Atrophy of the cholinergic basal forebrain in dementia with lewy bodies and alzheimer’s disease dementia

Journal of Neurology

Volumn 261, Issue 1, 2014, Pages 1939-1948

  Grothe, Michel J ^a   Schuster, Christina ^a   Bauer, Florian ^a   Prudlo, Johannes ^a,c   Teipel, Stefan J ^a,c   Heinsen, Helmut ^b  

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY OF ROSTOCK   (Germany)

Author keywords

Alzheimer s disease; Cholinergic basal forebrain; Dementia with Lewy bodies; Harmonized hippocampus protocol; MRI; Nucleus basalis Meynert

Indexed keywords

CHOLINERGIC RECEPTOR STIMULATING AGENT;

AGED; ALZHEIMER DISEASE; ANALYSIS OF VARIANCE; ATROPHY; DIFFUSE LEWY BODY DISEASE; FEMALE; FOREBRAIN; HIPPOCAMPUS; HUMAN; IMAGE PROCESSING; MALE; MENTAL HEALTH; METABOLISM; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ANALYSIS OF VARIANCE; ATROPHY; CHOLINERGIC AGENTS; FEMALE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; LEWY BODY DISEASE; MAGNETIC RESONANCE IMAGING; MALE; MENTAL STATUS SCHEDULE; NEUROPSYCHOLOGICAL TESTS; PROSENCEPHALON;

EID: 84914688045     PISSN: 03405354     EISSN: 14321459     Source Type: Journal    
DOI: 10.1007/s00415-014-7439-z     Document Type: Article

References (77)

1. Ballard C, Aarsland D, Francis P, Corbett A (2013) Neuropsychiatric symptoms in patients with dementias associated with cortical Lewy bodies: pathophysiology, clinical features, and pharmacological management. Drugs Aging 30:603-611
2. Barber R, Gholkar A, Scheltens P, Ballard C, McKeith IG, O’Brien JT (1999) Medial temporal lobe atrophy on MRI in dementia with Lewy bodies. Neurology 52:1153-1158
3. Basel MC (2005) CERAD-Plus: the consortium to establish a registry for Alzheimer’s disease. Univeristätsspital, Basel
4. Birks J (2006) Cholinesterase inhibitors for Alzheimer’s disease. Cochrane Database Syst Rev 1:CD005593
5. Boban M, Kostovic I, Simic G (2006) Nucleus subputaminalis: neglected part of the basal nucleus of Meynert. Brain 129:E42 (author reply E43)
6. Boccardi M, Bocchetta M, Ganzola R, Robitaille N, Redolfi A, Duchesne S, Jack CR Jr, Frisoni GB (2013) Operationalizing protocol differences for EADC-ADNI manual hippocampal segmentation. Alzheimers Dement. doi:10.1016/j.jalz.2013.03.001
7. Burton EJ, Barber R, Mukaetova-Ladinska EB, Robson J, Perry RH, Jaros E, Kalaria RN, O’Brien JT (2009) Medial temporal lobe atrophy on MRI differentiates Alzheimer’s disease from dementia with Lewy bodies and vascular cognitive impairment: a prospective study with pathological verification of diagnosis. Brain 132:195-203
8. Cagnin A, Gnoato F, Jelcic N, Favaretto S, Zarantonello G, Ermani M, Dam M (2013) Clinical and cognitive correlates of visual hallucinations in dementia with Lewy bodies. J Neurol Neurosurg Psychiatry 84:505-510
9. Candy J, Perry R, Perry E, Irving D, Blessed G, Fairbairn A, Tomlinson B (1983) Pathological changes in the nucleus of Meynert in Alzheimer’s and Parkinson’s diseases. J Neurol Sci 59:277-289
10. Chow N, Aarsland D, Honarpisheh H, Beyer MK, Somme JH, Elashoff D, Rongve A, Tysnes OB, Thompson PM, Apostolova LG (2012) Comparing hippocampal atrophy in Alzheimer’s dementia and dementia with Lewy bodies. Dement Geriatr Cogn Disord 34:44-50
11. Collerton D, Burn D, McKeith I, O’Brien J (2003) Systematic review and meta-analysis show that dementia with Lewy bodies is a visual-perceptual and attentional-executive dementia. Dement Geriatr Cogn Disord 16:229-237
12. Cummings J, Emre M, Aarsland D, Tekin S, Dronamraju N, Lane R (2010) Effects of rivastigmine in Alzheimer’s disease patients with and without hallucinations. J Alzheimers Dis 20:301-311
13. de Medeiros K, Robert P, Gauthier S, Stella F, Politis A, Leoutsakos J, Taragano F, Kremer J, Brugnolo A, Porsteinsson AP, Geda YE, Brodaty H, Gazdag G, Cummings J, Lyketsos C (2010) The Neuropsychiatric Inventory-Clinician rating scale (NPI-C): reliability and validity of a revised assessment of neuropsychiatric symptoms in dementia. Int Psychogeriatr 22:984-994
14. de Souza Silva MA, Lenz B, Rotter A, Biermann T, Peters O, Ramirez A, Jessen F, Maier W, Hull M, Schroder J, Frolich L, Teipel S, Gruber O, Kornhuber J, Huston JP, Muller CP, Schable S (2013) Neurokinin3 receptor as a target to predict and improve learning and memory in the aged organism. Proc Natl Acad Sci USA 110:15097-15102
15. Delli Pizzi S, Franciotti R, Tartaro A, Caulo M, Thomas A, Onofrj M, Bonanni L (2014) Structural alteration of the dorsal visual network in DLB patients with visual hallucinations: a cortical thickness MRI study. PLoS One 9:e86624
16. Eagger SA, Levy R, Sahakian BJ (1991) Tacrine in Alzheimer’s disease. Lancet 337:989-992
17. Ferman TJ, Smith GE, Boeve BF, Graff-Radford NR, Lucas JA, Knopman DS, Petersen RC, Ivnik RJ, Wszolek Z, Uitti R, Dickson DW (2006) Neuropsychological differentiation of dementia with Lewy bodies from normal aging and Alzheimer’s disease. Clin Neuropsychol 20:623-636
18. Folstein MF, Folstein SE, McHugh PR (1975) ‘‘Mini-mental state’’: a practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12:189-198
19. Förstl H, Burns A, Luthert P, Cairns N, Levy R (1993) The Lewybody variant of Alzheimer’s disease. Clinical and pathological findings. Br J Psychiatry 162:385-392
20. Fujishiro H, Umegaki H, Isojima D, Akatsu H, Iguchi A, Kosaka K (2006) Depletion of cholinergic neurons in the nucleus of the medial septum and the vertical limb of the diagonal band in dementia with Lewy bodies. Acta Neuropathol 111:109-114
21. Goldman JG, Stebbins GT, Dinh V, Bernard B, Merkitch D, deToledo-Morrell L, Goetz CG (2014) Visuoperceptive region atrophy independent of cognitive status in patients with Parkinson’s disease with hallucinations. Brain 137:849-859
22. Graff-Radford J, Boeve BF, Pedraza O, Ferman TJ, Przybelski S, Lesnick TG, Vemuri P, Senjem ML, Smith GE, Knopman DS, Lowe V, Jack CR Jr, Petersen RC, Kantarci K (2012) Imaging and acetylcholinesterase inhibitor response in dementia with Lewy bodies. Brain 135:2470-2477
23. Grothe M, Heinsen H, Teipel S (2013) Longitudinal measures of cholinergic forebrain atrophy in the transition from healthy aging to Alzheimer’s disease. Neurobiol Aging 34:1210-1220
24. Grothe M, Heinsen H, Teipel SJ (2012) Atrophy of the cholinergic Basal forebrain over the adult age range and in early stages of Alzheimer’s disease. Biol Psychiatry 71:805-813
25. Grothe M, Zaborszky L, Atienza M, Gil-Neciga E, Rodriguez-Romero R, Teipel SJ, Amunts K, Suarez-Gonzalez A, Cantero JL (2010) Reduction of basal forebrain cholinergic system parallels cognitive impairment in patients at high risk of developing Alzheimer’s disease. Cereb Cortex 20:1685-1695
26. Grothe MJ, Ewers M, Krause B, Heinsen H, Teipel SJ (2014) Basal forebrain atrophy and cortical amyloid deposition in nondemented elderly subjects. Alzheimers Dement
27. Halliday GM, Cullen K, Cairns MJ (1993) Quantitation and three-dimensional reconstruction of Ch4 nucleus in the human basal forebrain. Synapse 15:1-16
28. Hanyu H, Asano T, Sakurai H, Tanaka Y, Takasaki M, Abe K (2002) MR analysis of the substantia innominata in normal aging, Alzheimer disease, and other types of dementia. AJNR Am J Neuroradiol 23:27-32
29. Hanyu H, Shimizu S, Tanaka Y, Hirao K, Iwamoto T, Abe K (2007) MR features of the substantia innominata and therapeutic implications in dementias. Neurobiol Aging 28:548-554
30. Hanyu H, Tanaka Y, Shimizu S, Sakurai H, Iwamoto T, Abe K (2005) Differences in MR features of the substantia innominata between dementia with Lewy bodies and Alzheimer’s disease. J Neurol 252:482-484
31. Hepp DH, Ruiter AM, Galis Y, Voorn P, Rozemuller AJ, Berendse HW, Foncke EM, van de Berg WD (2013) Pedunculopontine cholinergic cell loss in hallucinating Parkinson disease patients but not in dementia with Lewy bodies patients. J Neuropathol Exp Neurol 72:1162-1170
32. Hirano S, Shinotoh H, Eidelberg D (2012) Functional brain imaging of cognitive dysfunction in Parkinson’s disease. J Neurol Neurosurg Psychiatry 83:963-969
33. Iraizoz I, Guijarro JL, Gonzalo LM, de Lacalle S (1999) Neuropathological changes in the nucleus basalis correlate with clinical measures of dementia. Acta Neuropathol 98:186-196
34. Janzen J, van’t Ent D, Lemstra AW, Berendse HW, Barkhof F, Foncke EM (2012) The pedunculopontine nucleus is related to visual hallucinations in Parkinson’s disease: preliminary results of a voxel-based morphometry study. J Neurol 259:147-154
35. Jicha GA, Schmitt FA, Abner E, Nelson PT, Cooper GE, Smith CD, Markesbery WR (2010) Prodromal clinical manifestations of neuropathologically confirmed Lewy body disease. Neurobiol Aging 31:1805-1813
36. Kantarci K, Ferman TJ, Boeve BF, Weigand SD, Przybelski S, Vemuri P, Murray MM, Senjem ML, Smith GE, Knopman DS (2012) Focal atrophy on MRI and neuropathologic classification of dementia with Lewy bodies. Neurology 79:553-560
37. Kilimann I, Grothe M, Heinsen H, Alho EJ, Grinberg L, Amaro E Jr, Dos Santos GA, da Silva RE, Mitchell AJ, Frisoni GB, Bokde AL, Fellgiebel A, Filippi M, Hampel H, Kloppel S, Teipel SJ (2014) Subregional basal forebrain atrophy in Alzheimer’s disease: a multicenter study. J Alzheimers Dis 40:687-700
38. Klein JC, Eggers C, Kalbe E, Weisenbach S, Hohmann C, Vollmar S, Baudrexel S, Diederich NJ, Heiss WD, Hilker R (2010) Neurotransmitter changes in dementia with Lewy bodies and Parkinson disease dementia in vivo. Neurology 74:885-892
39. Levy R, Eagger S, Griffiths M, Perry E, Honavar M, Dean A, Lantos P (1994) Lewy bodies and response to tacrine in Alzheimer’s disease. Lancet 343:176
40. Liberini P, Valerio A, Memo M, Spano PF (1996) Lewy-body dementia and responsiveness to cholinesterase inhibitors: a paradigm for heterogeneity of Alzheimer’s disease? Trends Pharmacol Sci 17:155-160
41. Lippa CF, Smith TW, Perry E (1999) Dementia with Lewy bodies: choline acetyltransferase parallels nucleus basalis pathology. J Neural Transm 106:525-535
42. Marra C, Quaranta D, Profice P, Pilato F, Capone F, Iodice F, Di Lazzaro V, Gainotti G (2012) Central cholinergic dysfunction measured ‘‘in vivo’’ correlates with different behavioral disorders in Alzheimer’s disease and dementia with Lewy body. Brain Stimul 5:533-538
43. Marui W, Iseki E, Kato M, Akatsu H, Kosaka K (2004) Pathological entity of dementia with Lewy bodies and its differentiation from Alzheimer’s disease. Acta Neuropathol 108:121-128
44. McKeith I, Dickson D, Lowe J, Emre M, O’brien J, Feldman H, Cummings J, Duda J, Lippa C, Perry E (2005) Diagnosis and management of dementia with Lewy bodies third report of the DLB consortium. Neurology 65:1863-1872
45. McKeith I, Mintzer J, Aarsland D, Burn D, Chiu H, Cohen-Mansfield J, Dickson D, Dubois B, Duda JE, Feldman H, Gauthier S, Halliday G, Lawlor B, Lippa C, Lopez OL, Machado JC, O’Brien J, Playfer J (2004) Dementia with Lewy bodies. Lancet Neurol 3:19-28
46. McKeith I, O’Brien J, Walker Z, Tatsch K, Booij J, Darcourt J, Padovani A, Giubbini R, Bonuccelli U, Volterrani D, Holmes C, Kemp P, Tabet N, Meyer I, Reininger C (2007) Sensitivity and specificity of dopamine transporter imaging with 123I-FP-CIT SPECT in dementia with Lewy bodies: a phase III, multicentre study. Lancet Neurol 6:305-313
47. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer’s disease Report of the NINCDS-ADRDA Work Group* under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology 34:939
48. Mesulam MM, Mufson EJ, Levey AI, Wainer BH (1983) 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 214:170-197
49. Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185-1201
50. Mori E, Ikeda M, Kosaka K (2012) Donepezil for dementia with Lewy bodies: a randomized, placebo-controlled trial. Ann Neurol 72:41-52
51. Morris J, Heyman A, Mohs R, Hughes J, Van Belle G, Fillenbaum G, Mellits E, Clark C, the CERAD investigators (1989) The consortium to establish a registry for Alzheimer’s disease (CERAD). Part I. Clinical and neuropsychological assessment of Alzheimer’s disease. Neurology 39:1159-1165
52. Muir JL (1997) Acetylcholine, aging, and Alzheimer’s disease. Pharmacol Biochem Behav 56:687-696
53. Narayanan NS, Rodnitzky RL, Uc EY (2013) Prefrontal dopamine signaling and cognitive symptoms of Parkinson’s disease. Rev Neurosci 24:267-278
54. Pappas BA, Bayley PJ, Bui BK, Hansen LA, Thal LJ (2000) Choline acetyltransferase activity and cognitive domain scores of Alzheimer’s patients. Neurobiol Aging 21:11-17
55. Perry EK, Haroutunian V, Davis KL, Levy R, Lantos P, Eagger S, Honavar M, Dean A, Griffiths M, McKeith IG et al (1994) Neocortical cholinergic activities differentiate Lewy body dementia from classical Alzheimer’s disease. NeuroReport 5:747-749
56. Rolinski M, Fox C, Maidment I, McShane R (2012) Cholinesterase inhibitors for dementia with Lewy bodies, Parkinson’s disease dementia and cognitive impairment in Parkinson’s disease. Cochrane Database Syst Rev 3:CD006504
57. Sanchez-Cubillo I, Perianez JA, Adrover-Roig D, Rodriguez-Sanchez JM, Rios-Lago M, Tirapu J, Barcelo F (2009) Construct validity of the Trail Making Test: role of task-switching, working memory, inhibition/interference control, and visuomotor abilities. J Int Neuropsychol Soc 15:438-450
58. Sarter M, Albin RL, Kucinski A, Lustig C (2014) Where attention falls: increased risk of falls from the converging impact of cortical cholinergic and midbrain dopamine loss on striatal function. Exp Neurol 257C:120-129
59. Scherfler C, Esterhammer R, Nocker M, Mahlknecht P, Stockner H, Warwitz B, Spielberger S, Pinter B, Donnemiller E, Decristoforo C, Virgolini I, Schocke M, Poewe W, Seppi K (2013) Correlation of dopaminergic terminal dysfunction and microstructural abnormalities of the basal ganglia and the olfactory tract in Parkinson’s disease. Brain 136:3028-3037
60. Shimada H, Hirano S, Shinotoh H, Aotsuka A, Sato K, Tanaka N, Ota T, Asahina M, Fukushi K, Kuwabara S (2009) Mapping of brain acetylcholinesterase alterations in Lewy body disease by PET. Neurology 73:273-278
61. Shulman KI (2000) Clock-drawing: is it the ideal cognitive screening test? Int J Geriatr Psychiatry 15:548-561
62. Takahashi R, Ishii K, Miyamoto N, Yoshikawa T, Shimada K, Ohkawa S, Kakigi T, Yokoyama K (2010) Measurement of gray and white matter atrophy in dementia with Lewy bodies using diffeomorphic anatomic registration through exponentiated lie algebra: a comparison with conventional voxel-based morphometry. AJNR Am J Neuroradiol 31:1873-1878
63. Tam CW, Burton EJ, McKeith IG, Burn DJ, O’Brien JT (2005) Temporal lobe atrophy on MRI in Parkinson disease with dementia: a comparison with Alzheimer disease and dementia with Lewy bodies. Neurology 64:861-865
64. Tanaka Y, Hanyu H, Sakurai H, Takasaki M, Abe K (2003) Atrophy of the substantia innominata on magnetic resonance imaging predicts response to donepezil treatment in Alzheimer’s disease patients. Dement Geriatr Cogn Disord 16:119-125
65. Teipel S, Heinsen H, Amaro E Jr, Grinberg LT, Krause B, Grothe M (2014) Cholinergic basal forebrain atrophy predicts amyloid burden in Alzheimer’s disease. Neurobiol Aging 35:482-491
66. Teipel SJ, Flatz W, Ackl N, Grothe M, Kilimann I, Bokde AL, Grinberg L, Amaro E Jr, Kljajevic V, Alho E, Knels C, Ebert A, Heinsen H, Danek A (2014) Brain atrophy in primary progressive aphasia involves the cholinergic basal forebrain and Ayala’s nucleus. Psychiatry Res 221:187-194
67. Teipel SJ, Flatz WH, Heinsen H, Bokde AL, Schoenberg SO, Stöckel S, Dietrich O, Reiser MF, Möller H-J, Hampel H (2005) Measurement of basal forebrain atrophy in Alzheimer’s disease using MRI. Brain 128:2626-2644
68. Teipel SJ, Meindl T, Grinberg L, Grothe M, Cantero JL, Reiser MF, Moller HJ, Heinsen H, Hampel H (2011) The cholinergic system in mild cognitive impairment and Alzheimer’s disease: an in vivo MRI and DTI study. Hum Brain Mapp 32: 1349-1362
69. Tiraboschi P, Hansen LA, Alford M, Merdes A, Masliah E, Thal LJ, Corey-Bloom J (2002) Early and widespread cholinergic losses differentiate dementia with Lewy bodies from Alzheimer disease. Arch Gen Psychiatry 59:946-951
70. Tiraboschi P, Salmon DP, Hansen LA, Hofstetter RC, Thal LJ, Corey-Bloom J (2006) What best differentiates Lewy body from Alzheimer’s disease in early-stage dementia? Brain 129:729-735
71. Vogels OJ, Broere CA, ter Laak HJ, ten Donkelaar HJ, Nieuwenhuys R, Schulte BP (1990) Cell loss and shrinkage in the nucleus basalis Meynert complex in Alzheimer’s disease. Neurobiol Aging 11:3-13
72. Whitehouse PJ, Hedreen JC, White CL, Price DL (1983) Basal forebrain neurons in the dementia of Parkinson disease. Ann Neurol 13:243-248
73. Whitehouse PJ, Price DL, Clark AW, Coyle JT, DeLong MR (1981) Alzheimer disease: evidence for selective loss of cholinergic neurons in the nucleus basalis. Ann Neurol 10:122-126
74. Whitwell JL, Weigand SD, Shiung MM, Boeve BF, Ferman TJ, Smith GE, Knopman DS, Petersen RC, Benarroch EE, Josephs KA, Jack CR Jr (2007) Focal atrophy in dementia with Lewy bodies on MRI: a distinct pattern from Alzheimer’s disease. Brain 130:708-719
75. Wider C, Ross OA, Nishioka K, Heckman MG, Vilarino-Guell C, Jasinska-Myga B, Erketin-Taner N, Rademakers R, Graff-Radford NR, Mash DC, Papapetropoulos S, Duara R, Uchikado H, Wszolek ZK, Farrer MJ, Dickson DW (2012) An evaluation of the impact of MAPT, SNCA and APOE on the burden of Alzheimer’s and Lewy body pathology. J Neurol Neurosurg Psychiatry 83:424-429
76. Zaborszky L, Csordas A, Mosca K, Kim J, Gielow MR, Vadasz C, Nadasdy Z (2013) Neurons in the basal forebrain project to the cortex in a complex topographic organization that reflects corticocortical connectivity patterns: an experimental study based on retrograde tracing and 3D reconstruction. Cereb Cortex
77. Zaborszky L, Hoemke L, Mohlberg H, Schleicher A, Amunts K, Zilles K (2008) Stereotaxic probabilistic maps of the magnocellular cell groups in human basal forebrain. Neuroimage 42:1127-1141