Ginsenoside Rg1 restores the impairment of learning induced by chronic morphine administration in rats

Journal of Psychopharmacology

Volumn 23, Issue 1, 2009, Pages 74-83

  Qi, D ^a   Zhu, Y ^a   Wen, L ^b   Liu, Q ^a   Qiao, H ^a  

^a SHANDONG UNIVERSITY OF TRADITIONAL CHINESE MEDICINE   (China)

^b SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Learning; Long term potentiation (LTP); Morphine; N methyl D aspartate (NMDA) receptor; Rg1

Indexed keywords

DIZOCILPINE; GINSENOSIDE RG 1; MORPHINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRODE; ELECTROPHYSIOLOGY; GINSENG; IN VIVO STUDY; LATENT PERIOD; LEARNING DISORDER; LONG TERM POTENTIATION; MALE; MAZE TEST; MORPHINE ADDICTION; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL DISCRIMINATION;

ANALGESICS, OPIOID; ANIMALS; BEHAVIOR, ANIMAL; CENTRAL NERVOUS SYSTEM AGENTS; DIZOCILPINE MALEATE; ELECTRIC STIMULATION; ELECTRODES; GINSENOSIDES; HIPPOCAMPUS; INJECTIONS, SUBCUTANEOUS; LEARNING DISORDERS; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MEDICINE, CHINESE TRADITIONAL; MORPHINE; PANAX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 58649111216     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881107082950     Document Type: Article

References (67)

1. Aguilar M.A., Minarro J., Simon V.M. (1998) Dose-dependent impairing effects of morphine on avoidance acquisition and performance in male mice. Neurobiol Learn Behav 69: 92-105
2. Bliss T.V., Collingridge G.L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39
3. Bliss T.V., Collingridge G.L., Morris R.G. (2003) Introduction. Long-term potentiation and structure of the issue. Philos Trans R Soc Lond B Biol Sci 358: 607-611
4. Chang Y.S., Wu C.R., Ho Y.L., Hsieh M.T. (1998) Effects of Panax ginseng and its constituents on drug-induced memory impairment in rats. Proc 7th Intl Symp Ginseng 289-299
5. Doyle C., Hö-lscher C., Rowan M.J., Anwyl R. (1996) The selective neuronal NO synthase inhibitor 7-nitor-indazole blocks both long-term potentiation and depotentiation of field EPSPs in rat hippocampal CA1 in vivo. J Neurosci 16: 418-424
6. Eisch A.J., Barrot M., Schad C.A., Self D.W., Nestler E.J. (2000) Opiates inhibit neurogenesis in the adult rat hippocampus. Proc Natl Acad Sci USA 97: 7579-7584
7. Fan G.H., Wang L.Z., Qiu H.C., Ma L., Pei G. (1999) Inhibition of calcium/calmodulin-dependent protein kinase II in rat hippocampus attenuates morphine tolerance and dependence. Mol Pharmacol 56: 39-45
8. Guerra D., Sole A., Cami J., Tobena A. (1987) Neuropsychological performance in opiate addicts after rapid detoxification. Drug Alcohol Depend 20: 261-270
9. Inhee M.J., Hong H.S., Boo J.H., Lee K.H., Yun S.H., Cheong M.Y., Joo I., Huh K., Jung M.W. (2001) Ginsenoside Rb1 and Rg1 improve spatial Learning and increase hippocampal synaptophysin level in mice. J Neurosci Res 63: 509-515
10. Ito Y., Tabata K., Makimura M., Fukuda H. (2001) Acute and chronic intracerebroventricular morphine infusions affect long-term potentiation differently in the lateral perforant path. Pharmacol Biochem Behav 70: 353-358
11. Jaenickes B., Kim E.J., Ahn J.W., Lee H.S. (1991) Effect of Panax ginseng extract on passive avoidance retention in old rats. Arch Pharm Res 14: 25-29
12. Jarrard L.E. (1993) On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol 60: 9-26
13. Jin S.H., Park J.K., Nam K.Y., Park S.N., Jung N.P. (1999) Korean red ginseng saponins with low ratios of protopanaxdiol and protopanaxatriol saponin improve scopolamine-induced learning disability and spatial working memory in mice. J Ethnopharmacol 66: 123-129
14. Kelley A.E., Bakshi V.P., Fleming S., Holahan M.R. (2000) A pharmacological analysis of the substrates underlying conditioned feeding induced by repeated opioid stimulation of the nucleus accumbens. Neuropsychopharmacology 23: 455-467
15. Kim H.S., Hong Y.T., Jang C.G. (1998) Effects of the ginsenosides Rg1 and Rb1 on morphine-induced hyperactivity and reinforcement in mice. J Pharma Pharmaco l50: 555-560
16. Lasarova M.B., Mosharrof A.H., Petkov V.D., Markovska V.L., Petkov V.V. (1987) Effect of piracetam and of standardized ginseng extract on the electroconvulsive shock-induced memory disturbances in 'step-down' passive avoidance. Acta Physiol Pharmacol Bulg 13: 11-17
17. Leshner A.I. (1997) Addiction is a brain disease, and it matters. Science 278: 45-47
18. Liu M., Zhang J.T. (1996) Effect of ginsenoside Rg1 on c-fos gene expression and cAMP levels in rat hippocampus. Acta Pharmacol Sin 17: 171-174
19. Lou L., Zhou T., Wang P., Pei G. (1999) Modulation of Ca 2+/calmodulindependent protein kinase II activity by acute and chronic morphine administration in rat hippocampus: differential regulation of α and β isoforms. Mol Pharmacol 55: 557-563
20. Lynch G.S., Jensen R.A., McGauch J.L., Davila K., Oliver M.W. (1981) Effects of enkephalin, morphine and naloxone on the electrical activity of the in vitro hippocampal slice preparation. Exp Neurol 71: 527-540
21. Lyubimov I.I., Borzenkov V.M., Chepurnova N.E., Chepurnov S.A. (1997) Effect of a polysaccharide fraction of ginseng root on learning and memory in rats (using an active escape response as an example). Neurosci Behav Physiol 27: 555-558
22. Malenka R.C., Nicoll R.A. (1999) Long-term potentiation-a decade progress? Science 285: 1870-1874
23. Morris R G M, Anderson E., Lynch G.S., Baudry M. (1986) Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319: 774-776
24. Moser E.I., Krobert K.A., Moser M.B., Morris R G M (1998) Impaired spatial learning after saturation of long-term potentiation. Science 281: 2038-2042
25. Nestler E.J. (2001) Total recall-the memory of addiction. Science 292: 2266-2267
26. Nestler E.J., Aghajanian G.K. (1997) Molecular and cellular basis of addiction. Science 278: 58-63
27. Ni X.H., Ohta H., Watanabe H., Matsumoto K. (1993) Panax ginseng extract improves scopolamine-induced deficits in working memory performance in the T-maze delayed alternation task in rats. Phytotherapy Res 7: 49-52
28. Nitta H., Matsumoto K., Shimizu M., Ni X.H., Watanabe H. (1995 a) Panax ginseng extract improves the performance of aged Fischer 344 rats in radial maze task but not in operant brightness discrimination task. Biol Pharm Bull 18: 1286-1288
29. Nitta H., Matsumoto K., Shimizu M., Ni X.H., Watanabe H. (1995 b) Panax ginseng extract improves the scopolamine-induced disruption of 8-arm radial maze performance in rats. Biol Pharm Bull 18: 1439-1442
30. O'Brien C.P. (1997) A range of research-based pharmacotherapies for addiction. Science 278: 66-70
31. Petkov V.D., Mosharrof A.H. (1987) Effects of standardized ginseng extract on learning, memory and physical capabilities. Am J Chin Med 15: 19-29
32. Petkov V.D., Mosharrof A.H., Petkov V.V., Kehayov R.A. (1990) Age-related differences in memory and in the memory effects of nootropic drugs. Acta Physiol Pharmacol Bulg 16: 28-36
33. Petkov V.D., Yinglin C., Todorov I., Lazarova M., Getova D., Stancheva S., Alova L. (1992) Behavioral effects of stem-leaves extract from Panax ginseng C.A. Meyer. Acta Physiol Pharmacol Bulg 18: 41-48
34. Petkov V.D., Kehayov R., Belcheva S., Konstantinova E., Petkov V.V., Getova D., Markovska V. (1993) Memory effects of standardized extracts of Panax ginseng (G115). Ginkgo biloba (GK 501) and their combination Gincosan (PHL-00701). Planta Med 59: 106-114
35. Pu L., Bao G.B., Xu N.J., Ma L., Pie G. (2002) Hippocampal long-term potentiation is reduced by chronic opiate treatment and can be restored by re-exposure to opiates. J Neurosci 22: 1914-1921
36. Qiao H.F., Yang S., Zhou W.X., Zhang Y.X. (2006) NT-1, an active constituent extracted from Tiaoxin Recipe, enhances long-term potentiation of CA1 subfield in rat hippocampal slices. Life Sci 79: 8-15
37. Ribeiro Do Couto B., Aguilar M.A., Manzanedo C., Rodríguez-Arias M., Miñarro J. (2005) NMDA glutamate but not dopamine antagonists blocks drug-induced reinstatement of morphine place preference. Brain Res Bull 64: 493-503
38. Riedel G., Micheau J. (2001) Function of the hippocampus in memory formation: desperately seeking resolution. Prog Neuropsychopharmacol Biol Psychiatry 25: 835-853
39. Riedel G., Micheau J., Lam A G M, Roloff E., Martin S. J, Bridge H., Hoz L., Poeschel B., McCulloch J., Morris R G M (1999) Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat Neurosci 2: 898-905
40. Robbins T.W., Everitt B.J. (1999) Drug addiction: bad habits add up. Nature 398: 567-570
41. Robinson J.H., Deadwyler S.A. (1980) Morphine excitation: effects on field potentials recorded in the in vitro hippocampal slice. Neuropharmacology 19: 507-514
42. Saito H. (1990) Effects of ginsenoside Rb1 and ginsenoside Rg1 on learning and memory. In Shibata S, Ohtsuka Y, Saito H (eds). Recent advances in ginseng studies. Hirokawa, Tokyo
43. Saito H., Tsuchiya M., Naka S., Takagi K. (1977) Effects of Panax ginseng root on conditioned avoidance response in rats. Jpn J Pharmacol 27: 509-516
44. Saito H., Tsuchiya M., Naka S., Takagi K. (1979) Effects of Panax ginseng root on acquisition of sound discrimination behavior in rats. Jpn J Pharmacol 29: 319-324
45. Sala M.M., Braida D.D., Leone M.M., Calcaterra P.P., Frattola D.D., Gori E.E. (1994) Chronic morphine affects working memory during treatment and withdrawal in rats: possible residual long-term impairment. Behav Pharmacol 5: 570-580
46. Salmanzadeh F., Fathollahi Y., Semnanian S., Shafizadeh M., Kazemnejad A. (2003) Dependence on morphine leads to a prominent sharing among the different mechanisms of long-term potentiation in the CA1 region of rat hippocampus. Brain Res 963: 93-100
47. Smith J.B. (1985) Effects of single and repeated daily injections of morphine, clonidine, and L-nantradol on avoidance responding of rats. Psycopharmacology 87: 425-429
48. Spain J.W., Newsom G.C. (1991) Chronic opioids impair acquisition of both radial maze and Y. maze choice escape. Psychopharmacology 105: 101-106
49. Stringer J.L., Greenfield L.J., Hackett J.T., Guyenet P.G. (1983) Blockade of long-term potentiation by phencyclidine and sigma opiates in the hippocampus in vivo and in vitro. Brain Res 280: 127-138
50. Tang Y.P., Shimizu E., Dube G.R., Rampon C., Kerchner G.A., Zhuo M., Liu G., Tsien J.Z. (1999) Genetic enhancement of learning and memory in mice. Nature 401: 63-69
51. Trujillo K.A., Akil H. (1991) Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801. Science 251: 85-87
52. Trujillo K.A. (2000) Are NMDA receptors involved in opiate-induced neural and behavioral plasticity? A review of preclinical studies. Psychopharmacology (Berl) 151: 121-141
53. Vorel S.R., Liu X., Hayes R.J., Spector J.A., Gardner E.L. (2001) Relapse to cocaine-seeking after hippocampal theta burst stimulation. Science 292: 1175-1178
54. Wang X.Y., Zhang J.T. (2001) Effect of ginsenoside Rg1 on synaptic plasticity of freely moving rats and its mechanism of action. Acta Pharmacol Sin 22: 657-662
55. Watanabe H., Ohta H., Matsumoto K. (1990) Effect of ginseng on spontaneous motor activity, water-maze learning and central dopaminergic systems in old rats. In Shibata S, Ohtsuka Y, Saito H (eds). Recent advances in ginseng studies. Hirokawa, Tokyo
56. Wen T.C., Yoshimura H., Matsuda S., Lim J.H., Sakanaka M. (1996) Ginseng root prevents learning disability and neuronal loss in gerbils with 5-minute forebrain ischemia. Acta Neuropathol 91: 15-22
57. Westbrook R.F., Good A.J., Kiernan M.J. (1997) Microinjection of morphine into the nucleus accumbens impairs contextual learning in rats. Behav Neurosci 111: 289-296
58. Whitlock J.R., Heynen A.J., Shuter M.G., Bear M.F. (2006) Learning induces long-term potentiation in the hippocampus. Science 313 (25). 1093-1097
59. Williams J.T., MacDonald J.C., Manzoni O. (2001) Cellular and synaptic adaptations mediating opioid dependence. Physiol Rev 81: 299-343
60. Woolf C.J., Salter M.W. (2000) Neuronal plasticity: increasing the gain pain. Science 288: 1765-1768
61. Xu L., Anwyl R., Rowan M.J. (1997) Behavioral stress facilitates the induction of long-term depression in the hippocampus. Nature 387: 497-500
62. Yang S., Qiao H.F., Wen L., Zhou W.X., Zhang Y.X. (2005) D-serine enhances impaired long-term potentiation in CA1 subfield of hippocampal slices from aged senescence-accelerated mouse prone/8. Neurosci Lett 379: 7-12
63. Ying Y., Zhang J.T., Shi C.Z., Qu Z.W., Liu Y. (1994) Study on the nootropic mechanism of ginsenoside Rb1 and Rg1 influence on mouse brain development. Acta Pharmacol Sin 29: 241-243
64. Zhang J.T., Qu Z.W., Liu Y., Deng H.L. (1990) Preliminary study on antianistic mechanism of ginsenoside Rg1 and Rb1. Chin Med J (Engl) 103: 932-938
65. Zhong Y.M., Nishijo, H., Uwano T., Yamaguchi H., Ono T. 1998. Red ginseng ameliorates place learning deficits in aged rats and in young rats with selective hippocampal lesions. Proc 7th Intl Symp Ginseng P1-11
66. Zhou H., Ge X., Wang L.Z., Ma L., Pei G. (1999) Attenuation of morphine tolerance and dependence in scopolamine-treated rats. NeuroReport 10: 2007-2010
67. Zhao R., McDaniel W.F. (1998) Ginseng improves strategic learning by normal and brain-damaged rats. Neuroreport 9: 1619-1624