hippocampus 8 (1998) 566-607
64. Weissenborn K., Bokemeyer M., Ahl B., Fischer-Wasels D., Giewekemeyer K., van den Hoff J., Köstler H., and Berding G. Functional imaging of the brain in patients with liver cirrhosis. Metab. Brain Dis. 19 (2004) 269-280
65. Weissenborn K., Burchert W., Bokemeyer M., Ehrenheim C., Kolbe H., Manns M.P., and Dengler R. Regional differences of cerebral glucose metabolism in patients with liver cirrhosis depending on the grade of portosystemic encephalopathy (PSE). In: Record C., and Al Mardini H. (Eds). Advances in Hepatic Encephalopathy and Metabolism in Liver Disease (1997), Medical Faculty, University Newcastle upon Tyne, Newcastle upon Tyne 359-363
66. Weissenborn K., Giewekemeyer K., Heidenreich S., Bokemeyer M., Berding G., and Ahl B. Attention, memory and cognitive function in hepatic encephalopathy. Metab. Brain Dis. 20 (2005) 359-367
67. Weissenborn K., Heidenreich S., Giewekemeyer K., Rückert N., and Hecker H. Memory function in early hepatic encephalopathy. J. Hepatol. 39 (2003) 320-325
68. Wong-Riley M.T.T. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci. 12 (1989) 94-101
69. World Health Organization, Global Burden of Disease, 2002. World health Report, 2003.
70. Xiangnong L., Irving S.B., and Barry A. Reproducible production of thioacetamide-induced macronodular cirrhosis in the rat with no mortality. J. Hepatol. 36 (2002) 488-493