Nicotine improves learning and memory in rats: Morphological evidence for acetylcholine involvement

International Journal of Neuroscience

Volumn 114, Issue 9, 2004, Pages 1163-1179

  Üzüm, Gülay ^a   Díler, A Sarper ^a   Bahçekapili, Nesrín ^a   Taşyüreklí, Mustafa ^b   Zíylan, Y Zíya ^a  

^a ISTANBUL UNIVERSITY   (Turkey)

^b ISTANBUL UNIVERSITY   (Turkey)

Author keywords

Acetylcholine receptor; Cognitive function; Learning; Memory; Nicotine

Indexed keywords

ACETYLCHOLINE; NICOTINE;

ACETYLCHOLINE RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE CELL; COGNITION; CONTROLLED STUDY; ELECTRON MICROSCOPY; HIPPOCAMPUS; LEARNING; LONG TERM MEMORY; MALE; NEUROCHEMISTRY; NEUROMODULATION; NONHUMAN; PASSIVE AVOIDANCE; RAT; SHORT TERM MEMORY; TEMPORAL CORTEX;

ACETYLCHOLINE; ANIMALS; AVOIDANCE LEARNING; FRONTAL LOBE; HIPPOCAMPUS; MALE; MEMORY; MICROSCOPY, ELECTRON; NICOTINE; NICOTINIC AGONISTS; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; SYNAPTIC VESICLES;

EID: 4444220684     PISSN: 00207454     EISSN: None     Source Type: Journal    
DOI: 10.1080/00207450490475652     Document Type: Article

References (69)

1. Abrous, D. N., Adriani, W., Montaron, M. F., Aurousseau, G. R., Moal, M. L., & Piazza, P. V. (2002). Nicotine self-administration impairs hippocampal plasticity. The Journal of Neuroscience, 22(9), 3656-3662.
2. Algan, O., Furedy, J. J., Demirgören, S., Vincent, A., & Pögün, S. (1997). Effects of tobacco smoking and gender on interhemispheric cognitive function: Performance and confidence measures. Behavioral Pharmacology, 8, 416-428.
3. Arthur, D., & Levin, E. D. (2002). Chronic inhibition of alpha4beta2 nicotinic receptors in the ventral hippocampus of rats: Impacts on memory and nicotine response. Psychopharmacology (Berl.), 160(2), 140-145.
4. Aubert, I., Araujo, D. M., Cecyre, D., Robitaille, Y., Gauthier, S., & Quirion, R. (1992). Comparative alterations of nicotinic and muscarinic binding sites in Alzheimer's and Parkinson's diseases. The Journal of Neuroscience, 58, 529-541.
5. Bammer, G. (1982). Pharmacological investigations of neurotransmitter involvement in passive avoidance responding: A review and some new results. Neuroscience Biobehavioral Review, 6, 247-296.
6. Bancroft, A., & Leven, E. D. (2000). Ventral hippocampal alpha4 beta2 nicotinic receptors and chronic nicotine effects on memory. Neuropharmacology, 19, 2770-2778.
7. Barazangi, N., & Role, L. W. (2001). Nicotine-induced enhancement of glutamatergic and GABAergic synaptic transmission in the mouse amygdala. Journal of Neurophysiology, 86(1), 463-474.
8. Bartus, R. T., Dean, R. L., Beer, B., & Lippa, A. S. (1982). The cholinergic hypothesis of geriatric memory dysfunction. Science, 217, 408-417.
9. Benwell, M. E. M., Balfour, D. J. K., & Anderson, J. M. (1988). Evidence that tobacco smoking increases the density of (-)-[3H]-nicotine binding sites in human brain. Journal of Neurochemistry, 50, 1243-1247.
10. Bettany, J. H., & Levin, E. D. (2001). Ventral hippocampal α7 nicotinic receptor blockade and chronic nicotine effects on memory performance in the radial-arm maze. Pharmacology, Biochemistry, and Behavior, 70, 461-414.
11. Breese, C. R., Marks, M. J., Logel, J., Adams, C. E., Sullivan, B., Collins, A. C., & Leonard, S. (1997). Effects of smoking history on [3H]-nicotine binding in human postmortem brain. Journal of Pharmacology and Experimental Therapeutics, 282, 7-13.
12. Buccafusco, J. J., & Jackson, W. J. (1991). Beneficial effects of nicotine administered prior to a delayed matching-to-sample task in young and aged monkeys. Neurobiology of Aging, 12, 233-238.
13. Clarke, P. B. S. (1987). Nicotine and smoking; A perspective from animal studies. Psychopharmacologia, 92, 135-143.
14. Collins, A. C., & Marks, M. J. (1987). The effects of chronic nicotine administration on brain nicotinic receptor numbers. In W. R. Martin, G. R. Van loon, E. T. Iwamoto, & L. Davis (Eds.), Tobacco smoking and nicotine. Plenum Press, New York, pp. 439-450.
15. Cregan, E., Ordy, J. M., Palmer, E., Blosser, J., Wengenack, T., & Thomas, G. (1989). Spatial working memory enhancement by nicotine of aged long Evans rats in the T-maze. Social Neuroscience Abstracts, 15, 731.
16. Decker, M. W., Majchrzak, M. J., & Anderson, D. J. (1992). Effects of nicotine on spatial memory deficits in rats with septal lesions. Brain Research, 572, 281-285.
17. Dunnett, S. B., & Martel, F. L. (1990). Proactive interference effects on short-term memory in rats: 1. Basic parameters and drug effects. Behavioral Neuroscience, 104, 655-665.
18. Elrod, K., & Buccafusco, J. J. (1991). Correlation of the amnestic effects of nicotinic antagonists with inhibition of regional brain acetylcholinc synthesis in rats. Journal of Pharmacology and Experimental Therapeutics, 258, 403-409.
19. Erickson, C. K. (1971). Studies on mechanism of avoidance facilitation by nicotine. Psychopharmacologia, 22, 357-368.
20. Ernst, M., Matochik, Ja., Heishman, S. J., VanHorn, J. D., Jons, P. H., Flenningfield, J. E., & London, E. D. (2001). Effect of nicotine on brain activation during performance of a working memory task. Proceedings of National Academy of Sciences, USA., 98(8), 4728-4733.
21. Evangelista, A. M., & Izquirierdo, I. (1972). Effects of atropine on avoidance condition: Interaction with nicotine and comparison with N-methyl-atropine. Psychopharmacologia, 27, 241-248.
22. Fedele, E., Varnier, G., Ansaldo, M. A., & Raiteri, M. (1998). Nicotine administration stimulates the in vivo N-methyl-D-aspartate receptor/nitric oxide/cyclic GMP pathway in rat hippocampus through glutamate release. British Journal of Pharmacology, 125(5), 1042-1048.
23. Felix, R., & Levin, E. D. (1997). Nicotinic antagonist administration into the ventral hippocampus and spatial working memory in rats. Neuroscience, 81, 1009-1017.
24. Fisher, J. L., Pidoplichko, V. I., & Dani, J. A. (1998). Nicotine modifies the activity of ventral tegmental area dopaminergic neurons and hippocampal GABAergic neurons. Journal de Physiologies (Paris), 92(3-4), 209-213.
25. Fujii, S., Ji, Z., Morita, N., & Sumikawa, K. (1999). Acute and chronic nicotine exposure differentially facilitate the induction of LTP. Brain Research, 846(1), 137-143.
26. Fujii, S., Jia, Y., Yang, A., & Sumikawa, K. (2000). Nicotine reverses GABAergic inhibition of long-term potentiation induction in the hippocampal CA1 region. Brain Research, 863(1-2), 259-265.
27. Fujii, S., & Sumikawa, K. (2001). Acute and chronic nicotine exposure reverse age-related declines in the induction of long-term potentiation in the rat hippocampus. Brain Research, 894(2), 347-353.
28. Gilliam, D. M., & Schlesinger, K. (1985). Nicotine-produced relearning deficit in CS7B1/ 6J and DBA/2J mice. Psychopharmacology, 86, 291-295.
29. Gray, R., Rajan, A. S., Radcliffe, K. A., Yakehiro, M., & Dani, J. (1996). Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature, 383, 713-716.
30. Haroutunian, V., Barnes, E., & Davis, K. L. (1985). Cholinergic modulation of memory in rats. Psychopharmacology, 87, 266-271.
31. Henningfield, J. E., Keenan, R. M., & Clarke, P. B. S. (1996). In C. R. Schuster & M. J. Kuhar (Eds.), Pharmacological aspects of drug dependence (pp. 271-314). Chapter 8 Nicotine. Germany: Springer-Verlag, Berlin Heidelberg.
32. Hodges, H., Gray, J. A., Alien, Y., & Sinden, J. (1991). The role of the forebrain cholinergic projection system in performance in the radial-maze in memory-impaired rats. In F. Aldkofer & K. Thurau (Eds.), Effects of nicotine on biologic systems (pp. 389-399). Boston: Birkhauser Verlag.
33. Houlihan, M. E., & Pritchard, W. S., & Robinson, J. H. (2001). Effects of smoking/nicotine on performance and event-related potentials during a short-term memory scanning task. Psychopharmacology (Berl.), 156(4), 388-396.
34. Jones, G. M. M., Sahakian, B. J., Levy, R., Warburton, D. M., & Gray, J. A. (1992). Effect of acute subcutaneous nicotine on attention, information processing and short-term memory in Alzheimer's disease. Psychopharmacology, 108, 485-494.
35. Kem, W. R. (2000). The brain alpha 7 nicotinic receptor may be an important therapeutic target for the treatment of Alzheimer's disease: Studies with DMXBA (GTS-21). Behavioural Brain Research, (1-2), 169-181.
36. Lange, K. W., Wells, F. R., Jenner, P., & Marsden, C. D. (1993). Altered muscarinic and nicotinic receptor densities in cortical and subcortical brain regions in Parkinson's Disease. Journal of Neurochemistry, 60, 197-203.
37. Levin, E. D. (1992). Nicotinic systems and cognitive function. Psychopharmacology, 108, 417-431.
38. Levin, E. D., Bettegowda, C., Blosser, J., & Gordon, J. (1999). AR-R 17779 and alpha? nicotinic agonist, improves learning and memory in rats. Behavioral Pharmacology, 10(6-7), 675-680.
39. Levin, E. D., Castonguay, M., & Ellison, G. D. (1987). Effects of nicotinic receptor blocker, mecamylamine on radial arm maze performance in rats. Behavioral and Neural Biology, 48, 206-212.
40. Levin, E. D., & Rose, J. E. (1991). Nicotinic and muscarinic interactions and choise accuracy in the radial-maze. Brain Research Bulletin, 27, 125-128.
41. Levin, E. D., &. Simon, B. B. (1998). Nicotinic acetylcholine involvement in cognitive function in animals. Psychopharmacology, 138(3-4), 217-230.
42. Marks, M. J., Romm, E., Campbell, S. M., & Collins, A. C. (1989). Variation of nicotinic binding sites among inbred strains. Pharmacology Biochemistry and Behavior, 33, 679-689.
43. Matsuyama, S., Matsumoto, A., Enomoto, T., & Nishizaka, T. (2000). Activation of nicotinic acetylcholine receptors induces long-term potentiation in vivo in the intact mouse dentate gyrus. European Journal of Neuroscience, 12(10), 3741-3747.
44. Maurice, T., Lockhart, B. P., & Privat, A. (1996). Amnesia induced in mice by centrally administered beta-amyloid peptides involves cholinergic dysfunction. Brain Research, 706, 181-193.
45. McGehee, D. S., Heath, M. J. S., Gelber, S., Devay, P., & Role, L. W. (1995). Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science, 269, 1692-1696.
46. Mundy, W. R., & Iwamoto, E. T. (1988). Nicotine impairs acquisition of radial-arm maze performance in rats. Pharmacology Biochemistry and Behavior, 40, 119-122.
47. Newcomer, J. W., & Krystal, J. H. (2001). NMDA receptor regulation of memory and behavior. Hippocampus, 11, 529-542.
48. Newhouse, P. A., & Kelton, M. (2000). Nicotinic systems in central nervous systems disease: Degenerative disorders and beyond. Pharmaceutica Acta Helvetiae, 74(2-3), 91-101.
49. Olariu, A., Tran, M. H., Yamada, K., Mizuno, M., Hefco, V., & Nabeshima, T. (2001). Memory deficits and increased emotionality induced by beta-amyloid (25-35) are correlated with the reduced acetylcholine release and altered phorbol dibutyrate binding in the hippocampus. Journal of Neural Transmission, 188(8-9), 1065-1079.
50. Park, S., Knopick, C., McGurk, S., & Meltzer, H. Y. (2000). Nicotine impairs spatial working memory while leaving spatial attention intact. Neuropsychopharmacology, 22(2), 200-209.
51. Pauly, J. R., Marks, M. J., Stitzel, J. A., Gross, S. D., & Collins, A. C. (1991). Chronic nicotine infusions and regulation of CNS nicotinic cholinergic receptors: An autoradiographic study. Journal of Pharmacology and Experimental Therapeutics,. 258, 1127-1136.
52. Pauly, J. R., Sheehan, K., Sparks, J. A., & Gairola, C. G. (1997). Increased density of neuronal nicotinic receptor subtypes in rats repeatedly exposed to tobacco smoke. Society for Research on Nicotine and Tobacco Annual Meeting, Paper 131.
53. Pauly, R. (1998). Nicotinic cholinergic receptor deficits in Alzhemier's disease: Where's the smoke? Alzheimer Disease Review, 3, 28-34.
54. Pomerleau, O. F., & Rosecrans, J. (1989). Neuroregulatory effects of nicotine. Psychoneuroendocrinology, 14(6), 407-423.
55. Pögün, S., Demirgören, S., Kutay, F. Z., & Okur, B. (1992). Learning induces changes in the central cholinergic system of the rat in a sexually dimorphic pattern. International Journal of Psychophysiology, 13, 17-23.
56. Sahakian, B. J., & Coull, J. T. (1994). Nicotine and tetrahydroaminoacradine: evidence for improved attention in patients with dementia of the Alzhemier type. Drug Development Research, 31, 80-88.
57. Sansone, M., Castellano, C., Battaglia, M., & Amassari-Teule, M. (1991). Effects of oxiracetam-nicotine combinations on active and passive avoidance learning in mice. Pharmacology, Biochemistry, and Behavior, 39, 197-200.
58. Sasaki, H., Yanai, M., Megoro, K., Sekizawa, K., Ikarashi, Y., Maruyatima, Y., Yamamoto, M., Matsuzaki, Y., & Takishima, T. (1991). Nicotine improves cognitive disturbance in rodents fed with a choline-deficient diet. Pharmacology, Biochemistry, and Behavior, 38, 921-925.
59. Stolerman, I. P., Mirza, N. R., Hahn, B., & Shoaib, M. (2000). Nicotine in an animal model of attention. European Journal of Pharmacology, 393(1-3), 147-154.
60. Villarreal, D. M., Do, V., Haddad, E., & Derrick, E. (2002). NMDA receptor antagonists sustain LTP and spatial memory: Active processes mediate LTP decay. Nature Neuroscience, 5(1), 48-52.
61. Warburton, D. M. (1992). Nicotine as a cognitive enhancer. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 16, 181-191.
62. Watanabe, H., Ni, J. W., Sakai, Y., Matsumoto, K., Murakami, Y., & Tohda, M. (1996). Permanent occlusion of bilateral internal carotid arteries produces cognitive deficits in two learning behavior tasks. Japanese Journal of Psychopharmacology, 16, 19-24.
63. Wesnes, K., & Warburton, D. M. (1983). Smoking, nicotine and human performance. Pharmacology & Therapeutics, 21, 189-208.
64. White, H. K., & Levin, E. D. (1999). Four-week nicotine skin patch treatment effects on cognitive performance in Alzheimer's disease. Psychopharmacology (Berl.), 143(2), 158-165.
65. Williams, M., & Arneric, sp. (1997). Alzheimer's Disease: Prospects for treatment in the next decade. In J. D. Brioni & M. W. Decker (Eds.), Pharmacological treatment of Alzheimer's Disease. New York: Wiley-Liss Inc.
66. Wilson, A. L., Langley, L. K., Monley, J., Bauer, T., Rottunda, S., McFalls, E., Kovera, C., & McCarten, J. R. (1995). Nicotine patches in Alzheimer's disease: Pilot study on learning, memory and safety. Pharmacology, Biochemistry, and Behavior, 51, 509-514.
67. Wonnacott, S. (1990). The paradox of nicotinic acetylcholinc receptor upregulation by nicotine. Trends in Pharmacological Sciences, 11, 216-219.
68. Yamaguchi, T., Suzuki, M., & Yamamoto, M. (1995). YM796 a novel muscaninic agonist, improves the impairment of learning behavior in a rat model of chronic focal cerebral ischemia. Brain Research, 669, 107-114.
69. Zoli, M., Picciotto, M. R., Ferrari, R., Cocchi, D., & Changeux, J. P. (1999). Increased neurodegenenation during ageing in mice lacking high-affinity nicotine receptors. EMBO Journal, 18(5), 1235-1244.