Cholinergic system function and cognition in mild cognitive impairment

Neurobiology of Aging

Volumn 33, Issue 5, 2012, Pages 867-877

  Haense, Cathleen ^a,b   Kalbe, Elke ^c,d   Herholz, Karl ^b,d   Hohmann, Christoph ^a   Neumaier, Bernd ^a   Krais, Roman ^a   Heiss, Wolf Dieter ^a  

^a MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF VECHTA   (Germany)

^d UNIVERSITY OF COLOGNE   (Germany)

Author keywords

11C MP4A; Acetylcholine esterase; Cholinergic system; Kinetic modeling; Memory; Mild cognitive impairment; Neuropsychological function; PET; Principal component analysis

Indexed keywords

ACETYLCHOLINESTERASE; N METHYL 4 PIPERIDYL ACETATE C 11; TRACER; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CHOLINERGIC SYSTEM; CLINICAL ARTICLE; COGNITION; COMPREHENSION; CONTROLLED STUDY; ENZYME ACTIVITY; EXECUTIVE FUNCTION; FEMALE; HUMAN; MALE; MEMORY; MENTAL PERFORMANCE; MILD COGNITIVE IMPAIRMENT; NEUROIMAGING; NEUROPSYCHOLOGICAL TEST; NONVERBAL MEMORY; POSITRON EMISSION TOMOGRAPHY; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; TEMPORAL LOBE; VERBAL MEMORY; VISUOSPATIAL FUNCTION;

ACETYLCHOLINESTERASE; AGED; AMYGDALA; CEREBRAL CORTEX; CHOLINERGIC NEURONS; COGNITION; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MIDDLE AGED; MILD COGNITIVE IMPAIRMENT; NEUROPSYCHOLOGICAL TESTS;

EID: 84858342780     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2010.08.015     Document Type: Article

References (77)

1. Arendt T., Bigl V., Tennstedt A., Arendt A. Neuronal loss in different parts of the nucleus basalis is related to neuritic plaque formation in cortical target areas in Alzheimer's disease. Neuroscience 1985, 14:1-14.
2. Arendt T., Taubert G., Bigl V., Arendt A. Amyloid deposition in the nucleus basalis of Meynert complex: a topographic marker for degenerating cell clusters in Alzheimer's disease. Acta Neuropathol 1988, 75:226-232.
3. Bartus R.T. On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp. Neurol 2000, 163:495-529.
4. Binder J.R., Frost J.A., Hammeke T.A., Bellgowan P.S., Springer J.A., Kaufman J.N., Possing E.T. Human temporal lobe activation by speech and nonspeech sounds. Cereb. Cortex 2000, 10:512-528.
5. Birks J. Cholinesterase inhibitors for Alzheimer's disease. Cochrane Database Syst Rev 2006, CD005593.
6. Bohnen N.I., Kaufer D.I., Hendrickson R., Ivanco L.S., Lopresti B., Davis J.G., Constantine G., Mathis C.A., Moore R.Y., DeKosky S.T. Cognitive correlates of alterations in acetylcholinesterase in Alzheimer's disease. Neurosci. Lett 2005, 380:127-132.
7. Bohnen N.I., Kaufer D.I., Hendrickson R., Ivanco L.S., Lopresti B.J., Koeppe R.A., Meltzer C.C., Constantine G., Davis J.G., Mathis C.A., Dekosky S.T., Moore R.Y. Degree of inhibition of cortical acetylcholinesterase activity and cognitive effects by donepezil treatment in Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 2005, 76:315-319.
8. Braak H., Braak E. Neuropathological staging of Alzheimer-related changes. Acta Neuropathol. 1991, 82:239-259.
9. Buccafusco J.J., Terry A.V. Multiple central nervous system targets for eliciting beneficial effects on memory and cognition. J. Pharmacol. Exp. Ther 2000, 295:438-446.
10. Chen K.S., Nishimura M.C., Armanini M.P., Crowley C., Spencer S.D., Phillips H.S. Disruption of a single allele of the nerve growth factor gene results in atrophy of basal forebrain cholinergic neurons and memory deficits. J. Neurosci 1997, 17:7288-7296.
11. Coyle J.T., Price D.L., DeLong M.R. Alzheimer's disease: a disorder of cortical cholinergic innervation. Science 1983, 219:1184-1190.
12. Damasio A.R., Graff-Radford N.R., Eslinger P.J., Damasio H., Kassell N. Amnesia following basal forebrain lesions. Arch. Neurol 1985, 42:263-271.
13. Davies P., Maloney A.J. Selective loss of central cholinergic neurons in Alzheimer's disease. Lancet 1976, 2:1403.
14. Davis K.L., Mohs R.C., Marin D., Purohit D.P., Perl D.P., Lantz M., Austin G., Haroutunian V. Cholinergic markers in elderly patients with early signs of Alzheimer disease. JAMA 1999, 281:1401-1406.
15. Davis K.L., Mohs R.C., Tinklenberg J.R., Pfefferbaum A., Hollister L.E., Kopell B.S. Physostigmine: improvement of long-term memory processes in normal humans. Science 1978, 201:272-274.
16. De Santi S., de Leon M.J., Rusinek H., Convit A., Tarshish C.Y., Roche A., Tsui W.H., Kandil E., Boppana M., Daisley K., Wang G.J., Schlyer D., Fowler J. Hippocampal formation glucose metabolism and volume losses in MCI and AD. Neurobiol. Aging 2001, 22:529-539.
17. Decker M.W., McGaugh J.L. The role of interactions between the cholinergic system and other neuromodulatory systems in learning and memory. Synapse 1991, 7:151-168.
18. DeKosky S.T., Ikonomovic M.D., Styren S.D., Beckett L., Wisniewski S., Bennett D.A., Cochran E.J., Kordower J.H., Mufson E.J. Upregulation of choline acetyltransferase activity in hippocampus and frontal cortex of elderly subjects with mild cognitive impairment. Ann. Neurol 2002, 51:145-155.
19. Delis D.C., Kramer J.H., Kaplan E., Ober B.A. California Verbal Learning Test: Adult Version Manual 1987, The Psychological Corporation, San Antonio.
20. Eggers C., Herholz K., Kalbe E., Heiss W.D. Cortical acetylcholine esterase activity and ApoE4-genotype in Alzheimer disease. Neurosci. Lett 2006, 408:46-50.
21. Emre M., Heckers S., Mash D.C., Geula C., Mesulam M.M. Cholinergic innervation of the amygdaloid complex in the human brain and its alterations in old age and Alzheimer's disease. J. Comp. Neurol. 1993, 336:117-134.
22. Etienne P., Robitaille Y., Wood P., Gauthier S., Nair N.P., Quirion R. Nucleus basalis neuronal loss, neuritic plaques and choline acetyltransferase activity in advanced Alzheimer's disease. Neuroscience 1986, 19:1279-1291.
23. Eustache F., Desgranges B., Giffard B., de la Sayette V., Baron J.C. Entorhinal cortex disruption causes memory deficit in early Alzheimer's disease as shown by PET. Neuroreport 2001, 12:683-685.
24. Feldman H.H., Ferris S., Winblad B., Sfikas N., Mancione L., He Y., Tekin S., Burns A., Cummings J., del Ser T., Inzitari D., Orgogozo J.M., Sauer H., Scheltens P., Scarpini E., Herrmann N., Farlow M., Potkin S., Charles H.C., Fox N.C., Lane R. Effect of rivastigmine on delay to diagnosis of Alzheimer's disease from mild cognitive impairment: the InDDEx study. Lancet Neurol 2007, 6:501-512.
25. Folstein M.F., Folstein S.E., McHugh P.R. "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res 1975, 12:189-198.
26. Fujita I. The inferior temporal cortex: architecture, computation, and representation. J. Neurocytol 2002, 31:359-371.
27. Garcia-Alloza M., Gil-Bea F.J., Diez-Ariza M., Chen C.P., Francis P.T., Lasheras B., Ramirez M.J. Cholinergic-serotonergic imbalance contributes to cognitive and behavioral symptoms in Alzheimer's disease. Neuropsychologia 2005, 43:442-449.
28. Gertz H.J., Cervos-Navarro J., Ewald V. The septo-hippocampal pathway in patients suffering from senile dementia of Alzheimer's type. Evidence for neuronal plasticity?. Neurosci. Lett 1987, 76:228-232.
29. Geula C., Mesulam M. Cholinergic systems in Alzheimer disease. Alzheimer Disease 1999, Lippincott Williams & Wilkins, Philadelphia. R.D. Terry, R. Katzman, K.L. Bick, S.S. Sisodia (Eds.).
30. Geula C., Mesulam M.M. Systematic regional variations in the loss of cortical cholinergic fibers in Alzheimer's disease. Cereb. Cortex 1996, 6:165-177.
31. Gilmor M.L., Erickson J.D., Varoqui H., Hersh L.B., Bennett D.A., Cochran E.J., Mufson E.J., Levey A.I. Preservation of nucleus basalis neurons containing choline acetyltransferase and the vesicular acetylcholine transporter in the elderly with mild cognitive impairment and early Alzheimer's disease. J. Comp. Neurol 1999, 411:693-704.
32. Härting C., Markowitsch H.J., Neufeld H., Calabrese P., Deisinger K., Kessler J. Wechsler Gedächtnistest - Revidierte Fassung (WMS-R), Testmanual, Deutsche Adaptation der revidierten Fassung der Wechsler Memory Scale von David Wechsler 2000, Hans Huber, Bern.
33. Herholz K. Acetylcholine esterase activity in mild cognitive impairment and Alzheimer's disease. Eur. J. Nucl. Med. Mol. Imaging 2008, 35(suppl 1):S25-S29.
34. Herholz K., Bauer B., Wienhard K., Kracht L., Mielke R., Lenz M.O., Strotmann T., Heiss W.D. In-vivo measurements of regional acetylcholine esterase activity in degenerative dementia: comparison with blood flow and glucose metabolism. J. Neural Transm 2000, 107:1457-1468.
35. Herholz K., Lercher M., Wienhard K., Bauer B., Lenz O., Heiss W.D. PET measurement of cerebral acetylcholine esterase activity without blood sampling. Eur. J. Nucl. Med 2001, 28:472-477.
36. Herholz K., Weisenbach S., Kalbe E., Diederich N.J., Heiss W.D. Cerebral acetylcholine esterase activity in mild cognitive impairment. Neuroreport 2005, 16:1431-1434.
37. Herholz K., Weisenbach S., Zundorf G., Lenz O., Schroder H., Bauer B., Kalbe E., Heiss W.D. In vivo study of acetylcholine esterase in basal forebrain, amygdala, and cortex in mild to moderate Alzheimer disease. Neuroimage 2004, 21:136-143.
38. Huber W., Poeck K., Weniger D., Willmes K. Der Aachener Aphasie Test. Hogrefe, Göttingen 1983.
39. Hughes C.P., Berg L., Danziger W.L., Coben L.A., Martin R.L. A new clinical scale for the staging of dementia. Br. J. Psychiatry 1982, 140:566-572.
40. Iyo M., Namba H., Fukushi K., Shinotoh H., Nagatsuka S., Suhara T., Sudo Y., Suzuki K., Irie T. Measurement of acetylcholinesterase by positron emission tomography in the brains of healthy controls and patients with Alzheimer's disease. Lancet 1997, 349:1805-1809.
41. Kadir A., Almkvist O., Wall A., Langstrom B., Nordberg A. PET imaging of cortical 11C-nicotine binding correlates with the cognitive function of attention in Alzheimer's disease. Psychopharmacology 2006, 188:509-520.
42. Kemppainen N., Ruottinen H., Nagren K., Rinne J.O. PET shows that striatal dopamine D1 and D2 receptors are differentially affected in AD. Neurology 2000, 55:205-209.
43. Klunk W.E., Engler H., Nordberg A., Wang Y., Blomqvist G., Holt D.P., Bergstrom M., Savitcheva I., Huang G.F., Estrada S., Ausen B., Debnath M.L., Barletta J., Price J.C., Sandell J., Lopresti B.J., Wall A., Koivisto P., Antoni G., Mathis C.A., Langstrom B. Imaging brain amyloid in Alzheimer's disease with Pittsburgh Compound B. Ann. Neurol 2004, 55:306-319.
44. Kuhl D.E., Koeppe R.A., Minoshima S., Snyder S.E., Ficaro E.P., Foster N.L., Frey K.A., Kilbourn M.R. In vivo mapping of cerebral acetylcholinesterase activity in aging and Alzheimer's disease. Neurology 1999, 52:691-699.
45. Loy C., Schneider L. Galantamine for Alzheimer's disease and mild cognitive impairment. Cochrane Database Syst. Rev 2006, CD001747.
46. Marien M.R., Colpaert F.C., Rosenquist A.C. Noradrenergic mechanisms in neurodegenerative diseases: a theory. Brain Res. Brain Res. Rev 2004, 45:38-78.
47. Markiewicz P.J., Matthews J.C., Declerck J., Herholz K. Robustness of multivariate image analysis assessed by resampling techniques and applied to FDG-PET scans of patients with Alzheimer's disease. Neuroimage 2009, 46:472-485.
48. Mesulam M.M. The cholinergic innervation of the human cerebral cortex. Prog. Brain Res 2004, 145:67-78.
49. Mesulam M.M., Geula C. Nucleus basalis (Ch4) and cortical cholinergic innervation in the human brain: observations based on the distribution of acetylcholinesterase and choline acetyltransferase. J Comp. Neurol 1988, 275:216-240.
50. Mitsis E.M., Cosgrove K.P., Staley J.K., Bois F., Frohlich E.B., Tamagnan G.D., Estok K.M., Seibyl J.P., van Dyck C.H. Age-related decline in nicotinic receptor availability with [(123)I]5-IA-85380 SPECT. Neurobiol. Aging 2009, 30:1490-1497.
51. Mitsis E.M., Reech K.M., Bois F., Tamagnan G.D., Macavoy M.G., Seibyl J.P., Staley J.K., van Dyck C.H. 123I-5-IA-85380 SPECT imaging of nicotinic receptors in Alzheimer disease and mild cognitive impairment. J. Nucl. Med 2009, 50:1455-1463.
52. Mufson E.J., Bothwell M., Kordower J.H. Loss of nerve growth factor receptor-containing neurons in Alzheimer's disease: a quantitative analysis across subregions of the basal forebrain. Exp. Neurol 1989, 105:221-232.
53. Namba H., Iyo M., Fukushi K., Shinotoh H., Nagatsuka S., Suhara T., Sudo Y., Suzuki K., Irie T. Human cerebral acetylcholinesterase activity measured with positron emission tomography: procedure, normal values and effect of age. Eur. J. Nucl. Med 1999, 26:135-143.
54. Newhouse P.A., Potter A., Corwin J., Lenox R. Age-related effects of the nicotinic antagonist mecamylamine on cognition and behavior. Neuropsychopharmacology 1994, 10:93-107.
55. Ota T., Shinotoh H., Fukushi K., Nagatsuka S., Namba H., Iyo M., Aotsuka A., Tanaka N., Sato K., Shiraishi T., Tanada S., Arai H., Irie T. A simple method for the detection of abnormal brain regions in Alzheimer's disease patients using [11C]MP4A: comparison with [123I]IMP SPECT. Ann. Nucl. Med 2004, 18:187-193.
56. Pappas B.A., Bayley P.J., Bui B.K., Hansen L.A., Thal L.J. Choline acetyltransferase activity and cognitive domain scores of Alzheimer's patients. Neurobiol. Aging 2000, 21:11-17.
57. Perry E., Walker M., Grace J., Perry R. Acetylcholine in mind: a neurotransmitter correlate of consciousness?. Trends Neurosci 1999, 22:273-280.
58. Perry E.K., Perry R.H., Blessed G., Tomlinson B.E. Necropsy evidence of central cholinergic deficits in senile dementia. Lancet 1977, 1:189.
59. Petersen R.C., Morris J.C. Mild cognitive impairment as a clinical entity and treatment target. Arch. Neurol 2005, 62:1160-1163. 1167.
60. Raschetti R., Albanese E., Vanacore N., Maggini M. Cholinesterase inhibitors in mild cognitive impairment: a systematic review of randomised trials. PLoS Med 2007, 4:e338.
61. Reitan R.M. Trail Making Test: Manual for Administration, Scoring and Interpretation, Indianapolis 1956.
62. Ridley R.M., Aitken D.M., Baker H.F. Learning about rules but not about reward is impaired following lesions of the cholinergic projection to the hippocampus. Brain Res. 1989, 502:306-318.
63. Ridley R.M., Samson N.A., Baker H.F., Johnson J.A. Visuospatial learning impairment following lesion of the cholinergic projection to the hippocampus. Brain Res. 1988, 456:71-87.
64. Ridley R.M., Timothy C.J., Maclean C.J., Baker H.F. Conditional learning and memory impairments following neurotoxic lesion of the CA1 field of the hippocampus. Neuroscience 1995, 67:263-275.
65. Rinne J.O., Kaasinen V., Jarvenpaa T., Nagren K., Roivainen A., Yu M., Oikonen V., Kurki T. Brain acetylcholinesterase activity in mild cognitive impairment and early Alzheimer's disease. J. Neurol. Neurosurg. Psychiatry 2003, 74:113-115.
66. Sabri O., Kendziorra K., Wolf H., Gertz H.J., Brust P. Acetylcholine receptors in dementia and mild cognitive impairment. Eur. J. Nucl. Med. Mol. Imaging 2008, 35(suppl 1):S30-S45.
67. Schaaf A., Kessler J., Grond M., Fink G. Memo Test. Ein verbaler Gedächtnistest Nach der Methode des selektiven Erinnerns 1992, Beltz-Test-Verlag, Weinheim.
68. Schliebs R. Basal forebrain cholinergic dysfunction in Alzheimer's disease - interrelationship with beta-amyloid, inflammation and neurotrophin signaling. Neurochem. Res 2005, 30:895-908.
69. Shinotoh H., Fukushi K., Nagatsuka S., Tanaka N., Aotsuka A., Ota T., Namba H., Tanada S., Irie T. The amygdala and Alzheimer's disease: positron emission tomographic study of the cholinergic system. Ann. N.Y. Acad. Sci 2003, 985:411-419.
70. Shinotoh H., Namba H., Fukushi K., Nagatsuka S., Tanaka N., Aotsuka A., Ota T., Tanada S., Irie T. Progressive loss of cortical acetylcholinesterase activity in association with cognitive decline in Alzheimer's disease: a positron emission tomography study. Ann. Neurol 2000, 48:194-200.
71. Spreen O., Strauss E. A Compendium of Neuropsychological Tests - Administration, Norms and Commentary 1998, Oxford University Press, New York.
72. Stopford C.L., Snowden J.S., Thompson J.C., Neary D. Distinct memory profiles in Alzheimer's disease. Cortex 2007, 43:846-857.
73. Terriere E., Dempsey M.F., Herrmann L.L., Tierney K.M., Lonie J.A., O'Carroll R.E., Pimlott S., Wyper D.J., Herholz K., Ebmeier K.P. 5-(123)I-A-85380 binding to the alpha4beta2-nicotinic receptor in mild cognitive impairment. Neurobiology of Aging 2010, 31:1885-1893.
74. Vitiello B., Martin A., Hill J., Mack C., Molchan S., Martinez R., Murphy D.L., Sunderland T. Cognitive and behavioral effects of cholinergic, dopaminergic, and serotonergic blockade in humans. Neuropsychopharmacology 1997, 16:15-24.
75. 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 1982, 215:1237-1239.
76. Zola-Morgan S., Squire L.R. Memory impairment in monkeys following lesions limited to the hippocampus. Behav. Neurosci 1986, 100:155-160.
77. Zundorf G., Herholz K., Lercher M., Wienhard K., Bauer B., Weisenbach S., Heiss W.D. PET functional parametric images of acetylcholine esterase activity without blood sampling. Brain Imaging Using PET 2002, 41-46. Academic Press, San Diego. M. Senda, Y. Kimura, P. Herscovitch (Eds.).