Metabolic Topography of Parkinsonism

  • Kim, Jae-Seung (Department of Nuclear Medicine, Asan Medical Center, University of Ulsan College of Medicine)
  • 김재승 (울산의대 서울아산병원 핵의학과)
  • Published : 2007.04.30

Abstract

Parkinson's disease is one of the most frequent neurodegenerative diseases, which mainly affects the elderly. Parkinson's disease is often difficult to differentiate from atypical parkinson diorder such as progressive supranuclear palsy, multiple system atrophy, dementia with Lewy body, and corticobasal ganglionic degeneration, based on the clinical findings because of the similarity of phenotypes and lack of diagnostic markers. The accurate diagnosis of Parkinson's disease and atypical Parkinson disorders is not only important for deciding on treatment regimens and providing prognosis, but also it is critical for studies designed to investigate etiology and pathogenesis of parkinsonism and to develop new therapeutic strategies. Although degeneration of the nigrostriatal dopamine system results in marked loss of striatal dopamine content in most of the diseases causing parkinsonism, pathologic studies revealed different topographies of the neuronal cell loss in Parkisonism. Since the regional cerebral glucose metabolism is a marker of integrated local synaptic activity and as such is sensitive to both direct neuronal/synaptic damage and secondary functional disruption at synapses distant from the primary site of pathology, an assessment of the regional cerebral glucose metabolism with F-18 FDG PET is useful in the differential diagnosis of parkinsonism and evaluating the pathophysiology of parkisonism.

파킨슨병은 노년층에 가장 흔한 퇴행성 뇌질환 중의 하나로 진행성핵상마비, 다중계 위축, 루이체 치매 등과 같은 비전형 파킨슨병과 임상적으로 감별이 어려울 수 있다. 파킨슨병과 비전형 파킨슨병의 감별은 치료방침 결정과 예후평가뿐만 아니라 파킨슨병의 원인과 병태생리를 연구하고 새로운 치료법 개발에 있어서도 매우 중요하다. 파킨슨병과 비전형 파킨슨병과 같이 파킨슨 증후군을 유발하는 질환은 선조체내 도파민 신경의 퇴행성 변화를 흔히 동반하지만 병태생리학적으로 서로 다른 뇌피질 및 피질하 구조물에서의 신경세포 소실을 동반하고 있다. 따라서 국소 시냅스 활성도와 신경 및 시냅스의 손상, 그리고 원발병변과 기능적으로 연결된 원격부위의 기능이상 등을 대변하는 뇌포도당 대사를 F-18FDG PET으로 평가하는 것은 파킨슨 병의 감별진단과 병태생리를 평가하는데 유용하다.

Keywords

References

  1. Fahn S, Przedborski S. Parkinsonism. In: Rowland LP, editor. Merritt's Neurology. 10th ed. Philadelphia: Lippincott Williams & Wilkins; 2000, p679-693
  2. Poewe W, Wenning G. The differential diagnosis of Parkinson's disease. Eur J Neurol 2002;9(S3):23-30
  3. Bosman T, Van Laere K, Santens P. Anatomically standardised (99m)Tc-ECD brain perfusion SPET allows accurate differentiation between healthy volunteers, multiple system atrophy and idiopathic Parkinson's disease. Eur J Nucl Med Mol Imaging 2003;30:16-24 https://doi.org/10.1007/s00259-002-1009-9
  4. Brooks DJ. Morphological and functional imaging studies on the diagnosis and progression of Parkinson's disease. J Neuro 2000;247 Suppl 2:II11-8
  5. Yekhlef F, Ballan G, Macia F, Delmer O, Sourgen C, Tison F. Routine MRI for the differential diagnosis of Parkinson's disease, MSA, PSP, and CBD. J Neural Transm 2003;110:151-69 https://doi.org/10.1007/s00702-002-0785-5
  6. Asato R, Akiguchi I, Masunaga S, Hashimoto N. Magnetic resonance imaging distinguishes progressive supranuclear palsy from multiple system atrophy. J Neural Transm 2000;107:1427-36 https://doi.org/10.1007/s007020070006
  7. Ghaemi M, Hilker R, Rudolf J, Sobesky J, Heiss WD. Differentiating multiple system atrophy from Parkinson's disease: contribution of striatal and midbrain MRI volumetry and multi-tracer PET imaging. J Neurol Neurosurg Psychiatry 2002;73:517-23 https://doi.org/10.1136/jnnp.73.5.517
  8. Taniwaki T, Nakagawa M, Yamada T, Yoshida T, Ohyagi Y, Sasaki M, Kuwabara Y, Tobimatsu S, Kira J. Cerebral metabolic changes in early multiple system atrophy: a PET study. J Neurol Sc .2002;200:79-84 https://doi.org/10.1016/S0022-510X(02)00151-X
  9. Schwarz J, Kraft E, Vogl T, Arnold G, Tatsch K, Oertel WH. Relative quantification of signal on T2-weighted images in the basal ganglia: limited value in differential diagnosis of patients with parkinsonism. Neuroradiology 1999;41:124-8 https://doi.org/10.1007/s002340050716
  10. Schulz JB, Skalej M, Wedekind D, Luft AR, Abele M, Voigt K, Dichgans J, Klockgether T. Magnetic resonance imaging-based volumetry differentiates idiopathic Parkinson's syndrome from multiple system atrophy and progressive supranuclear palsy. Ann Neurol 1999;45:65-74 https://doi.org/10.1002/1531-8249(199901)45:1<65::AID-ART12>3.0.CO;2-1
  11. Feigin A, Antonini A, Fukuda M, De Notaris R, Benti R, Pezzoli G, Mentis MJ, Moeller JR, Eidelberg D. Tc-99m ethylene cysteinate dimer SPECT in the differential diagnosis of parkinsonism. Mov Disord 2002;17:1265-70 https://doi.org/10.1002/mds.10270
  12. Tzen KY, Lu CS, Yen TC, Wey SP, Ting G. Differential diagnosis of Parkinson's disease and vascular parkinsonism by (99m)Tc- TRODAT-1. J Nucl Med 2001:42:408-13
  13. Burn DJ, Sawle GV, Brooks DJ. Differential diagnosis of Parkinson's disease, multiple system atrophy, and Steele-Richardson- Olszewski syndrome: discriminant analysis of striatal 18F-dopa PET data. J Neurol Neurosurg Psychiatry 1994;57:278-84 https://doi.org/10.1136/jnnp.57.3.278
  14. Schrag A, Good CD, Miszkiel K, Morris HR, Mathias CJ, Lees AJ, Quinn NP. Differentiation of atypical parkinsonian syndromes with routine MRI. Neurology 2000;54:697-702 https://doi.org/10.1212/WNL.54.3.697
  15. Schrag A, Ben-Shlomo Y, Quinn NP. Prevalence of progressive supranuclear palsy and multiple system atrophy: a cross-sectional study. Lancet 1999;354:1771-5 https://doi.org/10.1016/S0140-6736(99)04137-9
  16. Antonini A, Leenders KL, Vontobel P, Maguire RP, Missimer J, Psylla M, Gunther I. Complementary PET studies of striatal neuronal function in the differential diagnosis between multiple system atrophy and Parkinson's disease. Brain 1997;120:2187-95 https://doi.org/10.1093/brain/120.12.2187
  17. Varrone A, Marek KL, Jennings D, Innis RB, Seibyl JP. [(123)I]beta-CIT SPECT imaging demonstrates reduced density of striatal dopamine transporters in Parkinson's disease and multiple system atrophy. Mov Disord 2001;16:1023-32 https://doi.org/10.1002/mds.1256
  18. Kim YJ, Ichise M, Ballinger JR, Vines D, Erami SS, Tatschida T, Lang AE. Combination of dopamine transporter and D2 receptor SPECT in the diagnostic evaluation of PD, MSA, and PSP. Mov Disord 2002;17:303-12 https://doi.org/10.1002/mds.10042
  19. Eidelberg D, Moeller JR, Ishikawa T, Dhawan V, Spetsieris P, Chaly T, Belakhlef A, Mandel F, Przedborski S, Fahn S. Early differential diagnosis of Parkinson's disease with 18Ffluorodeoxyglucose and positron emission tomography. Neurology 1995;45:1995-2004 https://doi.org/10.1212/WNL.45.11.1995
  20. Hosaka K, Ishii K, Sakamoto S, Mori T, Sasaki M, Hirono N, Mori E. Voxel-based comparison of regional cerebral glucose metabolism between PSP and corticobasal degeneration. J Neurol Sci 2002;199:67-71 https://doi.org/10.1016/S0022-510X(02)00102-8
  21. Magistretti PJ, Pellerin L, Rothman DL, Shulman RG. Energy on demand. Science 1999;283:496-7 https://doi.org/10.1126/science.283.5401.496
  22. Lang AE, Lozano AM. Parkinson's disease. First of two parts. New Engl J Med 1998;339:1044-51 https://doi.org/10.1056/NEJM199810083391506
  23. Lang AE, Lozano AM. Parkinson's disease. Second of two parts. New Engl J Med 1998;339:1130-43 https://doi.org/10.1056/NEJM199810153391607
  24. Mohr E, Mann UM, Miletich RS, Sampson M, Goldberg TE, Grimes JD, et al. Neuropsychological and glucose metabolic profiles in asymmetric Parkinson's disease. Can J Neurol Sci 1992;19:163-9
  25. Piert M, Koeppe RA, Giordani B, Minoshima S, Kuhl DE. Determination of regional rate constants from dynamic FDG-PET studies in Parkinson's disease. J Nucl Med 1996;37:1115-22
  26. Antonini A, Schwarz J, Oertel WH, Pogarell O, Leenders KL. Longterm changes of striatal dopamine D2 receptors in patients with Parkinson's disease: a positron emission tomography and C-11 raclopride. Moc Disord 1997;12:33-8 https://doi.org/10.1002/mds.870120107
  27. Brooks DJ, Ibanez V, Sawle GV, Playford ED, Quinn N, Mathias CJ, et al. striatal D2 receptor status in patients with Parkinson's disease, striatonigral degeneration, and progressive supranuclear palsy, measured with C-11 raclopride and positron emission tomography. Ann Neurol 1992;31:184-92 https://doi.org/10.1002/ana.410310209
  28. Kuhl DE, Metter EJ, Riege WH. Patterns of local glucose utilization determined in Parkinson's disease by the F-18 FDG method. Ann Neurol 1984;15:419-24 https://doi.org/10.1002/ana.410150504
  29. Turjanski N, Brooks DJ. PET and the investigation of dementia in the parkinsonian patient. J Neural Trasm 1997;51:37-48
  30. Peppard RF, Martin W, Carr GD, Grochowski E, Schulzer M, Guttman M, et al. cerebral glucose metabolism in Parkinson's disease with and without dementia. Arch Neurol 1992;49;1262-8 https://doi.org/10.1001/archneur.1992.00530360060019
  31. Huges AJ, Daniel SE, Blankson S, Lees AJ. A clinicopathological study of 100 cases in Parkinson's disease. Arch Neurol 1993;50:140-8 https://doi.org/10.1001/archneur.1993.00540020018011
  32. Tison F, Dartigues JF, Auriacombe S, Letenneur S, Boller F, Alperovitch A. Dementia in Parkinson's disease: a population-based study in ambulatory and institutionalized individuals. Neurology 1995;45:705-8 https://doi.org/10.1212/WNL.45.4.705
  33. Bohnen NI, Minoshima S, Giordani B, Frey KA, Kuhl DE. Motor correlates of occipital glucose hypometabolism in Parkinson's disease without dementia. Neurology 1999;52:541-6 https://doi.org/10.1212/WNL.52.3.541
  34. Hu MTM, Taylor-Robinson SD, Chaudhuri KR, Bell JD, LabbeC, Cunningham VJ, Koepp MJ, et al. Cortical dysfunction in non-demented Parkinson's disease patients. A combined 31P-MRS and 18 FDG-PET study. Brain 2000;123:340-52 https://doi.org/10.1093/brain/123.2.340
  35. Peppard RF, Martin WR, Clark CM, Carr GD, McGeer PL, Calne DB. Cortical glucose metabolism in Parkinson's and Alzheimer disease. J Neurosci Res 1990;27:561-8 https://doi.org/10.1002/jnr.490270417
  36. ArahataY, Hirayama M, Ieda T, Koike Y, Kato T, Tadokoro M, et al. Parietooccipital glucose hypometabolism in Parkinson's disease with autonomic failure. J Neurol Sci 1999;163:119-26 https://doi.org/10.1016/S0022-510X(99)00011-8
  37. Otsuka M, Kuwabara Y, Ichiya Y, Hosokawa S, Sasaki M, Yoshida T, et al. Differentiating between multiple system atrophy and Parkinson's disease by positron emission tomography with 18F-dopa and 18F-FDG. Ann Nucl Med 1997;11:251-7 https://doi.org/10.1007/BF03164771
  38. Eberling JL, Richardson BC, Reed BR, Wolfe N, Jagust W. Cortical glucose metabolism in Parkinson's disease without dementia. Neurobiol Aging 1994;15:329-35 https://doi.org/10.1016/0197-4580(94)90028-0
  39. Kaasinen V, Nagren K, Hietala J, Oikonen V, Vilkman H, Farde L, et al. Extrastriatal dopamine D2 and D3 receptors in early and advanced Parkinson's disease. Neurology 2000;54:1482-7 https://doi.org/10.1212/WNL.54.7.1482
  40. Rinne JO, Portin R, Ruottinen H, Nurmi E, Bergman J, et al. Cognitive impairment and the brain dopaminergic system in Parkinson's disease: [18F]fluorodopa positron emission tomography. Arch Neurol 2000;57:470-5 https://doi.org/10.1001/archneur.57.4.470
  41. Daum I, Schugens MM, Spieker S, Poster U, Schonle PW, Birbaumer N. Memory skill acquisitions in Parkinson's disease and frontal lobe dysfunction. Cortex 1995;31:413-32 https://doi.org/10.1016/S0010-9452(13)80057-3
  42. Taylor AE, Sain-Cyr JA, Lang AE. Frontal lobe dysfunction in Parkinson's disease. The cortical focus of neostriatal outflow. Brain 1986;109:845-83 https://doi.org/10.1093/brain/109.5.845
  43. Broussolle E, Cinotti L, Pollak P, Landais P, Le Bars D, Galy G, et al. Relief of akinesia by apomorphine and cerebral metabolic changes in Parkinson'sdisease. Mov Disord 1993;8:459-62 https://doi.org/10.1002/mds.870080407
  44. Leenders KL, Wolfson L, Gibbs JM, Wise RJ, Causon R, Jones T, et al. The effect of L-Dopa on regional cerebral blood flow and oxygen metabolism in patients with Parkinson's disease. Brain 1985;108:171-91 https://doi.org/10.1093/brain/108.1.171
  45. Gotham AM, Brown RG, Marsden CD. Frontal cognitive function in patients with Parkinson's disease on and off levodopa. Brain 1988;111:299-321 https://doi.org/10.1093/brain/111.2.299
  46. Swainson R, Rogers RD, Sahakian BJ, Summers BA, Polkey CE, Robbins TW. Probabilistic learning and reversal deficits in patients with Parkinson's disease or frontal temporal lobe lesions: possible adverse effects of dopaminergic medication. Neuropsychologica 2000;38:596-612 https://doi.org/10.1016/S0028-3932(99)00103-7
  47. Berding G, Odin P, Brooks DJ, Nikkhah G, Matthies C, et al. Resting regional cerebral glucose metabolism in advanced Parkinson's disease studied in the Off and On conditions with [18F] FDG-PET. Mov Disord 2001;16(6):1014-22 https://doi.org/10.1002/mds.1212
  48. Cohen J, Low P, Fealey R, Sheps S, Jiang NS. Somatic and autonomic function in progressive autonomic failure and multiple system atrophy. Ann Neurol 1987;22:692-99 https://doi.org/10.1002/ana.410220604
  49. Quinn N. Multiple system atrophy-the nature of the beast. J Neurol Neurosurg Psychiatry 1989;52(special suppl):78-89 https://doi.org/10.1136/jnnp.52.Suppl.78
  50. Fulham MJ , Dubinsky RM , Polinsky RJ, Brooks RA, Brown RT, Curras MT, et al. Computed tomography, magnetic resonance imaging and positron emission tomography with [18F] fluorodeoxyglucose in multiple system atrophy and pure autonomic failure. Clin Auto Res 1991;1:27-36 https://doi.org/10.1007/BF01826055
  51. Borit A, Rubinstein LJ, Urich H. The striatonigral degenerations : putaminal pigments and nosology. Brain 1975;98:101-12 https://doi.org/10.1093/brain/98.1.101
  52. Landis DMD, Rosenberg RN, Landis SC, Schut L, Nyhan WL. Olivopontocerebellar degeneration: clinical and ultrastructural abnormalities. Arch Neurol 1974;31:295-307 https://doi.org/10.1001/archneur.1974.00490410043003
  53. Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 1992;55:181-4 https://doi.org/10.1136/jnnp.55.3.181
  54. Gilman S, Koeppe RA, Junck L, Kluin KJ, Lohman M, St Laurent RT. Patterns of cerebral glucose metabolism detected with positron emission tomography differ in multiple system atrophy and olivopontocerebellar atrophy. Ann Neurol 1994;36:166-75 https://doi.org/10.1002/ana.410360208
  55. Otsuka M, Kuwabara Y, Ichiya Y, Hosokawa S, Sasaki M, Yoshida T, et al. Differentiating between multiple system atrophy and Parkinson's disease by positron emission tomography with 18F-dopa and 18F-FDG. Ann Nucl Med 1997;11:2517
  56. Taniwaki T, Nakagawa M, Yamada T, Yoshida T, Ohyagi Y, Sasaki M, et al. Cerebral metabolic changes in early multiple system atrophy: a PET study. J Neurol Sci 2002;200:79-84 https://doi.org/10.1016/S0022-510X(02)00151-X
  57. Perani D, Bressi S, Testa D, Grassi F, Cortelli P, Gentrini S, et al. Clinical/metabolic correlations in multiple system atrophy: a fludeoxy glucose F18 positron emission tomographic study. Arch Neurol 1995;52:179-85 https://doi.org/10.1001/archneur.1995.00540260085021
  58. Rosenthal G, Gilman S, Koeppe RA, Kluin KJ, Markel DS, Junck L, et al. Motor dysfunction in olivopontocerebellar atrophy is related to cerebral metabolic rate studied with positron emission tomography. Ann Neurol 1988;24:41-49 https://doi.org/10.1002/ana.410240109
  59. Wenning GK, Tison F, Ben Shlomo Y, Daniel SE, Quinn NP. Multiple system atrophy: a review of 203 pathologically proven cases. Mov Disord 1997;12:133-47 https://doi.org/10.1002/mds.870120203
  60. Eidelberg D, Takikawa S, Moeller JR, Dhawan V, Redington K, Chaly T, et al. Striatal hypometabolism distinguishes striatonigral degeneration from Parkinson's disease. Ann Neurol 1993;33:518-27 https://doi.org/10.1002/ana.410330517
  61. Steele JC. Progressive supranuclear palsy. Brain 1972;95:693-704
  62. D'Antona R, Baron JC, Samson Y, et al. Subcortical dementia. Frontal cortex hypometabolism detected by positron tomography in patients with progressive supranuclearpalsy. Brain 1985;108:785-99 https://doi.org/10.1093/brain/108.3.785
  63. Foster NL, Gilman S, Berent S, Morin EM, Brown MB, Koeppe RA. Cerebral hypometabolism in progressive supranuclear palsy studied with positron emission tomography. Ann Neurol 1988;24: 399-406 https://doi.org/10.1002/ana.410240308
  64. Goffinet AM, De Volder AG, Gillain C, et al. Positron tomography demonstrates frontal lobe hypometabolism in progressive supranuclear palsy. Ann Neurol 1989;25:131-9 https://doi.org/10.1002/ana.410250205
  65. Foster NL, Sima AAF, D'Amato C, et al. Cerebral cortical pathology in progressive supranuclear palsy is correlated with severity of dementia. Neurology 1996;46:A363.Abstract
  66. Hosaka Kayo, Ishii K, Sakamoto S, Tetsuya M, Sasaki M, Hirono N, et al. Voxel-based comparison of regional cerebral glucose metabolism between PSP and corticobasal degeneration. J Neurol Sci 2002;199:67-71 https://doi.org/10.1016/S0022-510X(02)00102-8
  67. Ishino H, Otsuki S. Frequency of Alzheimer's neurofibrillary tangles in the cerebral cortex in progressive supranuclear palsy (subcortical argyrophilic dystrophy). J Neurol Sci 1976; 28:309-16 https://doi.org/10.1016/0022-510X(76)90024-1
  68. Schneider JA, Watts RL, Gearing M, Brewer RP, Mirra SS. Corti-cobasal degeneration: neuropathologic and clinical heterogeneity. Neurology 1997;48:959-69 https://doi.org/10.1212/WNL.48.4.959
  69. Blin J, Vidailhet MJ, Pillon B, DuboisB, Feve JR, Agid Y. Corti-cobasal degeneration: decreased and asymmetrical glucose consumption as studied with PET. Mov Disord 1992;7:348-54 https://doi.org/10.1002/mds.870070409
  70. Eidelberg D, Dhawan V, Moeller JR, Sidtis JJ, Ginos JZ, Strother SC, et al. The metabolic landscape of cortico-basal ganglionic degeneration: regional asymmetries studied with positron emission tomography. J Neurol Neurosurg Psychiatry 1991;54:856-62 https://doi.org/10.1136/jnnp.54.10.856
  71. Laureys S, Salmon E, Garraux G, Peigneux P, Lemaire C, Degueldre C, et al. Fluorodopa uptake and glucose metabolism in early stages of corticobasal degeneration. J Neurol 1999;246: 1151-8 https://doi.org/10.1007/s004150050534
  72. Galvin JE, Lee VMY, Schmidt ML, Tu PH, Iwatsubo T, and Trojanowski JQ. Pathophysiology of the Lewy body. Adv Neurol 1999;80:313-24
  73. McKeith LG, Galasko D, Kosaka K, et al. Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies DLB): report of the consortium on DLB international workshop. Neurology 1996;47:1113-24 https://doi.org/10.1212/WNL.47.5.1113
  74. Albin RL, Minoshima S, D'Amato CJ, et al. Fluoro-deoxyglucose positron emission tomography in diffuse Lewy body disease. Neurology 1996;47:462-6 https://doi.org/10.1212/WNL.47.2.462
  75. Minoshima S, Foster NL, Sima AAF, Frey KA, Albin RL, Kuhl DE. Alzheimer's disease versus dementia with Lewy bodies: Cerebral metabolic distinction with autopsy confirmation. Annal Neurol 2001;50(3):358-65 https://doi.org/10.1002/ana.1133
  76. Vander Borght T, Minoshima S, Giordani B, et al. Cerebral metabolic differences in Parkinson's and Alzheimer's diseases matched for dementia severity. J Nucl Med 1997;38:797-802
  77. Spampinato U, Habert MO, Mas JL, et al. (99mTc)-HM-PAO SPECT and cognitive impairment in Parkinson's disease: a comparison with dementia of the Alzheimer type. J Neurol Neurosurg Psychiatry 1991;54:787-92 https://doi.org/10.1136/jnnp.54.9.787
  78. Liu RS, Lin KN, Wang SJ, et al. Cognition and 99Tcm-HMPAO SPECT in Parkinson's disease. Nucl Med Commun 1992;13:744-8 https://doi.org/10.1097/00006231-199213100-00007
  79. Donnemiller E, Heilmann J, Wenning GK, et al. Brain perfusion scintigraphy with 99mTc-HMPAO or 99mTc-ECD and 123I-beta- CIT single-photon emission tomography in dementia of the Alzheimer-type and diffuse Lewy body disease. Eur J Nucl Med 1997;24:320-5 https://doi.org/10.1007/BF01728771
  80. Imamura T, Ishii K, Sasaki M, et al. Regional cerebral glucose metabolism in dementia with Lewy bodies and Alzheimer's disease: a comparative study using positron emission tomography. Neurosci Lett 1997;235:49-52 https://doi.org/10.1016/S0304-3940(97)00713-1
  81. Kuhl DE. Imaging local brain function with emission computed tomography. Radiology 1984;150:625-31 https://doi.org/10.1148/radiology.150.3.6607481
  82. Minoshima S, Frey KA, Foster NL, Kuhl DE. Preserved pontine glucose metabolism in Alzheimer disease: a reference region for functional brain image (PET) analysis. J Comput Assist Tomogr 1995;19:541-7 https://doi.org/10.1097/00004728-199507000-00006
  83. Gomez-Tortosa E, Newell K, Irizarry MC, et al. Clinical and quantitative pathologic correlates of dementia with Lewy bodies. Neurology 1999;53:1284-91 https://doi.org/10.1212/WNL.53.6.1284
  84. Rezaie P, Cairns NJ, Chadwick A, Lantos PL. Lewy bodies are located preferentially in limbic areas in diffuse Lewy body disease. Neurosci Lett 1996;212:111-4 https://doi.org/10.1016/0304-3940(96)12775-0
  85. Jagust WJ. Functional imaging patterns in Alzheimer's disease. Relationships to neurobiology. Ann NY Acad Sci 1996;777:30-6 https://doi.org/10.1111/j.1749-6632.1996.tb34398.x
  86. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol (Berl) 1991;82:239-59 https://doi.org/10.1007/BF00308809
  87. Minoshima S, Giordani B, Berent S, et al. Metabolic reduction in the posterior cingulate cortex in very early Alzheimer's disease. Ann Neurol 1997;42:85-94 https://doi.org/10.1002/ana.410420114
  88. Masliah E, Terry RD, Alford M, et al. Cortical and subcortical patterns of synaptophysinlike immunoreactivity in Alzheimer's disease. Am J Pathol 1991;138:235-46
  89. Hikosaka O, Sakamoto M, Miyashita N. Effects of caudate nucleus stimulation on substantia nigra cell activity in monkey. Exp Brain Res 1993;95:457-72
  90. Manford M, Andermann F. Complex visual hallucinations. Clinical and neurobiological insights. Brain 1998;121:1819-40 https://doi.org/10.1093/brain/121.10.1819
  91. Perry EK, McKeith I, Thompson P, et al. Topography, extent, and clinical relevance of neurochemical deficits in dementia of Lewy body type, Parkinson's disease, and Alzheimer's disease. Ann NY Acad Sci 1991;640:197-202 https://doi.org/10.1111/j.1749-6632.1991.tb00217.x