Portal hypertension in 18-month-old rats: Memory deficits and brain metabolic activity

Physiology and Behavior

Volumn 100, Issue 2, 2010, Pages 135-142

  Begega, Azucena ^a   Méndez, Marta ^a   Rubio, Sandra ^b   Santín, Luis J ^c   Aller, María A ^d   Arias, Jaime ^d   Arias, Jorge L ^a  

^a UNIVERSITY OF OVIEDO   (Spain)

^b UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^c UNIVERSITY OF MÁLAGA   (Spain)

^d UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Active avoidance; Chronic portal hypertension; Cytochrome c oxidase; Hepatic encephalopathy; Limbic system; Middle age; Spatial memory; Wistar rats

Indexed keywords

CYTOCHROME C OXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AVOIDANCE BEHAVIOR; BRAIN FUNCTION; BRAIN METABOLISM; CONTROLLED STUDY; DENTATE GYRUS; ENZYME ACTIVITY; FROZEN SECTION; HISTOCHEMISTRY; LEARNING; MALE; MAMMILLARY BODY; MEMORY DISORDER; NONHUMAN; PORTAL HYPERTENSION; PRIORITY JOURNAL; RAT; REFERENCE MEMORY; SHORT TERM MEMORY; SPATIAL MEMORY; STRIA TERMINALIS; TASK PERFORMANCE;

ANALYSIS OF VARIANCE; ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; BRAIN; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT COMPLEX IV; HYPERTENSION, PORTAL; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MAZE LEARNING; MEMORY DISORDERS; MEMORY, SHORT-TERM; RATS; RATS, WISTAR; REACTION TIME; SPATIAL BEHAVIOR;

EID: 77950952991     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2010.02.014     Document Type: Article

References (72)

1. Amodio P., Schiff S., Del Piccolo F., Mapelli D., Gatta A., Umilta C. Attention dysfunction in cirrhotic patients: an inquiry on the role of executive control, attention orienting and focusing. Metab Brain Dis 2005, 20:115-127.
2. Ortiz M., Córdoba J., Jacas C., Flavià M., Esteban R., Guardia J. Neuropsychological abnormalities in cirrhosis include learning impairment. J Hepatol 2006, 44:104-110.
3. Weissenborn K., Ennen J.C., Schomerus H., Rückert N., Hecker H. Neuropsychological characterization of hepatic encephalopathy. J Hepatol 2001, 34:768-773.
4. Weissenborn K., Heidenreich S., Giewekemeyer K., Rückert N., Hecker H. Memory function in early hepatic encephalopathy. J Hepatol 2003, 39:320-325.
5. Weissenborn K., Giewekemeyer K., Heidenreich S., Bokemeyer M., Berding G., Ahl B. Attention, memory and cognitive function in hepatic encephalopathy. Metab Brain Dis 2005, 20:359-367.
6. Butterworth R.F., Norenberg M.D., Felipo V., Ferenci P., Albrecht J., Blei A.T. Members of the ISHEN Commission on experimental models of HE. Experimental models of hepatic encephalopathy: ISHEN guidelines. Liver Int 2009, 29:783-788.
7. Dieguez B., Aller M.A., Nava M.P., Palma M.D., Arias J.L., López L., et al. Chronic portal hypertension in the rat by triple-portal stenosing ligation. J Investig Surg 2002, 15:329-336.
8. Laleman W., Landeghem L., Wilmer A., Fevery J., Nevens F. Portal hypertension: from pathophysiology to clinical practice. Liver Int 2005, 25:1079-1090.
9. Monterde G., Rodriguez-Fabián G., Vara E., López L., Arias J.L., Aller M.A., et al. Increased plasma levels of corticosterone and prolactin and decreased T3 and T4 levels in short-term prehepatic portal hypertension in rats. Dig Dis Sci 2000, 45:1865-1871.
10. Sánchez-Patán F., Anchuelo R., Aller M.A., Vara E., García C., Nava M.P., et al. Chronic prehepatic portal hypertension in the rat: is it a type of metabolic inflammatory syndrome?. Lipids Health Dis 2008, 7:4.
11. Herman J.P., Figueiredo H., Mueller N.K., Ulrich-Lai Y., Ostrander M.M., Choi D.C., et al. Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamic-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 2003, 24:151-180.
12. Brown S.M., Henning S., Wellman C.L. Mild, short-term stress alters dendritic morphology in rat medial prefrontal cortex. Cereb Cortex 2005, 15:1714-1722.
13. Joëls M. Corticosteroid actions in the hippocampus. J Neuroendocrinol 2001, 13:657-669.
14. Joëls M. Role of corticosteroid hormones in the dentate gyrus. Prog Brain Res 2007, 163:355-370.
15. Wellman C.L. Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J Neurobiol 2001, 49:245-253.
16. Woolley C., Gould E., McEwen B.S. Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 1990, 531:225-231.
17. Arbel I., Kadar T., Silbermann M., Levy A. The effects of long-term corticosterone administration on hippocampal morphology and cognitive performance of middle-aged rats. Brain Res 1994, 657:227-235.
18. Bodnoff S.R., Humphreyz A.G., Lehman J.C., Diamond D.M., Rose G.M., Meaney M.J. Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuropathology in young and mid-aged rats. J Neurosci 1995, 15:61-69.
19. De Quervain D.J.F., Roozendaal B., McGaugh J.L. Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 1998, 394:787-790.
20. Tata D.A., Anderson B.J. The effects of chronic glucocorticoid exposure on dendritic length, synapse numbers and glial volumen in animal models: implications for hippocampal volume reductions in depression. Physiol Behav 2010, 99:186-193.
21. Martignoni E., Costa A., Sinforiani E., Liuzzi A., Mauri M., Bono G., et al. The brain as a target for adrenocortical steroids: cognitive implications. Psychoneuroendocrinology 1992, 17:343-354.
22. Meijer O.C., Topic B., Steenbergen P.J., Jocham G., Huston J.P., Oitzl M.S. Correlations between hypothalamus-pituitary-adrenal axis parameters depend on age and learning capacity. Endocrinology 2005, 146:1372-1381.
23. Miller D.B., O'Callaghan J.P. Aging, stress and the hippocampus. Ageing Res Rev 2005, 4:123-140.
24. Herman J.P., Ostrander M.M., Mueller N.K., Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 2005, 29:1201-1213.
25. Choi D.C., Furay A.R., Evanson N.K., Ostrander M.M., Ulrich-Lai Y.M., Herman J.P. Bed nucleus of the stria terminalis subregions differentially regulate hypothalamic-pituitary-adrenal axis activity: implications for the integration of limbic inputs. J Neurosci 2007, 27:2025-2034.
26. García-Moreno L.M., Conejo N.M., González-Pardo H., Aller M.A., Nava M.P., Arias J., et al. Evaluation of two experimental models of hepatic encephalopathy in rats. Braz J Med Biol Res 2005, 38:127-132.
27. Méndez M., Méndez-López M., López L., Aller M.A., Arias J., Civadevilla J.M., et al. Spatial memory alterations in three models of hepatic encephalopathy. Behav Brain Res 2008, 188:32-40.
28. Ragozzino M.E., Detrick S., Kesner R.P. Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. J Neurosci 1999, 19:4585-4594.
29. Moser M.B., Moser E.I., Forrest E., Andersen P., Morris R.G. Spatial learning with a minislab in the dorsal hippocampus. Proc Natl Acad Sci U S A 1995, 92:9697-9701.
30. Aranda L., Santín L.J., Begega A., Aguirre J., Arias J.L. Supramamillary and adjacent nuclei lesions impair spatial working memory and induce anxiolitic-like behavior. Behav Brain Res 2006, 167:156-164.
31. Santín L.J., Rubio S., Begega A., Arias J.L. Effects of mammillary body lesions on spatial reference and working memory task. Behav Brain Res 1999, 102:137-150.
32. Vann S.D., Aggleton J.P. The mammillary bodies: two memory systems in one?. Nat Rev Neurosci 2004, 5:35-44.
33. Shumake J., Edwards E., Gonzalez-Lima F. Hypermetabolism of paraventricular hypothalamus in the congenitally helpless rat. Neurosci Lett 2001, 311:45-48.
34. Valla J., Berndt J.D., Gonzalez-Lima F. Energy hypometabolism in posterior cingulate cortex of Alzheimer's patients: superficial laminar cytochrome oxidase associated with disease duration. J Neurosci 2001, 21:4923-4930.
35. Wong-Riley M.T.T. Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 1989, 12:94-101.
36. 2. Clin Sci (Lond) 2009, 117:365-374.
37. Morris R.G.M. Developments of a water-maze procedure for studying spatial learning in the rat. J Neurosci Meth 1984, 11:47-60.
38. Gonzalez-Lima F., Cada A. Cytochrome oxidase activity in the auditory system of the mouse: a qualitative and quantitative histochemical study. Neuroscience 1994, 63:559-578.
39. Paxinos G., Watson Ch. The rat brain in Stereotaxic Coordinates - the new coronal set 2005, Elsevier Academic Press. 5th ed.
40. Scorticati C., Perazzo J.C., Rettori V., McCann S.M., De Laurentis A. Role of ammonia and nitric oxide in the decrease in plasma prolactin levels in prehepatic portal hypertensive male rats. Neuroimmunomodulation 2006, 13:152-159.
41. Monfort P., Cauli O., Montoliu C., Rodrgio R., Llansola M., Piedrafita B., el Mlili N., Boix J., Agustí A., Felipo V. Mechanisms of cognitive alterations in hyperammonemia and hepatic encephalopathy: therapeutical implications. Neurochem Int 2009, 55:106-112.
42. Aguilar M.A., Minarro J., Felipo V. Chronic hyperammonemia impairs active and passive avoidance behavior and conditional discrimination learning in rats. Exp Neurol 2000, 161:704-713.
43. Erceg S., Monfort P., Hernandez-Viadel M., Llansola M., Montoliu C., Felipo V. Restoration of learning ability in hyperammonemic rats by increasing extracellular cGMP in brain. Brain Res 2005, 1036:115-121.
44. Roozendaal R. System mediating acute glucocorticoid effects on memory consolidation and retrieval. Prog Neuropsychopharmacol Biol Psychiatry 2003, 27:1213-1223.
45. Dachir S., Kadar T., Robinzon B., Levy A. Cognitive deficits induced in young rats by long-term corticosterone administration. Behav Neural Biol 1993, 60:103-109.
46. McCaugh J.L., Cahill L., Roozendaal B. Involvement of the amygdala in memory storage: interaction with other brain systems. Proc Natl Acad Sci U S A 1996, 93:13,508-13,514.
47. Gray J.A., McNaughton N. Comparison between the behavioural effects of septal and hippocampal lesions: a review. Neurosci Biobehav Rev 1983, 7:119-188.
48. Van der Borght K., Leerlo P., Luiten P.G., Eggen B.J., Van der Zee E.A. Effects of active shock avoidance learning on hippocampal neurogenesis and plasma levels of corticosterone. Behav Brain Res 2005, 157:23-50.
49. Scorticati C., Prestifilippo J.P., Murer G., Lemberg A., Perazzo J.C. Functional alterations in central nervous system of prehepatic portal hypertensive rats. Medicina (B Aires) 2001, 61:673-675.
50. Grover V.P.B., Dresner M.A., Forton D.M., Counsell S., Larkman D.J., Patel N., et al. Current and future applications of magnetic resonance imaging and spectroscopy of the brain in hepatic encephalopathy. World J Gastroenterol 2006, 12:2969-2978.
51. Zwingmann C. Nuclear magnetic resonance studies of energy metabolism glutamine shunt in hepatic encephalopathy and hyperammonemia. J Neurosci Res 2007, 85:3429-3442.
52. Weissenborn K., Ahl B., Fischer-Wasels D., Van den Hoff J., Hecker H., Burchert W., et al. Correlations between magnetic resonance spectroscopy alterations and cerebral ammonia and glucose metabolism in cirrhotic patients with and without hepatic encephalopathy. Gut 2007, 56:1736-1742.
53. Miller D.B., O'Callaghan J.P. Effects of aging and stress on hippocampal structure and function. Metabolism 2003, 52:17-21.
54. Porter N.M., Landfield P.W. Stress hormones and brain aging: adding injury to insult?. Nat Neurosci 1998, 1:3-4.
55. Armanini M.P., Hutchins C., Stein B.A., Sapolsky R.M. Glucocorticoid endangerment of hippocampal neurons is NMDA-receptor dependent. Brain Res 1990, 532:7-12.
56. Lores-Arnaiz S., Perazzo J.C., Prestifilippo J.P., Lago N., D'Amico G., Czerniczyniec A., et al. Hippocampal mitochondrial dysfunction with decreased mtNOS activity in prehepatic portal hypertensive rats. Neurochem Int 2005, 47:362-368.
57. Joëls M. Corticosteroids effects in the brain: U-shape it. Trends Pharmacol Sci 2006, 27:244-250.
58. Joëls M. Functional actions of corticosteroids in the hippocampus. Eur J Pharmacol 2008, 583:312-321.
59. Hok V., Save E., Lenck-Santini P.P., Poucet B. Coding for spatial goals in the prelimbic/infralimbic area of the frontal cortex. Proc Natl Acad Sci U S A 2005, 102:4602-4607.
60. Neafsey E.J. Prefrontal cortical control of the autonomic nervous system: anatomical and physiological observations. Prog Brain Res 1990, 85:147-166.
61. Vertes R.P. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 2004, 51:32-58.
62. Fisk G.D., Wyss J.M. Descending projections of infralimbic cortex that mediate stimulation-evoked changes in arterial pressure. Brain Res 2000, 859:83-95.
63. Aranda L., Begega A., Sánchez-López J., Aguirre J.A., Arias J.L., Santín L.J. Temporary inactivation of the supramammillary area impairs spatial working memory and spatial reference memory retrieval. Physiol Behav 2008, 94:322-330.
64. Aggleton J.P., Brown M.W. Episodic memory, amnesia, and the hippocampal anterior thalamic axis. Behav Brain Sci 1999, 22:425-489.
65. Gaffan D. What is a memory system? Horel's critique revisited. Behav Brain Res 2001, 127:5-11.
66. Swanson L.W., Cowan W.M. An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 1977, 172:49-84.
67. Cauli O., Rodrigo R., Llansola M., Montoliu C., Monfort P., Piedrafita B., el Mlili N., Boix J., Agustí A., Felipo V. Glutamatergic and gabaergic neurotransmission and neuronal circuits in hepatic encephalopathy. Metab Brain Dis 2009, 24:69-80.
68. Herman J.P., Mueller N.K., Figueiredo H. Role of GABA and glutamate circuitry in hypothalamo-pituitary-adrenocortical stress integration. Ann N Y Acad Sci 2004, 1018:35-45.
69. Radley J.J., Gosselink K.L., Sawchenko P.E. A discrete GABAergic relay mediates medial prefrontal cortical inhibition of the neuroendocrine stress response. J Neurosci 2009, 29:7330-7340.
70. Leranth C., Hajszan T. Extrinsic afferent systems to the dentate gyrus. Prog Brain Res 2007, 163:63-79.
71. Felipo V. Contribution of altered signal transduction associated to glutamate receptors in brain to the neurological alterations of hepatic encephalopathy. World J Gastroenterol 2006, 12:7737-7743.
72. Muñoz M.D., Monfort P., Gaztelu J.M., Felipo V. Hyperammonemia impairs NMDA receptor-dependent long-term potentiation in the CA1 of rat hippocampus in vitro. Neurochem Res 2000, 25:437-441.