Strategies that support declining cholinergic neurotransmission in Alzheimer's disease patients

Gerontology

Volumn 45, Issue SUPPL. 1, 1999, Pages 3-14

  Sirviö, Jouni ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

Author keywords

Acetylcholine; Alzheimer's disease; Cholinergic hypothesis; Treatment

Indexed keywords

3 METHYL 5 (1 METHYL 2 PYRROLIDINYL)ISOXAZOLE; 4 AMINOBUTYRIC ACID A RECEPTOR; ACETYLCHOLINE; ALPHA 2 ADRENERGIC RECEPTOR; ATIPAMEZOLE; CHOLINE; CHOLINESTERASE INHIBITOR; CYCLOSERINE; DIAZOXIDE; DONEPEZIL; EXCITATORY AMINO ACID; LEVACECARNINE; LINOPIRDINE; METRIFONATE; MUSCARINIC M2 RECEPTOR ANTAGONIST; NERVE GROWTH FACTOR; NEUROTRANSMITTER; PHOSPHATIDYLCHOLINE; RIVASTIGMINE; SELEGILINE; SEROTONIN 3 RECEPTOR; TACRINE; XANOMELINE;

ALZHEIMER DISEASE; AUTOPSY; BIOCHEMISTRY; BRAIN BIOPSY; CHOLINERGIC NERVE CELL; CHOLINERGIC TRANSMISSION; CLINICAL TRIAL; CONFERENCE PAPER; DISEASE CONTROL; DISEASE COURSE; HISTOPATHOLOGY; HUMAN; LEARNING; MEMORY; META ANALYSIS; METABOLISM; NONHUMAN; PAIN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; RAT;

ACETYLCHOLINE; AGED; ALZHEIMER DISEASE; CHOLINESTERASE INHIBITORS; HUMANS; LONG-TERM POTENTIATION; NERVE GROWTH FACTORS; NEURAL PATHWAYS; RECEPTORS, CHOLINERGIC; SYNAPTIC TRANSMISSION;

EID: 0032928310     PISSN: 0304324X     EISSN: None     Source Type: Journal    
DOI: 10.1159/000052759     Document Type: Conference Paper

References (127)

1. Masliah E: Mechanisms of synaptic dysfunction in Alzheimer's disease. Histol Histopathol 1995;10:509-519.
2. Geula C, Mesulam M-M: Cholinergic systems and related neuropathological predilection patterns in Alzheimer disease; in Terry RD, Katzman R, Bick KL(eds): Alzheimer Disease. New York, Raven Press, 1994, pp 263-291.
3. Wenk GL: The nucleus basalis magnocellularis cholinergic system: One hundred years of progress. Neurobiol Learn Mem 1997;67:85-95.
4. Gauthier S: Clinical Diagnosis and Management of Alzheimer's Disease. London, Dunitz, 1996.
5. Francis PT, Cross AJ, Bowen DM: Neurotransmitters and neuropeptides; in Terry RD, Katzman R, Bick KL (eds): Alzheimer Disease. New York, Raven Press, 1994, pp 247-261.
6. Reinikainen KJ, Soininen H, Riekkinen PJ: Neurotransmitter changes in Alzheimer's disease: Implications to diagnostics and therapy. J Neurosci Res 1990;27:576-586.
7. Foote SL, Morrison JH: Extrathalamic modulation of cortical function. Annu Rev Neurosci 1987;10:67-95.
8. Mesulam MM: Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann Neurol 1990;28: 597-613.
9. Hasselmo ME: Neuromodulation and cortical function: Modeling the physiological basis of behavior. Behav Brain Res 1995;67:1-27.
10. McGaugh JL, Cahill L: Interactions of neuromodulatory systems in modulating memory storage. Behav Brain Res 1997;83:31-38.
11. Gomez-Isla T, Hyman BT: The role of damage to temporal lobe memory-related neural systems in early Alzheimer's disease; in Salonen T, Sivenius J, Sirviö J, Riekkinen P Jr, Salminen A (eds): 20 Years of Brain Research in Kuopio. Kuopio, Salminen Offsetpaino L, Tuovinen, 1996, pp 29-36.
12. Soininen HS, Riekkinen PJ Sr: Apolipoprotein E, memory and Alzheimer's disease. Trends Neurosci 1996;19:224-227.
13. Bartus RT, Dean RL, Beer B, Lippa AS: The cholinergic hypothesis of geriatric memory dysfunction. Science 1982;217:408-417.
14. Perry EK: The cholinergic hypothesis - ten years on. Br Med Bull 1986;42:63-69.
15. Cooper JR, Bloom FE, Roth RH: The Biochemical Basis of Neuropharmacology, ed 7. New York, Oxford University Press, 1996.
16. Barbelevien A, MacKenzie ET, Dauphin F: Regional cerebral blood flow responses to neurochemical stimulation of the substantia innominata in an anaesthetized rat. Neurosci Lett 1995;190:81-84.
17. Young AB, Penney JB Jr: Neurotransmitter receptors in Alzheimer disease: in Terry RD. Katzman R, Bick KL (eds): Alzheimer Disease. New York, Raven Press, 1994, pp 293-303.
18. Warpman U, Nordberg A: Epibatidine and ABT 418 reveal selective losses of alpha 4 beta 2 nicotinic receptors in Alzheimer brains. Neuroreport 1995;6:2419-2423.
19. Quirion R, Richard J, Wilson A: Muscarinic and nicotinic modulation of cortical acetylcholine release monitored by in vivo microdialysis in freely moving adult rats. Synapse 1994;17: 92-100.
20. Sirviö J, Riekkinen PJ: Brain and cerebrospinal fluid cholinesterases in Alzheimer's disease, Parkinson's disease and aging. A critical review of clinical and experimental studies. J Neural Transm 1992;4:337-358.
21. Fernandez HL, Moreno RD, Inestrosa NC: Tetrameric (G4) acetylcholinesterase: Structure, localization and physiological regulation. J Neurochem 1996;66:1335-1346.
22. Thoenen H: Neurotrophins and neuronal plasticity. Science 1995;270:593-598.
23. Mufson EJ, Lavine N, Jaffar S, Kordower JH, Quirion R, Saragovi HU: Reduction in p 140-TrkA receptor protein within the nucleus basalis and cortex in Alzheimer's disease. Exp Neurol 1997;146:91-103.
24. Page KJ, Sofroniew MV: The ascending basal forebrain cholinergic system. Prog Brain Res 1996;107:513-522.
25. Givens B, Sarter M: Modulation of cognitive processes by transsynaptic activation of the basal forebrain. Behav Brain Res 1997;84:1-22.
26. Acquas E, Wilson C, Fibiger HC: Conditioned and unconditioned stimuli increase frontal cortical and hippocampal acetylcholine release: Effects of novelty, habituation and fear. J Neurosci 1996;16:3089-3096.
27. Sarter M, Bruno JP: Cognitive functions of cortical acetylcholine: Toward a unifying hypothesis. Brain Res Rev 1997;23:28-46.
28. Sarter M, Bruno JP, Dudchenko P: Activating the damaged basal forebrain cholinergic system: Tonic stimulation versus signal amplification. Psychopharmacology (Berl) 1990;101:1-17.
29. Everitt BJ, Robbins TW; Central cholinergic systems and cognition. Annu Rev Psychol 1997;48:649-684.
30. Robbins TW, McAlonan G, Muir JL, Everitt BJ: Cognitive enhancers in theory and practice: Studies of the cholinergic hypothesis of cognitive deficits in Alzheimer's disease. Behav Brain Res 1997;83:15-23.
31. Heckers S, Ohtake T, Wiley RG, Lappi DA, Geula C, Mesulam M-M: Complete and selective cholinergic denervation of rat neocortex and hippocampus but not amygdala by an immunotoxin against the p75 NGF receptor. J Neurosci 1994;14:1271-1289.
32. Blokland A: Acetylcholine: A neurotransmitter for learning and memory. Brain Res Rev 1996; 21:285-300.
33. Sarter M, Hagan J, Duchenko P: Behavioral screening for cognition enhancers: From indiscriminate to valid testing. I. Psychopharmacology (Berl) 1992;107:144-159.
34. Winkler J, Suhr ST, Gage FH, Thal LJ, Fisher LJ: Essential role of neocortical acetylcholine in spatial memory. Nature 1995;375:484-487.
35. McClelland JL, McNaughton BL, O'Reilly RC: Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychol Rev 1995;102:419-457.
36. Eichenbaum H: How does the brain organize memories. Science 1997;277:330-332.
37. Weinberger NM: Learning-induced changes of auditory receptive fields. Curr Opin Neurobiol 1993;3:570-577.
38. McCormick DA, Bal T: Sleep and arousal: Thalamocortical mechanisms. Annu Rev Neurosci 1997;20:185-215.
39. Marin DB, Davis KL: Experimental therapeutics: in Bloom FE, Kupfer DJ (eds): Psychopharmacology, The Fourth Generation of Progress. New York, Raven Press, 1995, pp 1417-1426.
40. Patel SV: Pharmacotherapy of cognitive impairment in Alzheimer's disease: A review. J Geriatr Psychiatry Neurol 1995;8:81-95.
41. Giacobini E: New trends in cholinergic therapy for Alzheimer disease: Nicotinic agonists or cholinesterase inhibitors? Prog Brain Res 1996; 109:311-323.
42. Thal LJ: Cholinomimetic treatment of Alzheimer's disease. Prog Brain Res 1996; 109: 299-309.
43. Kumar V, Calache M: Treatment of Alzheimer's disease with cholinergic drugs. Int J Clin Pharmacol Ther 1991;29:23-37.
44. Sudhof TC: The synaptic vesicle cycle: A cascade of protein-protein interactions. Nature 1995;375:645-653.
45. Holttum JR. Gershon S: The cholinergic model of dementia, Alzheimer type: Progression from the unitary transmitter concept. Dementia 1992;3:174-185.
46. Ögren SO, Andersson P, Pramanik A: Galanin: Potential role in learning and memory. Eur Neuropsychopharmacol 1993;3:195-196.
47. 2-muscarinic receptor antagonist in aged memory-impaired rats. J Neurosci 1995;15:1455-1462.
48. Aura J, Sirviö J, Riekkinen P Jr: Methoctramine moderately improves memory but pirenzepine disrupts performance in delayed nonmatching to position test. Eur J Pharmacol 1997;333:129-134.
49. Bodick NC, Offen WW, Levey AI, Cutler NR, Gauthier SG, Satlin A, Shannon HE, Tollefson GD, Rasmunssen K, Bymaster FP, Hurley DJ, Potter WZ, Paul SM: Effects of xanomeline, a selective muscarinic receptor agonist, on cognitive function and behavioral symptoms in Alzheimer disease. Arch Neurol 1997;54:465-473.
50. Giacobini E: Cholinesterase inhibitors: From molecular structure to Alzheimer therapy; in Salonen T, Sivenius J. Sirviö J, Riekkinen P Jr, Salminen A (eds): 20 Years of Brain Research in Kuopio. 1996, Offsetpaino L, Tuovinen Ltd. pp 55-62.
51. Quirion R: Cholinergic markers in Alzheimer disease and the autoregulation of acetylcholine release. J Psychiatry Neurosci 1993;18:226-234.
52. Lawrence AD, Sahakian BJ: Alzheimer's disease, attention and the cholinergic system. Alzheimer Dis Assoc Disord 1995;9:43-49.
53. Arneric SP, Sullivan JP, Decker MW, Brioni JD, Bannon AW, Briggs CA, Donnelly-Roberts D, Radek RJ, Marsh KC, Kynel J, Williams M, Boccafusco JJ: Potential treatment of Alzheimer disease using cholinergic channel activators (ChCAs) with cognitive enhancement, anxiolytic-like, and cytoprotective properties. Alzheimer Dis Assoc Disord 1995;9(suppl):50-61.
54. Albuquerque EX, Pereira EF, Castro EF, Alkondon M, Reinhardt S, Schroder H, Maelicke A: Nicotinic receptor function in the mammalian central nervous system. Ann NY Acad Sci 1995;757:48-72.
55. Riekkinen P Jr, Riekkinen M, Soininen H, Kuikka J, Laakso M, Riekkinen P Sr: Frontal dysfunction blocks the therapeutic effect of THA on attention in Alzheimer's disease. Neuroreport 1997;8:1845-1849.
56. Riekkinen M, Soininen H, Riekkinen P Sr, Laakso M, Helkala E-L, Partanen J, Riekkinen P Jr: Tetrahydroaminoacridine improves the recency effect in Alzheimer's disease. Neuroscience 1998;83:471-479.
57. Geddes JW, Cotman CW: Plasticity, pathology and Alzheimer's disease. Neurobiol Aging 1989;10:571-573.
58. Samuels SC, Davis KL: A risk-benefit assessment of tacrine in the treatment of Alzheimer's disease. Drug Saf 1997;16:66-77.
59. McGuffey EC: Alzheimer's disease - An overview for the pharmacist. J Am Pharm Assoc (Wash) 1997;37:347-352.
60. Perry EK, Perry RH: Acetylcholine and hallucinations: Disease-related compared to drug-induced alterations in human consciousness. Brain Cogn 1995;28:240-258.
61. Jones DNC, Barnes JC, Kirby DL. Higgins GA: Age-associated impairments in a test of attention: Evidence for involvement of cholinergic systems. J Neurosci 1995;15:7282-7292.
62. Yavich L, Sirviö J, Haapalinna A, Puumala T, Koivisto E, Heinonen E, Riekkinen P Sr: The systemic administration of tacrine or selegiline facilitate spatial learning in aged Fisher 344 rats. J Neural Transm 1996;103:619-626.
63. Aubert I, Rowe W, Meaney MJ, Gauthier S, Quirion R: Cholinergic markers in aged cognitively impaired Long-Evans rats. Neuroscience 1995;67:277-292.
64. Koliatsos VE: Biological therapies for Alzheimer's disease: Focus on trophic factors. Crit Rev Neurobiol 1996;10:205-238.
65. Nordberg A: Pharmacological treatment of cognitive dysfunction in dementia disorders. Acta Neurol Scand 1996;168(suppl):87-92.
66. Winkler J, Ramirez GA, Kuhn HG, Peterson DA, Day-Lollini PA, Stewart GR, Tuszynski MH, Gage FH, Thal LJ: Reversible Schwann cell hyperplasia and sprouting of sensory and sympathetic neurites after intraventricular administration of nerve growth factor. Ann Neurol 1997;41:82-93.
67. Frade JM, Rodriguez-Tebar A, Barde YA: Induction of cell death by endogenous nerve growth factor through its p75 receptor. Nature 1996;383:166-168.
68. NGFR-deficient mice. Science 1996;274:1729-1732.
69. Giacobini E, Mori F, Lai C-C: The effect of cholinesterase inhibitors on the secretion of APPS from rat brain cortex. Ann NY Acad Sci 1996;777:393-398.
70. Parnetti L, Senin U, Mecocci P: Cognitive enhancement therapy for Alzheimer's disease-The way forward. Drugs 1997;53:752-768.
71. Danysz W, Zajaczkowski W, Parsons CG: Modulation of learning processes by ionotropic glutamate receptor ligands. Behav Pharmacol 1995;6:455-474.
72. Li H-B, Matsumoto K, Tohda M, Yamamoto M, Watanabe H: NMDA antagonists potentiate scopolamine-induced amnesic effect. Behav Brain Res 1997;83:225-228.
73. Lanthorn TH: D-Cycloserine: Agonist turned antagonist. Amino Acids 1994;6:247-260.
74. Puumala T, Greijus S, Narinen K, Haapalinna A, Riekkinen P Sr, Sirviö J: Stimulation of alpha-adrenergic receptors facilitates spatial learning in rats. Eur Neuropsychopharmacol 1998;8:17-26.
75. Sirviö J. Ekonsalo T, Riekkinen P Jr, Lahtinen H, Riekkinen PJ: D-Cycloserine, a modulator of the N-methyl-D-aspartate receptor, improves spatial learning in rats treated with muscarinic antagonist. Neurosci Lett 1992;146: 215-218.
76. Pitkänen M, Sirviö J, MacDonald E, Ekonsalo T, Riekkinen P Sr: The effects of D-cycloserine, a partial agonist at the glycine binding site, on spatial learning and memory in scopolaminetreated rats. J Neural Transm 1995;9:133-144.
77. Fishkin RJ, Ince ES, Carlezon WA Jr, Dunn RW: D-Cycloserine attenuates scopolamine-in-duced learning and memory deficits in rats. Behav Neural Biol 1993;59:150-157.
78. Squire LR: Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychol Rev 1992;99:195-231.
79. Riekkinen M, Riekkinen P Jr: Nicotine and D-cycloserine enhance acquisition of water maze spatial navigation in aged rats. Neuroreport 1997;8:699-703.
80. Mohr E, Knott V, Sampson M, Wesnes K, Herting R, Mendis T: Cognitive and quantified electroencephalographic correlates of cycloserine treatment in Alzheimer's disease. Clin Neuropharmacol 1995;18:28-38.
81. Randolph C, Roberts JW, Tierney MC, Bravi D, Mouradian MM, Chase TN: D-Cycloserine treatment of Alzheimer's disease. Alzheimer Dis Assoc Disord 1994;8:198-205.
82. Schwartz BL, Hashtroudi S, Herting RL, Schwartz P, Deutsch SI: D-Cycloscrine enhances implicit memory in Alzheimer patients. Neurology 1996;46:420-424.
83. Quartermain D, Mower J, Rafferty MF, Herting RL, Lanthorn TH: Acute but not chronic activation of the NMDA-coupled glycine receptor with D-cycloserine facilitates learning and retention. Eur J Pharmacol 1994;257:7-12.
84. Ingvar M, Ambros-Ingerson J, Davis M, Granger R, Kessler M, Rogers G, Schehr RS, Lynch G: Enhancement by an ampakine of memory encoding in humans. Exp Neurol 1997;146: 553-559.
85. Granger R, Deadwyler S, Davis M, Moskovitz B, Kessler M, Rogers G, Lynch G: Facilitation of glutamate receptors reverses an age-associated memory impairment in rats. Synapse 1996; 22:332-337.
86. Stäubli U, Perez Y, Xu F, Rogers G, Ingvar M, Stone-Elander S, Lynch G: Centrally active modulators of glutamate receptors facilitate the induction of long-term potentiation in vivo. Proc Natl Acad Sci USA 1994;91:11158-11162.
87. Pitkänen M, Sirviö J, Lahtinen H, Koivisto E, Riekkinen P: D-Cycloserine, a partial agonist at the glycine site, enhances the excitability of dentate granule cells in vivo in rats. Eur J Pharmacol 1994;253:125-129.
88. Sirviö J, Larson JL, Quach CN, Rogers GA, Lynch G: Effects of pharmacologically facilitating glutamatergic transmission in the trisynaptic intrahippocampal circuit. Neuroscience 1996;74:1025-1035.
89. Thiels E, Weisz DJ, Berger TW: In vivo modulation of N-methyl-D-aspartate receptor-dependent long-term potentiation by the glycine modulatory site. Neuroscience 1992;46:501-509.
90. Zivkovic I, Thompson DM, Bertolino M, Uzunov D, Dibella M, Costa E, Guidotti A:7-Chloro-3-methyl-3,4-dihydro-2H-1,2,4-benzothiazine-S,S-dioxide (IDRA 21): A benzothiazine derivative that enhances cognition by attentuating DL-α-amino-2,3-dihydro-5-methyl-3-oxo-4-isoxazolepropanoic acid (AMPA) receptor desensitization. J Pharmacol Exp Ther 1995;272:300-309.
91. Choi DW: Glutamate receptors and the induction of excitotoxic neuronal death; in Bloom FE (ed): Progress in Brain Research. Neuroscience: From the Molecular to the Cognitive. Amsterdam, Elsevier Science, 1994, vol 100, pp 47-51.
92. Tellez S, Colpaert F, Marien M: Acetylcholine release in the rat prefrontal cortex in vivo: Modulation by alpha-2-adrenoceptor agonists and antagonists. J Neurochem 1997;68:778-785.
93. 2-antagonist, can reduce scopolamine-induced hyperactivity in rats. Behav Pharmacol 1997;8:465-470.
94. 2-antagonist, on the performance of rats in a five-choice serial reaction time task. Pharmacol Biochem Behav 1993;45:123-129.
95. 2-noradrenergic system. Drugs Aging 1994;5:116-126.
96. Yavich L, Sirviö J, Heinonen E, Riekkinen P Sr: The interaction of L-deprenyl and scopolamine on spatial learning/memory in rats. J Neural Transm 1993;6:189-197.
97. Sano M, Ernesto C, Thomas RG, Klauber MR, Schafer K, Grundman M, Woodbury P, Growdon J, Cotman CW, Pfeiffer E, Schneider LS, Thal LJ: A controlled trial of selegiline, alphatocopherol, or both as treatment for Alzheimer's disease. N Engl J Med 1997;336:1216-1222.
98. Freedman M, Rewilak D, Xerri T, Cohen S, Gordon AS, Shandling M, Logan AG: L-Deprenyl in Alzheimer's disease. Cognitive and behavioral effects. Neurology 1998;50: 660-668.
99. Costall B, Domency AM, Kelly ME, Naylor RJ: Influence of 5-HT on cognitive performance. Adv Biosci 1992;85:147-164.
100. Morris RGM, Anderson E, Lynch G, Baudry M: Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP-5. Nature 1986;319:774-776.
101. Rogan MT, Stäubli UV, LeDoux JE: Fear conditioning induces associative long-term potentiation in the amygdala. Nature 1997; 390:604-607.
102. Bliss TVP, Collingridge GL: A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 1993;361:31-39.
103. Malenka RC, Nicoll RA: Never fear, LTP is here. Nature 1997;390:552-553.
104. Artola A, Singer W: Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci 1993;16:480-487.
105. Nicoll RA, Malenka RC: Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 1995;377:115-118.
106. Burgard EC, Sarvey JM: Muscarinic receptor activation facilitates the induction of long-term potentiation in the rat dentate gyrus. Neurosci Lett 1990;116:34-39.
107. 2+ channels involved? Neuropharmacology 1995;34:1549-1557.
108. Hsu K-S, Huang C-C, Gean P-W: Muscarinic depression of excitatory synaptic transmission mediated by the presynaptic M3 receptors in the rat neostriatum. Neurosci Lett 1995;197:141-144.
109. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA: Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 1996;383:713-716.
110. Blitzer RD, Gil O, Landau EM: Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci Lett 1990;119:207-210.
111. 1 agonist, facilitates the induction of long-term potentiation in rat hippocampal slices. Eur J Pharmacol 1992;222:21-25.
112. Hasselmo ME, Barkai E: Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation. J Neurosci 1995;15:6592-6604.
113. Iga Y, Arisawa H, Ise M, Yasuda H, Takeshita Y: Modulation of rhythmical slow activity, long-term potentiation and memory by muscarinic receptor agonists. Eur J Pharmacol 1996;308:13-19.
114. Kaneko S, Maeda T, Satoh M: Cognitive enhancers and hippocampal long-term potentiation in vitro. Behav Brain Res 1997;83:45-49.
115. Auerbach JM, Segal M: A novel cholinergic induction of long-term potentiation in rat hippocampus. J Neurophysiol 1994;72:2034-2040.
116. Hunter BE, de Fiebre CM, Papke RL, Kem WR, Meyer EM: A novel nicotinic agonist facilitates induction of long-term potentiation in the rat hippocampus. Neurosci Lett 1994; 168:130-134.
117. Abe K, Nakata A, Mizutani A, Saito H: Facilitatory, but non-essential role of the muscarinic cholinergic system in the generation of long-term potentiation of population spikes in the dentate gyrus in vivo. Neuropharmacology 1994;33:847-852.
118. Bröcher S, Artola A, Singer W: Agonists of cholinergic and noradrenergic receptors facilitate synergistically the induction of long-term potentiation in slices of rat visual cortex. Brain Res 1992;573:27-36.
119. Hirotsu I, Hori N, Katsuda N, Ishihara T: Effect of anticholinergic drug on long-term potentiation in rat hippocampal slices. Brain Res 1989;482:194-197.
120. Ito T, Miura Y, Kadokawa T: Effects of physostigmine and scopolamine on long-term potentiation of hippocampal population spikes in rats. Can J Physiol Pharmacol 1988;66: 1010-1016.
121. Jouvenceau A, Billard JM, Lamour Y, Dutar P: Persistence of CA1 hippocampal LTP after selective cholinergic denervation. Neuroreport 1996;7:948-952.
122. Stringer JL, Greenfield LJ, Hackett JT, Guyenet PG: Blockade of long-term potentiation by phencyclidine and sigma opiates in the hippocampus in vivo and in vitro. Brain Res 1983;28:127-138.
123. Watanabe Y, Ikegaya Y, Saito H, Abe K: Roles of GABA-A, NMDA and muscarinic receptors in induction of long-term potentiation in the medial and lateral amygdala in vitro. Neurosci Res 1995;21:317-322.
124. Larson J, Xiao P, Lynch G: Reversal of LTP by theta frequency stimulation. Brain Res 1993;600:97-102.
125. Huerta PT, Lisman JE: Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron 1995;15:1053-1063.
126. Tanaka Y, Sakurai M, Hayashi S: Effect of scopolamine and HP 029, a cholinesterase inhibitor, on long-term potentiation in hippocampal slices of guinea pig. Neurosci Lett 1989;98:179-183.
127. Ito T, Miura Y, Kadokawa T: Physostigmine induces in rats a phenomenon resembling long-term potentiation. Eur J Pharmacol 1988;156:351-359.