Neuropsychiatric aspects of Alzheimer's disease: The cholinergic hypothesis revisited

Neurology

Volumn 47, Issue 4, 1996, Pages 876-883

  Cummings, Jeffrey L ^a   Kaufer, Daniel ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 ETHYL 8 METHYL 2,8 DIAZASPIRO[4.5]DECANE 1,3 DIONE; ACETYLCHOLINE; ARECOLINE; BETHANECHOL; CHOLINERGIC RECEPTOR STIMULATING AGENT; CHOLINESTERASE INHIBITOR; HALOPERIDOL; PHYSOSTIGMINE; PLACEBO; SCOPOLAMINE; TACRINE;

AGITATION; ALZHEIMER DISEASE; ANIMAL MODEL; CHOLINERGIC SYSTEM; CLINICAL ARTICLE; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DEMENTIA; DEPRESSION; HUMAN; INTRACEREBROVENTRICULAR DRUG ADMINISTRATION; MULTICENTER STUDY; NEUROPSYCHIATRY; NONHUMAN; PERSONALITY DISORDER; PRIORITY JOURNAL; PSYCHOSIS; REVIEW; TREATMENT OUTCOME;

EID: 0029838038     PISSN: 00283878     EISSN: None     Source Type: Journal    
DOI: 10.1212/WNL.47.4.876     Document Type: Review

References (101)

1. Davies P, Maloney AJF. Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 1976;2:1403.
2. Perry EK, Perry RH, Blessed G, Tomlinson BE. Necropsy evidence of central cholinergic deficits in senile dementia. Lancet 1977;1:189.
3. Spillane JA, White P, Goodhardt MJ, et al. Selective vulnerability of neurons in organic dementia. Nature 1977;266: 558-559.
4. White P, Goodhardt MJ, Keet JP, et al. Neocortical cholinergic neurons in elderly people. Lancet 1977;1:668-671.
5. Davies P. Studies on the neurochemistry of central cholinergic systems in Alzheimer's disease. In: Katzman R, Terry RD, Bick KL, eds. Alzheimer's disease: senile dementia and related disorders. New York: Raven Press, 1978:453-459.
6. Whitehouse PJ, Price DL, Clark AW, et al. Alzheimer disease: evidence for selective loss of cholinergic neurons in the nucleus basalis. Ann Neurol 1981;10:122-126.
7. Coyle JT, Price DL, DeLong MR. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science 1983;219: 1184-1190.
8. Goyan RK. Muscarinic receptor subtypes: physiology and clinical implications. N Engl J Med 1989;321:1022-1029.
9. Mash DC, Flynn DD, Potter LT. Loss of M2 muscarinic receptors in the cerebral cortex in Alzheimer's disease and experimental cholinergic denervation. Science 1985;228: 1115-1117.
10. Perry EK, Perry RH, Smith CJ, et al. Cholinergic receptors in cognitive disorders. Can J Neurol Sci 1986;13:521-527.
11. Taylor P, Brown JH. Acetylcholine. In: Siegel GJ, Agranoff BW, Albers RW, Molinoff PB, eds. Basic neurochemistry: molecular, cellular, and medical aspects. 5th ed. New York: Raven Press, 1994:231-281.
12. Perry EK, Perry RH, Smith CJ, et al. Nicotinic receptor abnormalities in Alzheimer's and Parkinson's diseases. J Neurol Neurosurg Psychiatry 1987;50:806-809.
13. Whitehouse PJ, Martino AM, Wagster MV, et al. Reductions in [3H]nicotinic acetylcholine binding in Alzheimer's disease and Parkinson's disease: autoradiographic study. Neurology 1988;38:720-723.
14. Wallace W, Lieburg I, Schenk D, et al. Chronic elevation of soluble amyloid precursor protein and amyloid beta peptide secretion in subcortically lesioned rats. J Neurosci 1995;15: 4896-4905.
15. Bartus RT, Dean RL III, Beer B, Lippa AS. The cholinergic hypothesis of geriatric memory dysfunction. Science 1982; 217:408-417.
16. Collerton D. Cholinergic function and intellectual decline in Alzheimer's disease. Neuroscience 1986;19:1-28.
17. Smith G. Animal models of Alzheimer's disease: experimental cholinergic denervation. Brain Res Rev 1988;13:103-118.
18. Perry EK, Tomlinson BE, Blessed G, et al. Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. BMJ 1978;2:1457-1459.
19. Wilcock GK, Esiri MM, Bowen DM, Smith CCT. Alzheimer's disease. Correlation of cortical cholinergic acetyltransferase activity with the severity of dementia and histopathological abnormalities. J Neurol Sci 1982;57:407-417.
20. Francis PT, Palmer AM, Sims NR, et al. Neurochemical studies of early-onset Alzheimer's disease. N Engl J Med 1985; 313:7-11.
21. Sims NR, Smith CCT, Davison AN, et al. Glucose metabolism and acetylcholine synthesis in relation to neuronal activity in Alzheimer's disease. Lancet 1980;1:333-335.
22. Sunderland T, Tariot PN, Cohen RM, et al. Anticholinergic sensitivity in patients with dementia of the Alzheimer type and age-matched controls. Arch Gen Psychiatry 1987;44: 418-426.
23. Drachman DA. Memory and cognitive function in man: does the cholinergic system have a specific role? Neurology 1977; 27:783-790.
24. Galasko DR, Thai LJ. Cholinomimetic agents. In: Cummings JL, Miller BL, eds. Alzheimer's disease: treatment and long-term management. New York: Marcel Dekker, 1990:23-36.
25. Knapp MJ, Knopman DS, Solomon PR, et al. A 30-week randomized controlled trial of high-dose tacrine in patients with Alzheimer's disease. JAMA 1994;271:985-991.
26. Martinez-Murillo R, Rodrigo J. The localization of cholinergic neurons and markers in the CNS. In: Stone TW, ed. CNS neurotransmitters and neuromodulators: acetylcholine. Boca Raton, FL: CRC Press, 1995:1-37.
27. Nieuwenhuys R. Chemoarchitecture of the brain. New York: Springer-Verlag, 1985.
28. Mesulam M-M, Mufson EJ, Levey AI, Wainer BH. Cholinergic innervation of cortex by the basal forebrain: cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (substantia innominata), and hypothalamus in the rhesus monkey. J Comp Neurol 1983; 214:170-197.
29. Hedreen JC, Struble RG, Whitehouse PJ, Price DL. Topography of the magnocellular basal forebrain system in human brain. J Neuropathol Exp Neurol 1984;43:1-21.
30. Mesulam M-M, Volicer L, Marquis JK, et al. Systematic regional differences in the cholinergic innervation of the primate cerebral cortex: distribution of enzyme activities and some behavioral implications. Ann Neurol 1986;19:144-151.
31. Schliebs R, Robner S. Distribution of muscarinic acetylcholine receptors in the CNS. In: Stone TW, ed. CNS neurotransmitters and neuromodulators: acetylcholine. Boca Raton, FL: CRC Press: 1995:67-83.
32. Mesulam M-M, Mufson EJ. Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. Brain 1984;107:253-274.
33. Pirch JH. Electrophysiological effects of acetylcholine on central neurons (whole cells and interactions). In: Stone TW, ed. CNS neurotransmitters and neuromodulators: acetylcholine. Boca Raton, FL: CRC Press, 1995:115-128.
34. Cummings JL, Victoroff JI. Noncognitive neuropsychiatric syndromes in Alzheimer's disease. Neuropsychiatr Neuropsychol Behav Neurology 1990;3:140-158.
35. Mega M, Cummings JL, Fiorello T, Gornbein J. The spectrum of behavioral changes in Alzheimer's disease. Neurology 1996;46:130-135.
36. Mendez MF, Martin RJ, Smyth KA, et al. Psychiatric symptoms associated with Alzheimer's disease. J Neuropsychiatry Clin Neurosci 1993;2:28-33.
37. Wragg RE, Jeste DV. Overview of depression and psychosis in Alzheimer's disease. Am J Psychiatry 1989;146:577-587.
38. Sunderland T, Tariot PN, Newhouse PA. Differential responsivity of mood, behavior, and cognition to cholinergic agents in elderly neuropsychiatric populations. Brain Res Rev 1988; 13:371-389.
39. Cummings JL, Gorman DG, Shapira J, Physostigmine ameliorates the delusions of Alzheimer's disease. Biol Psychiatry 1993;33:536-541.
40. Perry EK, Kerwin J, Perry RH, et al. Cerebral cholinergic activity is related to the incidence of visual hallucinations in senile dementia of Lewy body type. Dementia 1990;1:2-4.
41. Mentis MJ, Weinstein EA, Horwitz B, et al. Abnormal glucose metabolism in the delusional misidentification syndromes: a positron emission tomography study in Alzheimer's disease. Biol Psychiatry 1995;38:438-449.
42. Starkstein SE, Vazquez S, Petracca G, et al. A SPECT study of delusions in Alzheimer's disease. Neurology 1994;44:2055-2059.
43. Sultzer DL, Mahler ME, Mandelkern MA, et al. Psychiatric symptoms are associated with regional cortical metabolism in Alzheimer's disease. J Neuropsychiatry Clin Neurosci 1995;7:476-484.
44. Cummings JL. Psychosis in neurologic disease. Neurobiology and pathogenesis. Neuropsychiatr Neuropsychol Behav Neurology 1992;5:144-150.
45. Granacher RP, Baldessarini RJ. Physostigmine: its use in acute anticholinergic syndrome with antidepressant and antiparkinson drugs. Arch Gen Psychiatry 1975;32:375-380.
46. Singh MM, Kay SR. Therapeutic antagonism between anticholinergic anti-Parkinsonism agents and neuroleptics in schizophrenia: implications for a neuropharmacological model. Neuropsychobiology 1979;5:74-86.
47. Rosenthal R, Bigelow LB. The effects of physostigmine in phenothiazine resistant chronic schizophrenic patients: preliminary observations. Compr Psychiatry 1973;14:489-494.
48. Karson CN, Casanova MF, Kleinman JE, Griffin WS. Choline acetyltransferase in schizophrenia. Am J Psychiatry 1993;149:454-459.
49. Freedman R, Hall M, Adler LE, Leonard S. Evidence of postmortem brain tissue for decreased numbers of hippocampal nicotinic receptors in schizophrenia. Biol Psychiatry 1995;38: 22-33.
50. Adler LE, Hoffer LJ, Wiser A, Freedman R. Cigarette smoking normalizes auditory physiology in schizophrenia. Am J Psychiatry 1993;150:1856-1861.
51. Klein C, Andersen B. On the influence of smoking upon smooth pursuit eye movements of schizophrenics and normal controls. J Psychophysiology 1991;5:361-369.
52. Janowsky DS, Risch SC, Gillin JC. Adrenergic-cholinergic balance and the treatment of affective disorders. Prog Neuropsychopharmacol Biol Psychiatry 1983;7:297-307.
53. Berger M, Riemann D, Hochli D, Spiegel R. The cholinergic rapid eye movement sleep induction tests with RS-86. Arch Gen Psychiatry 1989;46:421-428.
54. Goggin DA, Solomon GF. Trihexyphenidyl abuse for euphorigenic effect. Am J Psychiatry 1979;136:459-460.
55. Janowsky DS, El-Yousef K, Davis JM, Sekerke HJ. Parasympathetic suppression of manic symptoms by physostigmine. Arch Gen Psychiatry 1973;28:542-547.
56. Risch SC, Cohen RM, Janowsky DS, et al. Physostigmine induction of depressive symptomatology in normal human subjects. Psychiatry Res 1981;4:89-94.
57. Burns A, Jacoby R, Levy R. Psychiatric phenomena in Alzheimer's disease. III. Disorders of mood. Br J Psychiatry 1990;157:81-86.
58. Cummings JL, Miller B, Hill MA, Neshkes R. Neuropsychiatric aspects of multi-infarct dementia and dementia of the Alzheimer type. Arch Neurol 1987;44:389-393.
59. Weiner MF, Edland SD, Luszcynska H. Prevalence and incidence of major depression in Alzheimer's disease. Am J Psychiatry 1994;151:1006-1009.
60. Davis KL, Hollander E, Davidson M, et al. Induction of depression with oxotremorine in patients with Alzheimer's disease. Am J Psychiatry 1987;144:468-471.
61. Whitehouse P. Intraventricular bethanechol in Alzheimer's disease: a continuing controversy. Neurology 1988;38:307-308.
62. Sunderland T, Tariot PN, Newhouse PA. Differential responsivity of mood, behavior, and cognition to cholinergic agents in elderly neuropsychiatric populations. Brain Res Rev 1988; 13:371-389.
63. Newhouse PA, Sunderland T, Tariot PN, et al. Intravenous nicotine in Alzheimer's disease: a pilot study. Psychopharmacology (Berl) 1988;95:171-175.
64. Bliwise DL, Tinklenberg J, Yesavage JA, et al. REM latency in Alzheimer's disease. Biol Psychiatry 1989;25:320-328.
65. Kapen S, Fleming PD, Drachman DA. Cholinergic enhancement and REM sleep latency in the aged: lecithin does not reproduce physostigmine effect. Neurology 1986;36:1079-1083.
66. Gillin JC, Sutton L, Ruiz C, et al. Dose dependent inhibition of REM sleep in normal volunteers by biperiden, a muscarinic antagonist. Biol Psychiatry 1991;30:151-156.
67. Doerr P, Berger M. Physostigmine-induced escape from dexamethasone suppression in normal adults. Biol Psychiatry 1983;18:261-288.
68. Balldin J, Gottfries C-G, Karlsson I, et al. Dexamethasone suppression test and serum prolactin in dementia disorders. Br J Psychiatry 1983;143:277-281.
69. Greenwald BS, Mathe AA, Mohs RC, et al. Cortisol and Alzheimer's disease. II. Dexamethasone suppression, dementia severity, and affective symptoms. Am J Psychiatry 1986;143: 442-446.
70. Kumar V, Smith RC, Sherman KA, et al. Cortisol responses to cholinergic drugs in Alzheimer's disease. Int J Clin Pharmacol Ther Toxicol 1988;26:471-476.
71. Mohs RC, Davis BM, Johns CA, et al. Oral physostigmine treatment of patients with Alzheimer's disease. Am J Psychiatry 1985;142:28-33.
72. Gershon S, McIntyre IM, Pomara N, et al. Alterations in cholinergic receptors mediate the effects of dexamethasone on corticosterone. Biol Psychiatry 1985;20:451-460.
73. Cohen-Mansfield J, Billig N. Agitated behaviors in the elderly. I. A conceptual overview. J Am Geriatr Soc 1986;34: 711-721.
74. Swearer JM, Drachman DA, O'Donnell BF, Mitchell AL. Troublesome and disruptive behaviors in dementia. J Am Geriatr Soc 1988;36:784-790.
75. Colenda CC III. Agitation: a conceptual overview. In: Lawlor BA, ed. Behavioral complications in Alzheimer's disease. Washington, DC: American Psychiatric Press, 1995:3-17.
76. Aarsland D, Cummings JL, Yener G, Miller B. The relationship of aggressive behavior to psychosis and depression in patients with Alzheimer's disease. Am J Psychiatry 1996; 153:243-247.
77. German DG, Read S, Cummings JL. Cholinergic therapy of behavioral disturbances in Alzheimer's disease. Neuropsychiatr Neuropsychol Behav Neurology 1993;6:229-234.
78. Murillo JR, Mendoza DL, Diaz JL. Behavioral effect of scopolamine in cats. Int J Neurosci 1988;4:223-230.
79. Kaufer DI, Cummings JL. Response of behavioral symptoms in Alzheimer's disease to tacrine [abstract], J Neuropsychiatry Clin Neurosci 1995;7:397.
80. Hollander E, Davidson M, Mohs RC, et al. RS 86 in the treatment of Alzheimer's disease: cognitive and biological effects. Biol Psychiatry 1987;22:1067-1078.
81. Penn RD, Martin EM, Wilson RS, et al. Intraventricular bethanechol infusion for Alzheimer's disease: results of double-blind and escalating dose trials. Neurology 1988;38:219-222.
82. Read SL, Frazee J, Shapira J, et al. Intracerebroventricular bethanechol for Alzheimer's disease. Arch Neurol 1990;47: 1025-1030.
83. Rosen WG, Mohs RC, Davis KL. A new rating scale for Alzheimer's disease. Am J Psychiatry 1984;141:1356-1364.
84. Davis KL, Thai LJ, Gamzu ER, et al. A double-blind placebo-controlled multicenter study of tacrine for Alzheimer's disease. N Engl J Med 1992;327:1253-1259.
85. Farlow M, Gracon SI, Hershey LA, et al. A controlled trial of tacrine in Alzheimer's disease. JAMA 1992;268:2523-2529.
86. Maltby N, Broe G, Creasey H, et al. Efficacy of tacrine and lecithin in mild to moderate Alzheimer's disease: double blind trial. BMJ 1994;308:879-883.
87. Gauthier S, Bouchard R, Lamontagne A, et al. Tetrahydroaminoacridine-lecithin combination treatment in patients with intermediate-stage Alzheimer's disease: results of a Canadian double-blind, cross-over, multicenter study. N Engl J Med 1990;322:1272-1276.
88. Kaufer DI, Cummings JL, Christine D. Effect of tacrine on behavior in Alzheimer's disease: an open-label study. J Geriatr Psychiatry Neurol 1996;9:1-6.
89. Sahakian BJ. Cholinergic drugs and human cognitive performance. In: Iversen LL, Iversen DS, Snyder SH, eds. Handbook of psychopharmacology, vol 20. Psychopharmacology of the aging nervous system. New York: Plenum Press, 1988: 393-424.
90. Cummings JL, Benson DF. Dementia: a clinical approach. 2nd ed. Boston: Butterworth-Heinemann, 1992.
91. Roberts GW, Leigh PN, Weinberger DR. Neuropsychiatric disorders. St. Louis: Wolfe, 1993.
92. Procter AW, Lowe SL, Palmer AM, et al. Topographical distribution of neurochemical changes in Alzheimer's disease. J Neurol Sci 1988;84:125-140.
93. Honer W, Prohovnik I, Smith G, Lucas L. Scopolamine reduces frontal cortex perfusion. J Cereb Blood Flow Metab 1988;8:635-641.
94. Hunter R, Wyper DJ, Patterson J, et al. Cerebral pharmacodynamics of physostigmine in Alzheimer's disease investigated using single photon-emission tomography. Br J Psychiatry 1991;158:351-357.
95. Schneider LS, Farlow MR. Predicting response to cholinesterase inhibitors in Alzheimer's disease: possible approaches. CNS Drugs 1995;4:114-124.
96. McCormick DA. Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog Neurobiol 1992;39:337-388.
97. Perry EK, Marshall E, Kerwin J, et al. Evidence of a monoaminergic-cholinergic imbalance related to visual hallucinations in Lewy body dementia. J Neurochem 1990;55:1454-1456.
98. Cummings JL, Benson DF. The role of the nucleus basalis of Meynert in dementia: review and reconsideration. Alzheimer Dis Assoc Disord 1987;1:128-145.
99. Smith DE, King MB, Hoebel BG. Lateral hypothalamic control of killing: evidence of a cholinoceptic mechanism. Science 1970;167:900-901.
100. Bear D, Rosenbaum J, Norman R. Aggression in cat and human precipitated by a cholinesterase inhibitor. Psychosomatics 1986;27:535-536.
101. Devinsky O, Kernan J, Bear DM. Aggressive behavior following exposure to cholinesterase inhibitors. J Neuropsychiatry Clin Neurosci 1992;4:189-194.