The M1 muscarinic agonist CI-1017 facilitates trace eyeblink conditioning in aging rabbits and increases the excitability of CA1 pyramidal neurons

Journal of Neuroscience

Volumn 20, Issue 2, 2000, Pages 783-790

  Weiss, Craig ^a   Preston, Alison R ^a,c   Oh, M Matthew ^a   Schwarz, Roy D ^b   Welty, Devin ^b   Disterhoft, John F ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b PFIZER INC   (United States)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Acetylcholine; Afterhyperpolarization; Alzheimer's disease; Cholinesterase; Hippocampus; Learning

Indexed keywords

1 AZABICYCLO[2.2.1]HEPTAN 3 ONE O [3 (3' METHOXYPHENYL) 2 PROPYNYL]OXIME MALEATE; ATROPINE; MUSCARINIC M1 RECEPTOR AGONIST; PIRENZEPINE; UNCLASSIFIED DRUG;

AFTERHYPERPOLARIZATION; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DOSE RESPONSE; EYELID REFLEX; FEMALE; HIPPOCAMPUS; HYPERSALIVATION; LEARNING; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RABBIT; SPIKE;

EID: 0034651105     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-02-00783.2000     Document Type: Article

References (71)

1. Akase E, Thompson LT, Disterhoft JF (1994) A system for quantitative analysis of associative learning. II. Real-time software for MS-DOS microcomputers. J Neurosci Methods 54:119-130.
2. Bartus RT, Dean RL, Beer B, Lippa S (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408-416.
3. Benardo LS, Prince DA (1981) Acetylcholine induced modulation of hippocampal pyramidal neurons. Brain Res 211:227-234.
4. Benardo LS, Prince DA (1982) Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res 249:315-331.
5. Bonner TI, Buckley NJ, Young AC, Brann MR (1987) Identification of a family of muscarinic acetylcholine receptor genes. Science 237:527-532.
6. Buxbaum JD, Oishi M, Chen HI, Pinkas-Kramarski R, Jaffe EA, Gandy SE, Greengard P (1992) Cholinergic agonists and interleukin 1 regulate processing and secretion of the Alzheimer beta/A4 amyloid protein precursor. Proc Natl Acad Sci USA 89:10075-10078.
7. Bymaster FP, Heath I, Hendrix JC, Shannon HE (1993) Comparative behavioral and neurochemical activities of cholinergic antagonists in rats. J Pharmacol Exp Ther 267:16-24.
8. Caulfield MP, Higgins GA, Straughan DW (1983) Central administration of the muscarinic receptor subtype-selective antagonist pirenzepine selectively impairs passive avoidance learning in the mouse. J Pharm Pharmacol 35:131-132.
9. Cole AE, Nicoll RA (1983) Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science 221:1299-1301.
10. Cole AE, Nicoll RA (1984a) Characterization of a slow cholinergic post-synaptic potential recorded in vitro from rat hippocampal pyramidal cells. J Physiol (Lond) 352:173-188.
11. Cole AE, Nicoll RA (1984b) The pharmacology of cholinergic excitatory responses in hippocampal pyramidal cells, Brain Res 305:283-290.
12. Coulter DA, LoTurco JJ, Kubota M, Disterhoft JF, Moore JW, Alkon DL (1989) Classical conditioning reduces amplitude and duration of calcium-dependent afterhyperpolarization in rabbit hippocampal pyramidal cells. J Neurophysiol 61:971-981.
13. de Jonge MC, Black J, Deyo RA, Disterhoft JF (1990) Learning-induced afterhyperpolarization reductions in hippocampus arc specific for cell type and potassium conductance. Exp Brain Res 80:456-462.
14. Deyo RA, Straube K, Disterhoft JF (1989) Nimodipinc facilitates trace conditioning of the eye-blink response in aging rabbits. Science 243:809-811.
15. Disterhoft JF, Kwan HH, Lo WD (1977) Nictitating membrane conditioning to tone in the immobilized albino rabbit. Brain Res 137:127-143.
16. Disterhoft JF, Coulter DA, Alkon DL (1986) Conditioning-specific membrane changes of rabbit hippocampal neurons measured in vitro. Proc Natl Acad Sci USA 83:2733-2737.
17. Disterhoft JF, Golden DT, Read HL, Coulter DA, Alkon DL (1988) AHP reductions in rabbit hippocampal neurons during conditioning correlate with acquisition of the learned response. Brain Res 462:118-125.
18. Disterhoft JF, Thompson LT, Weiss C, Moyer Jr JR, Van der Zee E, Carrillo MC, Kronforst-Collins M, Power J (1995) The calcium hypothesis for Alzheimer's disease: insights from animal and human studies. Neurosci Res Commun 17:121-131.
19. Disterhoft JF, Carrillo MC, Hopkins RO, Gabrieli JDE, Kesncr RP, (1996a) Impaired trace eyeblink conditioning in severe medial temporal lobe amnesics. Soc Neurosci Abstr 22:1866.
20. Disterhoft JF, Thompson LT, Moyer Jr JR, Mogul DJ (1996b) Calcium-dependent afterhyperpolarization and learning in young and aging hippocampus. Life Sci 59:413-420.
21. Ferrari-DiLeo G, Mash DC, Flynn DD (1995) Attenuation of muscarinic receptor-G-protein interaction in Alzheimer disease. Mol Chem Neuropathol 24:69-91.
22. Fisher A, Heldman E. Gurwitz D, Haring R. Karton Y, Meshulam H, Pittel Z. Marciano D, Brandeis R, Sadot E, Barg Y, Pinkas-Kramarski R, Vogel Z, Ginzburg I, Treves TA, Verchovsky R, Klimowsky S, Korczyn AD (1996) M1 agonists for the treatment of Alzheimer's disease. Novel properties and clinical update. Ann NY Acad Sci 777:189-196.
23. Flynn DD, Ferrari-DiLeo G, Mash DC, Levey AI (1995) Differential regulation of molecular subtypes of muscarinic receptors in Alzheimer's disease. J Neurochem 64:1888-1891.
24. Geula C, Mesulam M-M (1994) Cholinergic systems and related neuropathological predilection patterns in Alzheimer disease. In: Alzheimer disease (Terry RD, Katzman R, and Bick KL, eds). New York: Raven.
25. Hagan JJ, Jansen JH, Broekkamp CL (1987) Blockade of spatial learning by the M1 muscarinic antagonist pirenzepine. Psychopharmacology 93:470-476.
26. Halliwell JV (1990) Physiological mechanisms of cholinergic action in the hippocampus. Prog Brain Res 84:255-272.
27. Harvey JA, Gormezano I, Cool-Hauser VA (1985) Relationship between heterosynaptic reflex facilitation and acquisition of the nictitating membrane response in control and scopolamine-injected rabbits. J Neurosci 5:596-602.
28. Hulme EC, Birdsall NJ, Buckley NJ (1990) Muscarinic receptor subtypes. Ann Rev Pharmacol Toxicol 30:633-673.
29. Hung AY, Haass C, Nitsch RM, Qiu WQ, Citron M, Wurtman RJ, Growdon JH, Selkoe DJ (1993) Activation of protein kinase C inhibits cellular production of the amyloid beta-protein. J Biol Chem 268:22959-22962.
30. Hunter AJ, Roberts FF (1988) The effect of pirenzepine on spatial learning in the Morris water maze. Pharmacol Biochem Behav 30:519-523.
31. 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 (1995) In vitro and in vivo evaluation of the subtype-selective muscarinic agonist PD 151832. Life Sci 56:845-852.
32. Kaneko T, Thompson RF (1997) Disruption of trace conditioning of the nictitating membrane response in rabbits by central cholinergic blockade. Psychopharmacology 131:161-166.
33. Kim JJ, Clark RE, Thompson RF (1995) Hippocampectomy impairs the memory of recently, but not remotely, acquired trace eyeblink conditioned responses. Behav Neurosci 109:195-203.
34. Kowalska M, Disterhoft JF (1994) Relation of nimodipine dose and serum concentration to learning enhancement in aging rabbits. Exp Neurol 127:159-166.
35. Kronforst-Collins MA (1998) Limbic, cortical, and cholinergic systems function in rabbit eyeblink conditioning. PhD thesis, Northwestern University.
36. Kronforst-Collins MA, Moriearty PL, Schmidt B, Disterhoft JF (1997) Metrifonate improves associative learning and retention in aging rabbits. Behav Neurosci 111:1031-1040.
37. 2+-dependent afterhyperpolarizations in hippocampal neurons of aged rats. Science 226:1089-1092.
38. Levey AI (1996) Muscarinic acetylcholine receptor expression in memory circuits: Implications for treatment of Alzheimer disease. Proc Natl Acad Sci USA 93:13541-13546.
39. Madison DV, Nicoll RA (1984) Control of the repetitive discharge of rat CAl pyramidal neurones in vitro. J Physiol (Lond) 354:319-331.
40. Martin GK, Lonsbury-Martin BL, Kimm J (1980) A rabbit preparation for neuro-behavioral auditory research. Hear Res 2:65-78.
41. Mash DC, Flynn DD, Potter LT (1985) Loss of M2 muscarine receptors in the cerebral cortex in Alzheimer's disease and experimental cholinergic denervation. Science 228:1115-1117.
42. McGlinchey-Berroth R, Carrillo MC, Gabrieli JDE, Brawn CM, Disterhoft JF (1997) Impaired trace eyeblink conditioning in bilateral medial temporal lobe amnesia. Behav Neurosci 111:873-882.
43. Messer Jr WS, Hoss W (1987) Selectivity of pirenzepine in the central nervous system. I. Direct autoradiographic comparison of the regional distribution of pirenzepine and carbamylcholine binding sites. Brain Res 407:27-36.
44. Messer Jr WS, Thomas GJ, Hoss W (1987) Selectivity of pirenzepine in the central nervous system. II. Differential effects of pirenzepine and scopolamine on performance of a representational memory task. Brain Res 407:37-45.
45. Messer Jr WS, Bohnett M, Stibbe J (1990) Evidence for a preferential involvement of Ml muscarinic receptors in representational memory. Neurosci Lett 116:184-189.
46. Moyer Jr JR, Deyo RA, Disterhoft JF (1990) Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behav Neurosci 104:243-252.
47. Moyer Jr JR, Thompson LT, Black JP, Disterhoft JF (1992) Nimodipine increases excitability of rabbit CAl pyramidal neurons in an age-and concentration-dependent manner. J Neurophysiol 68:2100-2109.
48. Moyer Jr JR, Thompson LT, Disterhoft JF (1996) Trace eyeblink conditioning increases CA1 excitability in a transient and learning-specific manner. J Neurosci 16:5536-5546.
49. Nitsch RM, Slack BE, Wurtman RJ, Growdon JH (1992) Release of Alzheimer amyloid precursor derivatives stimulated by activation of muscarinic acetylcholine receptors. Science 258:304-307.
50. Oh MM, Power JM, Thompson LT, Moriarty P, Disterhoft JF (1999) Metrifonate increases neuronal excitability in CA1 pyramidal neurons from both young and aging rabbit hippocampus. J Neurosci 19:1814-1823.
51. Ohno M, Yamamoto T, Watanabe S (1994) Blockade of hippocampal M1 muscarinic receptors impairs working memory performance of rats. Brain Res 650:260-266.
52. Pearce BD, Potter LT (1991) Coupling of m1 muscarinic receptors to G protein in Alzheimer disease. Alzheimer Dis Assoc Disord 5:163-172.
53. AHP, by acetylcholine, hut not by glutamate, in hippocampal neurons. Pflügers Arch 431:723-728.
54. Perry EK, Tomlinson BE, Blessed G, Bergmann K, Gibson PH, Perry RH (1978) Correlation of cholincrgic abnormalities with senile plaques and mental test scores in senile dementia. Br Med J 2:1457-1459.
55. Potier B, Rascol O, Jazat F, Lamour Y, Dutar P (1992) Alterations in the properties of hippocampal pyramidal neurons in the aged rat. Neuroscience 48:793-806.
56. Robinson MR, Harrell LE (1997) Cholinergic activity and amyloid precursor protein metabolism. Brain Res Rev 25:50-69.
57. Schwarz RD, Callahan MJ, Davis RE, Jaen JC, Tecle H (1997) Development of M1 subtype selective muscarinic agonists for Alzheimer's disease: translation of in vitro selectivity into in vivo efficacy. Drug Dev Res 40:133-143.
58. Solomon PR, Vander Schaaf ER, Thompson RF, Weisz DJ (1986) Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behav Neurosci 100:729-744.
59. Solomon PR, Levine E, Bein T, Pendlebury WW (1991) Disruption of classical conditioning in patients with Alzheimer's disease. Neurobiol Aging 12:283-287.
60. Solomon PR, Brett M, Groccia-Ellison ME, Oyler C, Tomasi M, Pendlehury WW (1995) Classical conditioning in patients with Alzheimer's disease: a multiday study. Psychol Aging 10:248-254.
61. Symons JP, Davis, RE, Marriott JG (1988) Water maze learning and effects of cholinergic drugs in mouse strains with high and low hippocampal pyramidal cell counts. Life Sci 42:375-383.
62. Tecle H, Barrett SD, Lauffer DJ, Augelii-Szafran C, Brann MR, Callahan MJ, Caprathe BW, Davis RE, Doyle PD, Eubanks D, Lipiniski W, Mirzadegan T, Moos WH, Moreland DW, Nelson CB, Pavia MR, Raby C, Schwarz RD, Spencer CJ, Thomas AJ, Jaen JC (1998) Design and synthesis of mi-selective muscarinic agonists: (R)-(-)-(Z)-1-azabicyclo[2.2.1]heptan-3-one, O-(3-(3′-methoxyphenyl)-2-propynyl) oxime maleate (CI-1017), a functionally m1-sclective muscarinic agonist. J Med Chem 41:2524-2536.
63. Thompson LT, Moyer Jr JR, Akase E, Disterhoft JF (1994) A system for quantitative analysis of associative learning. I. Hardware interfaces with cross-species applications. J Neurosci Methods 54:109-117.
64. Thompson LT, Moyer Jr JR, Disterhoft JF (1996a) Trace eyeblink conditioning in rabbits demonstrates heterogeneity of learning ability both between and within age groups. Neurobiol Aging 17:619-629.
65. Thompson LT, Moyer Jr JR, Disterhoft JF (1996b) Transient changes in excitability of rabbit CA3 neurons with a time course appropriate to support memory consolidation. J Neurophysiol 76:1836-1849.
66. Van der Zee EA, Kronforst-Collins MA, Maizels ET, Hunzicker-Dunn M, Disterhoft JF (1997) gamma Isoform-selective changes in PKC immunoreactivity after trace eyeblink conditioning in the rabbit hippocampus. Hippocampus 7:271-285.
67. Weisz DJ, LoTurco JJ (1988) Reflex facilitation of the nictitating membrane response remains after cercbellar lesions. Behav Neurosci 102:203-209.
68. Whitchouse PJ, Au KS (1986) Cholinergic receptors in aging and Alzheimer's disease. Prog Neuropsychopharmacol Biol Psychiatry 10:665-676.
69. Whitehouse PJ, Struble RG, Clark AW, Price DL (1982) Alzheimer disease: plaques, tangles, and the basal forebrain. Ann Neurol 12:494.
70. Woodruff-Pak DS, Papka M (1996) Alzheimer's disease and eyeblink conditioning: 750 ms trace vs. 400 ms delay paradigm. Neurobiol Aging 17:397-404.
71. Woodruff-Pak DS, Finkbiner RG, Sasse DK (1990) Eyeblink conditioning discriminates Alzheimer's patients from non-demented aged. NeuroReport 1:45-49.