Modulation of cholinergic transmission enhances excitability of hippocampal pyramidal neurons and ameliorates learning impairments in aging animals

Neurobiology of Learning and Memory

Volumn 80, Issue 3, 2003, Pages 223-233

  Disterhoft, John F ^a   Oh, M Matthew ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Accommodation; Acetylcholine; Afterhyperpolarization; Hippocampus; Rabbit

Indexed keywords

3 [3 (3 METHOXYPHENYL) 2 PROPYNYLOXYIMINO] 1 AZABICYCLO[2.2.1]HEPTANE; CHOLINESTERASE INHIBITOR; GALANTAMINE; METRIFONATE; MUSCARINIC AGENT;

AGING; ALZHEIMER DISEASE; BEHAVIOR; BRAIN SLICE; CHOLINERGIC SYSTEM; CONFERENCE PAPER; HIPPOCAMPUS; HUMAN; HYPERPOLARIZATION; LEARNING; LEARNING DISORDER; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; POSTSYNAPTIC INHIBITION; PYRAMIDAL TRACT; RABBIT; REDUCTION; TASK PERFORMANCE;

EID: 0141763649     PISSN: 10747427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nlm.2003.08.004     Document Type: Conference Paper

References (98)

1. Alzheimer A., Stelzmann R.A., Schnitzlein H.N., Murtagh F.R. An English translation of Alzheimer's 1907 paper, "Uber eine eigenartige Erkankung der Hirnrinde" Clinical Anatomy. 8:1995;429-431.
2. Barazangi N., Role L.W. Nicotine-induced enhancement of glutamatergic and GABAergic synaptic transmission in the mouse amygdala. Journal of Neurophysiology. 86:2001;463-474.
3. Bartus R.T. On neurodegenerative diseases, models, and treatment strategies: Lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Experimental Neurology. 163:2000;495-529.
4. Bartus R.T., Dean III R.L., Beer B., Lippa A.S. The cholinergic hypothesis of geriatric memory dysfunction. Science. 217:1982;408-414.
5. Becker R.E., Moriearty P., Unni L. The second generation of cholinesterase inhibitors: Clinical and pharmacological effects. Becker R.E., Giacobini E. Cholinergic basis for Alzheimer therapy. 1991;263-296 Birkhauser, Boston.
6. Benardo L.S., Prince D.A. Acetylcholine induced modulation of hippocampal pyramidal neurons. Brain Research. 211:1981;227-234.
7. Benardo L.S., Prince D.A. Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Research. 249:1982;315-331.
8. Bonner T.I., Buckley N.J., Young A.C., Brann M.R. Identification of a family of muscarinic acetylcholine receptor genes. Science. 237:1987;527-532.
9. Caulfield M.P., Higgins G.A., Straughan D.W. Central administration of the muscarinic receptor subtype-selective antagonist pirenzepine selectively impairs passive avoidance learning in the mouse. Journal of Pharmacy and Pharmacology. 35:1983;131-132.
10. Cole A.E., Nicoll R.A. Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science. 221:1983;1299-1301.
11. Cole A.E., Nicoll R.A. Characterization of a slow cholinergic post-synaptic potential recorded in vitro from rat hippocampal pyramidal cells. Journal of Physiology (Lond). 352:1984;173-188.
12. Cole A.E., Nicoll R.A. The pharmacology of cholinergic excitatory responses in hippocampal pyramidal cells. Brain Research. 305:1984;283-290.
13. Corkin S. What's new with the amnesic patient H.M.? Nature Reviews Neuroscience. 3:2002;153-160.
14. Coulter D.A., Lo Turco J.J., Kubota M., Disterhoft J.F., Moore J.W., Alkon D.L. Classical conditioning reduces amplitude and duration of calcium-dependent after hyperpolarization in rabbit hippocampal pyramidal cells. Journal of Neurophysiology. 61:1989;971-981.
15. Cullen K.M., Halliday G.M., Double K.L., Brooks W.S., Creasey H., Broe G.A. Cell loss in the nucleus basalis is related to regional cortical atrophy in Alzheimer's disease. Neuroscience. 78:1997;641-652.
16. Cummings, J. L., Cyrus, P. A., Bieber, F., Mas, J., Orazem, J., Gulanski, B., & and the Metrifonate Study Group (1998). Metrifonate treatment of the cognitive deficits of Alzheimer's Disease. Neurology, 50, 1214-1221.
17. Dachir S., Schmidt B., Levy A. Effects of metrifonate on radial-arm maze acquisition in middle-aged rats. Brain Research. 777:1997;251-254.
18. Dani J.A. Overview of nicotinic receptors and their roles in the central nervous system. Biological Psychiatry. 49:2001;166-174.
19. de Jonge M.C., Black J., Deyo R.A., Disterhoft J.F. Learning-induced afterhyperpolarization reductions in hippocampus are specific for cell type and potassium conductance. Experimental Brain Research. 80:1990;456-462.
20. Deyo R.A., Straube K.T., Disterhoft J.F. Nimodipine facilitates associative learning in aging rabbits. Science. 243:1989;809-811.
21. Disterhoft J.F., Coulter D.A., Alkon D.L. Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proceedings of the National Academy of Sciences of the United States of America (Washington, DC). 83:1986;2733-2737.
22. Disterhoft J.F., Golden D.T., Read H.L., Coulter D.A., Alkon D.L. AHP reductions in rabbit hippocampal neurons during conditioning correlate with acquisition of the learned response. Brain Research. 462:1988;118-125.
23. Everitt B.J., Robbins T.W. Central cholinergic systems and cognition. Annual Review of Psychology. 48:1997;649-684.
24. Ferrari-DiLeo G., Mash D.C., Flynn D.D. Attenuation of muscarinic receptor-G-protein interaction in Alzheimer disease. Molecular and Chemical Neuropathology. 24:1995;69-91.
25. Flynn D.D., Ferrari-DiLeo G., Mash D.C., Levey A.I. Differential regulation of molecular subtypes of muscarinic receptors in Alzheimer's disease. Journal of Neurochemistry. 64:1995;1888-1891.
26. Fulton B., Benfield P. Galanthamine. Drugs Aging. 9:1996;60-65.
27. Gabrieli J.D., McGlinchey-Berroth R., Carrillo M.C., Gluck M.A., Cermak L.S., Disterhoft J.F. Intact delay-eyeblink classical conditioning in amnesia. Behavioral Neuroscience. 109:1995;819-827.
28. Gray R., Rajan A.S., Radcliffe K.A., Yakehiro M., Dani J.A. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature. 383:1996;713-716.
29. Hagan J.J., Jansen J.H., Broekkamp C.L. Blockade of spatial learning by the M1 muscarinic antagonist pirenzepine. Psychopharmacology. 93:1987;470-476.
30. Harvey J.A., Gormezano I., Cool-Hauser V.A. Effects of scopolamine and methylscopolamine on classical conditioning of the rabbit nictitating membrane response. The Journal of Pharmacology and Experimental Therapeutics. 225:1983;42-49.
31. Hunter A.J., Roberts F.F. The effect of pirenzepine on spatial learning in the Morris water maze. Pharmacology, Biochemistry and Behavior. 30:1988;519-523.
32. Iliev A., Traykov V., Prodanov D., Mantchev G., Yakimova K., Krushkov I., Boyadjieva N. Effect of the acetylcholinesterase inhibitor galanthamine on learning and memory in prolonged alcohol intake rat model of acetylcholine deficit. Methods and Findings in Experimental and Clinical Pharmacology. 21:1999;297-301.
33. Iliev A.I., Traykov V.B., Mantchev G.T., Stoykov I., Prodanov D., Yakimova K.S., Krushkov I.M. A post-ischaemic single administration of galanthamine, a cholinesterase inhibitor, improves learning ability in rats. Journal of Pharmacy and Pharmacology. 52:2000;1151-1156.
34. Itoh A., Nitta A., Katono Y., Usui M., Naruhashi K., Iida R., Hasegawa T., Nabeshima T. Effects of metrifonate on memory impairment and cholinergic dysfunction in rats. European Journal of Pharmacology. 322:1997;11-19.
35. Jaen J., Barrett S., Brann M., Callahan M., Davis R., Doyle P., Eubanks D., Lauffer D., Lauffer L., Lipinski W., Moreland D., Nelson C., Raby C., Schwarz R., Spencer C., Tecle H. In Vitro and in vivo evaluation of the subtype-selective muscarinic agonist PD 151832. Life Sciences. 56:1995;845-852.
36. Kaneko T., Thompson R.F. Disruption of trace conditioning of the nictitating membrane response in rabbits by central cholinergic blockade. Psychopharmacology. 131:1997;161-166.
37. Kim J.J., Clark R.E., Thompson R.F. Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behavioral Neuroscience. 109:1995;195-203.
38. Knuttinen M.G., Gamelli A.E., Weiss C., Power J.M., Disterhoft J.F. Age-related effects on eyeblink conditioning in the F344 x BN F1 hybrid rat. Neurobiology of Aging. 22:2001;1-8.
39. Knuttinen M.G., Power J.M., Preston A.R., Disterhoft J.F. Awareness in classical differential eyeblink conditioning in young and aging humans. Behavioral Neuroscience. 115:2001;747-757.
40. Kronforst-Collins M.A., Moriearty P.L., Ralph M., Becker R.E., Schmidt B., Thompson L.T., Disterhoft J.F. Metrifonate treatment enhances acquisition of eyeblink conditioning in aging rabbits. Pharmacology, Biochemistry and Behavior. 56:1997;103-110.
41. Kronforst-Collins M.A., Moriearty P.L., Schmidt B., Disterhoft J.F. Metrifonate improves associative learning and retention in aging rabbits. Behavioral Neuroscience. 111:1997;1031-1040.
42. Kumar A., Foster T.C. 17beta-estradiol benzoate decreases the AHP amplitude in CA1 pyramidal neurons. Journal of Neurophysiology. 88:2002;621-626.
43. 2+-dependent afterhyperpolarizations in hippocampal neurons of aged rats. Science. 226:1984;1089-1092.
44. Lena C., de Kerchove d'Exaerde A., Cordero-Erausquin M., LeNovere N., del Mar Arroyo-Jimenez M., Changeux J.P. Diversity and distribution of nicotinic acetylcholine receptors in the locus ceruleus neurons. Proceedings of the National Academy of Sciences USA. 96:1999;12126-12131.
45. Levey A.I. Muscarinic acetylcholine receptor expression in memory circuits: Implications for treatment of Alzheimer disease. Proceedings of the National Academy of Sciences USA. 93:1996;13541-13546.
46. Maelicke A., Samochocki M., Jostock R., Fehrenbacher A., Ludwig J., Albuquerque E.X., Zerlin M. Allosteric sensitization of nicotinic receptors by galantamine, a new treatment strategy for Alzheimer's disease. Biological Psychiatry. 49:2001;279-288.
47. Madison D.V., Nicoll R.A. Control of the repetitive discharge of rat CA1 pyramidal neurones in vitro. Journal of Physiology (London). 354:1984;319-331.
48. Mash D.C., Flynn D.D., Potter L.T. Loss of M2 muscarine receptors in the cerebral cortex in Alzheimer's disease and experimental cholinergic denervation. Science. 228:1985;1115-1117.
49. McGaughy J., Everitt B.J., Robbins T.W., Sarter M. The role of cortical cholinergic afferent projections in cognition: Impact of new selective immunotoxins. Behavioural Brain Research. 115:2000;251-263.
50. McGlinchey-Berroth R., Carrillo M.C., Gabrieli J.D., Brawn C.M., Disterhoft J.F. Impaired trace eyeblink conditioning in bilateral, medial-temporal lobe amnesia. Behavioral Neuroscience. 111:1997;873-882.
51. Messer W.S. Jr., Thomas G.J., Hoss W. Selectivity of pirenzepine in the central nervous system. II. Differential effects of pirenzepine and scopolamine on performance of a representational memory task. Brain Research. 407:1987;37-45.
52. Messer W.S. Jr., Bohnett M., Stibbe J. Evidence for a preferential involvement of M1 muscarinic receptors in representational memory. Neuroscience Letters. 116:1990;184-189.
53. Morris J., Cyrus P.A., Orazem J., Mas J., Bieber F., Ruzicka B.B., Gulanski B. Metrifonate benefits cognitive, behavioral, and global function in patients with Alzheimer's disease. Neurology. 50:1998;1222-1230.
54. Moyer J.R. Jr., Deyo R.A., Disterhoft J.F. Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behavioral Neuroscience. 104:1990;243-252.
55. Moyer J.R. Jr., Thompson L.T., Black J.P., Disterhoft J.F. Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age- and concentration-dependent manner. Journal of Neurophysiology. 68:1992;2100-2109.
56. Moyer J.R. Jr., Power J.M., Thompson L.T., Disterhoft J.F. Increased excitability of aged rabbit CA1 neurons after trace eyeblink conditioning. The Journal of Neuroscience. 20:2000;5476-5482.
57. Moyer J.R. Jr., Thompson L.T., Disterhoft J.F. Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. The Journal of Neuroscience. 16:1996;5536-5546.
58. Muir J.L. Acetylcholine, aging, and Alzheimer's disease. Pharmacology, Biochemistry and Behavior. 56:1997;687-696.
59. Nordgren I., Bergstrom M., Holmstedt B., Sandoz M. Transformation and action of metrifonate. Archives of Toxicology. 41:1978;31-41.
60. Oh M.M., Power J.M., Thompson L.T., Moriearty P.L., Disterhoft J.F. Metrifonate increases neuronal excitability in CA1 pyramidal neurons from both young and aging rabbit hippocampus. The Journal of Neuroscience. 19:1999;1814-1823.
61. Oh M.M., Wu W.W., Vogel R.W., Woodruff-Pak D.S., Disterhoft J.F. Galanthamine enhances CA1 neuronal excitability & facilitates learning in young & aging rabbits. Society for Neuroscience Abstracts. 26:2000;2014.
62. Ohno M., Yamamoto T., Watanabe S. Blockade of hippocampal M1 muscarinic receptors impairs working memory performance of rats. Brain Research. 650:1994;260-266.
63. Pearce B.D., Potter L.T. Coupling of m1 muscarinic receptors to G protein in Alzheimer disease. Alzheimer Disease and Associated Disorders. 5:1991;163-172.
64. AHP, by acetylcholine, but not by glutamate, in hippocampal neurons. Pflugers Archives of European Journal of Physiology (Berlin). 431:1996;723-728.
65. Pereira E.F., Alkondon M., Reinhardt S., Maelicke A., Peng X., Lindstrom J., Whiting P., Albuquerque E.X. Physostigmine and galanthamine: Probes for a novel binding site on the. α 4 β 2 subtype of neuronal nicotinic acetylcholine receptors stably expressed in fibroblast cells Journal of Pharmacology and Experimental Therapeutics. 270:1994;768-778.
66. Pettigrew L.C., Bieber F., Lettier J., Wermeling D.P., Schmitt F.A., Tikhtman A.J., Ashford J.W., Smith C.D., Wekstein D.R., Markesbery W.R., Orazem J., Ruzicka B.B., Mas J., Gulanski B. A study of the pharmacokinetics, pharmacodynamics and safety of metrifonate in Alzheimer's Disease patients. Journal of Clinical Pharmacology. 38:1998;236-245.
67. AHP in CA1 pyramidal neurons in vitro. Journal of Neurophysiology. 85:2001;319-322.
68. Power J.M., Wu W.W., Sametsky E., Oh M.M., Disterhoft J.F. Age-related enhancement of the slow outward calcium-activated potassium current in hippocampal CA1 pyramidal neurons in vitro. The Journal of Neuroscience. 22:2002;7234-7243.
69. Raskind M.A., Peskind E.R., Wessel T., Yuan W. Galantamine in AD: A 6-month randomized, placebo-controlled trial with a 6-month extension. The Galantamine USA-1 Study Group. Neurology. 54:2000;2261-2268.
70. Riekkinen M., Schmidt B., Kuitunen J., Riekkinen P. Jr. Subchronic treatment increases the duration of the cognitive enhancement induced by metrifonate. European Journal of Pharmacology. 338:1997;105-110.
71. Riekkinen P. Jr., Schmidt B., Stefanski R., Kuitunen J., Riekkinen M. Metrifonate improves spatial navigation and avoidance behavior in scopolamine-treated, medial septum-lesioned and aged rats. European Journal of Pharmacology. 309:1996;121-130.
72. Schmidt B.H., Hinz V.C., van der Staay F.J. The preclinical pharmacology of metrifonate, a long-acting and well tolerated cholinesterase inhibitor for Alzheimer therapy. Fisher A., Yoshida M., Hanin I. Progress in Alzheimer's and Parkinson's Diseases. 1998;579-586 Plemum Press, New York.
73. Schwarz R.D., Callahan M.J., Davis R.E., Jaen J.C., Tecle H. Development of M1 subtype selective muscarinic agonists for Alzheimer's disease: Translation of in vitro selectivity into in vivo efficacy. Drug Development Research. 40:1997;133-143.
74. Scoville W.B., Milner B. Loss of recent memory after bilateral hippocampal lesions. The Journal of Neurology, Neurosurgery and Psychiatry. 20:1957;11-21.
75. Solomon P.R., Groccia-Ellison M.E. Classic conditioning in aged rabbits: Delay, trace, and long-delay conditioning. Behavioral Neuroscience. 110:1996;427-435.
76. Solomon P.R., Groccia-Ellison M.E., Flynn D., Mirak J., Edwards K.R., Dunehew A., Stanton M.E. Disruption of human eyeblink conditioning after central cholinergic blockade with scopolamine. Behavioral Neuroscience. 107:1993;271-279.
77. Solomon P.R., Solomon S.D., Schaaf E.V., Perry H.E. Altered activity in the hippocampus is more detrimental to classical conditioning than removing the structure. Science. 220:1983;329-331.
78. Solomon P.R., Vander Schaaf E.R., Thompson R.F., Weisz D.J. Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behavioral Neuroscience. 100:1986;729-744.
79. Squire L.R., Zola M.Z. Structure and function of declarative and nondeclarative memory systems. Proceedings of the National Academy of Sciences USA. 93:1996;13515-13522.
80. Sweeney J.E., Bachman E.S., Coyle J.T. Effects of different doses of galanthamine, a long-acting acetylcholinesterase inhibitor, on memory in mice. Psychopharmacology. 102:1990;191-200.
81. Sweeney J.E., Hohmann C.F., Moran T.H., Coyle J.T. A long-acting cholinesterase inhibitor reverses spatial memory deficits in mice. Pharmacology, Biochemistry and Behavior. 31:1988;141-147.
82. Symons J.P., Davis R.E., Marriott J.G. Water maze learning and effects of cholinergic drugs in mouse strains with high and low hippocampal pyramidal cell counts. Life Science. 42:1988;375-383.
83. Tariot P.N., Solomon P.R., Morris J.C., Kershaw P., Lilienfeld S., Ding C. A 5-month, randomized, placebo-controlled trial of galantamine in AD. The Galantamine USA-10 Study Group. Neurology. 54:2000;2269-2276.
84. Taylor L., Griffith W.H. Age-related decline in cholinergic synaptic transmission in hippocampus. Neurobiology of Aging. 14:1993;509-515.
85. ′ -methoxyphenyl)-2-propynyl) oxime maleate (CI-1017), a functionally m1-selective muscarinic agonist Journal of Medicinal Chemistry. 41:1998;2524-2536.
86. Thompson L.T., Moyer J.R. Jr., Disterhoft J.F. Trace eyeblink conditioning in rabbits demonstrates heterogeneity of learning ability both between and within age groups. Neurobiology of Aging. 17:1996;619-629.
87. Thompson L.T., Moyer J.R. Jr., Disterhoft J.F. Transient changes in excitability of rabbit CA3 neurons with a time course appropriate to support memory consolidation. Journal of Neurophysiology. 76:1996;1836-1849.
88. van der Staay F.J., Hinz V.C., Schmidt B.H. Effects of metrifonate on escape and avoidance learning in young and aged rats. Behavioural Pharmacology. 7:1996;56-64.
89. Weible, A. P., Weiss, C. & Disterhoft, J. F. (2003). Galanthamine facilitates acquisition of trace eyeblink conditioning in aged rabbits. Program No. 626.5. 2003 Abstract Viewer/Itinerary Planner. Washington D.C. Society for Neuroscience Abstracts, Online.
90. Weiss C., Thompson R.F. Delayed acquisition of eyeblink conditioning in aged F1 hybrid (Fischer-344 x Brown Norway) rats. Neurobiology of Aging. 13:1992;319-323.
91. Weiss C., Bouwmeester H., Power J.M., Disterhoft J.F. Hippocampal lesions prevent trace eyeblink conditioning in the freely moving rat. Behavioural Brain Research. 99:1999;123-132.
92. Weiss C., Preston A.R., Oh M.M., Schwarz R.D., Welty D., Disterhoft J.F. The M1 muscarinic agonist CI-1017 facilitates trace eyeblink conditioning in aging rabbits and increases the excitability of CA1 pyramidal neurons. The Journal of Neuroscience. 20:2000;783-790.
93. Whitehouse P.J., Price D.L., Clark A.W., Coyle J.T., DeLong M.R. Alzheimer disease: Evidence for selective loss of cholinergic neurons in the nucleus basalis. Annals of Neurology. 10:1981;122-126.
94. Whitehouse P.J., Price D.L., Struble R.G., Clark A.W., Coyle J.T., Delon M.R. Alzheimer's disease and senile dementia: Loss of neurons in the basal forebrain. Science. 215:1982;1237-1239.
95. Wonnacott S. Presynaptic nicotinic ACh receptors. Trends in Neuroscience. 20:1997;92-98.
96. Woodruff-Pak D.S., Thompson R.F. Classical conditioning of the eyeblink response in the delay paradigm in adults aged 18-83 years. Psychology and Aging. 3:1988;219-229.
97. Woodruff-Pak D.S., Vogel R.W., Wenk G.L. Galantamine: Effect on nicotinic receptor binding, acetylcholinesterase inhibition, and learning. Proceedings of the National Academy of Sciences USA. 98:2001;2089-2094.
98. Zola-Morgan S., Squire L.R., Amaral D.G. Human amnesia and the medial temporal region: Enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. The Journal of Neuroscience. 6:1986;2950-2967.