Download PDF

Journal of Neurology

, Volume 246, Supplement 2, pp II6–II15 | Cite as

Neuropathologic differentiation of progressive supranuclear palsy and corticobasal degeneration

Article

Abstract

Progressive supranuclear palsy (PSP) and corticobasal degeneration (CBD) are usually sporadic multisystem degenerations associated with filamentous tau inclusions in neurons and glia. As such they can be considered sporadic tauopathies in contrast to familial tauopathies linked to mutations in the tau gene. Mutations have not been found in the tau gene in either PSP or CBD. The clinical syndromes and neuroimaging of typical cases of PSP and CBD are distinct; however, atypical cases are described that have overlapping clinical and pathologic features. Both PSP and CBD have similar biochemical alterations in the tau protein, with the abnormal tau protein containing predominantly four-repeat tau. While there is overlap in the pathology in PSP and CBD, there are sufficient differences to continue the present day trend to consider these separate disorders. Several important pathologic features differentiate PSP from CBD. Ballooned neurons are frequent and nearly a sine qua non for CBD, but they are found in PSP at a frequency similar to that of other neurodegenerative diseases, such as Alzheimer’s disease. Astrocytic lesions are different, with tufted astrocytes found in motor cortex and striatum in PSP and astrocytic plaques in focal atrophic cortices in CBD. The most characteristic neuronal tau pathology in CBD is wispy, fine filamentous inclusions within neuronal cell bodies, while affected neurons in PSP have compact, dense filamentous aggregates characteristic of globose neurofibrillary tangles. Thread-like processes in gray and white matter are much more numerous and widespread in CBD than in PSP. The brunt of the pathology in CBD is in the cerebrum, while the basal ganglia, diencephalon and brainstem are the targets of PSP. Further clinicopathologic studies will refine our understanding of these disorders and open the possibility that common etiologic factors may be identified for these unusual sporadic tauopathies.

Key words

Corticobasal degeneration Progressive supranuclear palsy Tau Neuropathology 
Download to read the full article text

References

  1. 1.
    Agid Y, Javoy-Agid F, Ruberg M, Pillon B, Dubois B, Duyckaerts C, Hauw JJ, Baron JC, Scatton B (1987) Progressive supranuclear palsy: anatomoclinical and biochemical considerations. Adv Neurol 45: 191–206PubMedGoogle Scholar
  2. 2.
    Arai N (1987) “Grumose degeneration” of the dentate nucleus. A light and electron microscopic study in PSP and dentatorubropallidoluysian atrophy. J Neurol Sci 90: 131–145CrossRefGoogle Scholar
  3. 3.
    Baker M, Litvan J, Houlden H, Adamson J, Dickson D, Perez-Tur J, Hardy J, Lynch T, Bigio E, Hutton M (1999) Association of an extended haplotype in the tau gene with progressive supranuclear palsy. Human Mol Gen 8: 711–715CrossRefGoogle Scholar
  4. 4.
    Bancher C, Lassmann H, Budka H, Grundke-Iqbal I, Iqbal K, Wiche G, Seitelberger F, Wisniewski HM (1987) Neurofibrillary tangles in Alzheimer’s disease and progressive supranuclear palsy: Antigenic similarities and differences. Acta Neuropathol 74: 39–46PubMedCrossRefGoogle Scholar
  5. 5.
    Baron JC, Maziere B, Loch C, Cambon H, Sgouropoulos P, Bonnet AM, Agid Y (1986) Loss of striatal [76Br] bromospiperone binding sites demonstrated by positron tomography in progressive supranuclear palsy. J Cerebral Blood Flow Metab 6: 131–136Google Scholar
  6. 6.
    Blin J, Vidailhet M-J, Pillon B, Dubois B, Feve J-R, Agid Y (1992) Corticobasal degeneration: decreased and asymmetrical glucose consumption as studied with PET. Movement Disorders 7: 348–354PubMedCrossRefGoogle Scholar
  7. 7.
    Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82: 239–259PubMedCrossRefGoogle Scholar
  8. 8.
    Braak H, Jellinger K, Braak E, Bohl J (1992) Allocortical neurofibrillary changes in progressive supranuclear palsy. Acta Neuropathol 84: 478–483PubMedCrossRefGoogle Scholar
  9. 9.
    Brooks DJ, Ibanez V, Sawle GV, Quinn N, Lees AJ, Mathias CJ, Bannister R, Marsden CD, Frakowiak RSJ (1990) Differing patterns of striatal18F-dopa uptake in Parkinson’s disease multiple system atrophy and progressive supranuclear palsy. Ann Neurol 28: 547–555PubMedCrossRefGoogle Scholar
  10. 10.
    Bugiani O, Mancardi GL, Brusa A, Ederli A (1979) The fine structure of subcortical neurofibrillary tangles in progressive supranuclear palsy. Acta Neuropathol 45: 147–152PubMedCrossRefGoogle Scholar
  11. 11.
    Chin SS, Goldman JE (1996) Glial inclusions in CNS degenerative diseases. J Neuropathol Exp Neurol 55: 499–508PubMedCrossRefGoogle Scholar
  12. 12.
    Clark AW, Manz HJ, White CL 3rd, Lehmann J, Miller D, Coyle JT (1986) Cortical degeneration with swollen chromatolytic neurons: its relationship to Pick’s disease. J Neuropathol Exp Neurol 45: 268–284PubMedCrossRefGoogle Scholar
  13. 13.
    Collins SJ, Ahlskog JE, Parisi JE, Maraganore DM (1995) Progressive supranuclear palsy: neuropathologically based diagnostic clinical criteria. J Neurol Neurosurg Psychiatry 58: 167–173PubMedCrossRefGoogle Scholar
  14. 14.
    Conrad C, Andreadis A, Trojanowski JQ, Dickson DW, Kang D, Chen X, Wiederholt W, Hansen L, Masliah E, Thal LJ, Katzman R, Xia Y, Saitoh T (1997) Genetic evidence for the involvement of τ in progressive supranuclear palsy. Ann Neurol 41: 277–281PubMedCrossRefGoogle Scholar
  15. 15.
    Cruz-Sanchez FF, Rossi ML, Cardozo A, Deacon P, Tolosa E (1992) Clinical and pathological study of two patients with progressive supranuclear palsy and Alzheimer’s changes. Antigenic determinants that distinguish cortical and subcortical neurofibrillary tangles. Neurosci Lett 136: 43–46PubMedCrossRefGoogle Scholar
  16. 16.
    Cruz-Sanchez FF, Rossi ML, Cardozo A, Picardo A, Tolosa E (1992) Immunohistological study of grumose degeneration of the dentate nucleus in progressive supranuclear palsy. J Neurological Sci 110: 228–231CrossRefGoogle Scholar
  17. 17.
    D’Antona R, Baron JC, Sanson Y, Serdaru M, Viader F, Agid Y, Cambier J (1985) Subcortical dementia: frontal cortex hypometabolism detected by positron tomography in patients with progressive supranuclear palsy. Brain 108: 785–799PubMedCrossRefGoogle Scholar
  18. 18.
    Davis DG, Wang HZ, Markesbery WR (1992) Image analysis of neuropil threads in Alzheimer’s Pick’s diffuse Lewy body disease and in progressive supranuclear palsy. J Neuropathol Exp Neurol 51: 594–600PubMedCrossRefGoogle Scholar
  19. 19.
    Davis PH, Bergeron C, McLachlan R (1985) Atypical presentation of progressive supranuclear palsy. Ann Neurol 17: 337–343PubMedCrossRefGoogle Scholar
  20. 20.
    Davis PH, Golbe LI, Duvoisin RC, Schoenberg BS (1988) Risk factors for progressive supranuclear palsy. Neurology 38: 1546–1552PubMedGoogle Scholar
  21. 21.
    de Yébenes YG, Sarasa JL, Daniel SE, Lees AJ (1995) Familial progressive supranuclear palsy: description of a pedigree and review of the literature. Brain 118: 1095–1103PubMedCrossRefGoogle Scholar
  22. 22.
    Dickson DW (1997) Neurodegenerative diseases with cytoskeletal pathology: a biochemical classification. Ann Neurol 42: 541–544PubMedCrossRefGoogle Scholar
  23. 23.
    Dickson DW (1998) Pick’s disease: a modern approach. Brain Pathol 8: 339–354PubMedGoogle Scholar
  24. 24.
    Dickson DW, Yen S-H, Suzuki KI, Davies P, Garcia JH, Hirano A (1986) Ballooned neurons in select neurodegenerative diseases contain phosphorylated neurofilament epitopes. Acta Neuropathol 71: 216–23PubMedCrossRefGoogle Scholar
  25. 25.
    Dubois B, Pillon B, Legault F, Agid Y, Lhermitte F (1988) Slowing of cognitive processing progressive supranuclear palsy: a comparison with Parkinson’s disease. Arch Neurol 45: 1194–1199PubMedGoogle Scholar
  26. 26.
    Feany MB, Dickson DW (1995) Astrocytic plaques and widespread cytoskeletal pathology characterize corticobasal degeneration. Am J Pathol 146: 1388–1396PubMedGoogle Scholar
  27. 27.
    Feany MB, Ksiezak-Reding H, Liu W-K, Vincent I, Yen S-H, Dickson DW (1995) Epitope expression and hyperphosphorylation of tau protein in corticobasal degeneration: differentiation from progressive supranuclear palsy. Acta Neuropathol 90: 37–43PubMedCrossRefGoogle Scholar
  28. 28.
    Feany MB, Mattiace LA, Dickson DW (1996) Neuropathologic overlap of progressive supranuclear palsy Pick’s disease and corticobasal degeneration. J Neuropathol Exp Neurol 55: 53–67PubMedCrossRefGoogle Scholar
  29. 29.
    Flament S, Delacourte A, Verny M, Hauw J-J, Javoy-Agid F (1991) Abnormal tau proteins in progressive supranuclear palsy. Acta Neuropathol 81: 591–596PubMedCrossRefGoogle Scholar
  30. 30.
    Foster NL, Gilman S, Berent S, Morin EM, Brown MB, Koeppe RA (1988) Cerebral hypometabolism in progressive supranuclear palsy studied with positron emission tomography. Ann Neurol 24: 399–406PubMedCrossRefGoogle Scholar
  31. 31.
    Foster NL, Wilhelmsen K, Sima AAF, Jones MZ, D’Amato CJ, Gilman S, Conference Participants (1997) Frontotemporal dementia and parkinsonism linked to chromosome 17: A consensus conference. Ann Neurol 41: 706–715PubMedCrossRefGoogle Scholar
  32. 32.
    Gazeley S, Maguire JA (1996) Familial progressive supranuclear palsy. Clin Neuropathol 15: 215–220PubMedGoogle Scholar
  33. 33.
    Gearing M, Olson DA, Watts RL, Mirra SS (1994) Progressive supranuclear palsy: Neuropathologic and clinical heterogeneity. Neurology 44: 1015–1024PubMedGoogle Scholar
  34. 34.
    Geddes JF, Hughes AJ, Lees AJ, Daniel SE (1993) Pathological overlap in cases of parkinsonism associated with neurofibrillary tangles. Brain 116: 281–302PubMedCrossRefGoogle Scholar
  35. 35.
    Gibb WRG, Luthert PJ, Marsden CD (1989) Corticobasal degeneration. Brain 112: 1171–1192PubMedCrossRefGoogle Scholar
  36. 36.
    Golbe LI, Davis PH, Schoenberg BS, Duvoisin RC (1988) Prevalence and natural history of progressive supranuclear palsy. Neurology 38: 1031–1034PubMedGoogle Scholar
  37. 37.
    Golbe LI (1993) Progressive supranuclear palsy. In: Stern MB, Koller WC (eds) Parkinsonian Syndromes. Marcel Dekker, New York, pp 227–247Google Scholar
  38. 38.
    Grafman J, Litvan I, Gomez C, Chase TN (1990) Frontal lobe function in progressive supranuclear palsy. Arch Neurol 47: 553–558PubMedGoogle Scholar
  39. 39.
    Greenberg SC, Davies P (1990) A preparation of Alzheimer paired helical filaments that displays distinct tau proteins by polyacrylamide gel electrophoresis. Proc Natl Acad Sci (USA) 87: 5827–5831CrossRefGoogle Scholar
  40. 40.
    Hauw J-J, Daniel SE, Dickson D, Horoupian DS, Jellinger K, Lantos PL, McKee A, Tabaton M, Litvan I (1994) Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology 44: 2015–2019PubMedGoogle Scholar
  41. 41.
    Hauw J-J, Verny M, Delaere P, Cervera P, He Y, Duyckaerts C (1990) Constant neurofibrillary changes in the neocortex in progressive supranuclear palsy: Basic differences with Alzheimer’s disease and aging. Neurosci Lett 119: 182–186PubMedCrossRefGoogle Scholar
  42. 42.
    Hof PR, Delacourte A, Bouras C (1992) Distribution of cortical neurofibrillary tangles in progressive supranuclear palsy: A quantitative analysis of six cases. Acta Neuropathol 84: 45–51PubMedCrossRefGoogle Scholar
  43. 43.
    Horoupian DS, Chu PL (1994) Unusual case of corticobasal degeneration with tau/Gallyas-positive neuronal and glial tangles. Acta Neuropathol 88: 592–598PubMedCrossRefGoogle Scholar
  44. 44.
    Hughes AJ, Daniel SE, Blankson S, Lees AJ (1993) A clincopathologic study of 100 cases of Parkinson’s disease. Arch Neurol 50: 140–148PubMedGoogle Scholar
  45. 45.
    Hutton M, Lendon CL, Rizzu P, Baker M, Froelich S, Houlden H, Pickering-Brown S, Chakraverty S, Isaacs A, Grover A, Hackett J, Abramson J, Lincoln S, Dickson D, Davies P, Petersen RC, Stevens M, de Graaf E, Wauters E, van Baren J, Hillebrand M, Joosen M, Kwon J, Nowotny J, CheLK, Norton J, Morris JC, Reed LA, Trojanowski J, Basun H, Lannfelt L, Neystat M, Fahn S, Dark F, Tannenberg T, Dodd PR, Hayward N, Kwok JBJ, Schofield PR, Andreadis A, Snowden J, Crauford D, Neary D, Owen F, Oostra BA, Hardy J, Goate A, van Swieten J, Mann D, Lynch T, Heutink P (1998) Association of missense and 5′-splice-site mutations in tau with the inherited dementia (FTDP-17). Nature 393: 702–705PubMedCrossRefGoogle Scholar
  46. 46.
    Ikeda K Akiyama H, Haga C, Kondo H, Arima K, Oda T (1994) Argyrophilic thread-like structure in corticobasal degeneration and supranuclear palsy. Neurosci Lett 174: 157–159PubMedCrossRefGoogle Scholar
  47. 47.
    Iqbal K, Grundke-Iqbal I, Smith AJ, George L, Tung Y-C, Zaidi T (1989) Identification and localization of tau peptide to paired helical filaments of Alzheimer disease. Proc Natl Acad Sci (USA) 86: 5646–5650CrossRefGoogle Scholar
  48. 48.
    Ishino H, Otsuki S (1976) Frequency of Alzheimer’s neurofibrillary tangles in the cerebral cortex in progressive supranuclear palsy (subcortical argyrophilic dystrophy). J Neurol Sci 28: 309–316PubMedCrossRefGoogle Scholar
  49. 49.
    Iwatsubo T, Hasegawa M, Ihara Y (1994) Neuronal and glial tau-positive inclusions in diverse neurologic diseases share common phosphorylation characteristics. Acta Neuropathol 88: 129–136PubMedCrossRefGoogle Scholar
  50. 50.
    Jellinger K (1971) Progressive supranuclear palsy (subcortical argyrophilic dystrophy). Acta Neuropathol 19: 347–352PubMedCrossRefGoogle Scholar
  51. 51.
    Jellinger KA, Bancher C (1992) Neuropathology. In: Litvan I, Agid Y (eds) Progressive Supranuclear Palsy: Clinical and Research Approaches. Oxford University Press, New York, pp 44–88Google Scholar
  52. 52.
    Jendroska K, Rossor MN, Mathias CJ, Daniel SE (1995) Morphological overlap between corticobasal degeneration and Pick’s disease: a clinicopathological report. Movement Dis 10: 111–114PubMedCrossRefGoogle Scholar
  53. 53.
    Ksiezak-Reding H, Morgan K, Mattiace LA, Davies P, Liu W-K, Yen S-H, Weidenheim KM, Dickson DW (1994) Ultrastructure and biochemical composition of paired helical filaments in corticobasal degeneration. Am J Pathol 145: 1496–1508PubMedGoogle Scholar
  54. 54.
    Lang AE, Riley DE, Bergeron C (1994) Cortical-basal ganglionic degeneration. In: Calne DB (ed) Neurodegenerative Diseases. WB Saunders, Philadelphia, pp 877–894Google Scholar
  55. 55.
    Leenders KL, Frackowiak RSJ, Lees J (1988) Steele-Richardson-Olszewski syndrome: Brain energy metabolism blood flow and fluorodopa uptake measured by positron emission tomography. Brain 111: 615–630PubMedCrossRefGoogle Scholar
  56. 56.
    Leiguarda R, Lees AJ, Merello M, Starkstein S, Marsden CD (1994) The nature of apraxia in corticobasal degeneration. J Neurol Neurosurg Psychiatry 57: 455–459PubMedCrossRefGoogle Scholar
  57. 57.
    Litvan I, Grafman J, Gomez C, Chase TN (1989) Memory impairment in patients with progressive supranuclear palsy. Arch Neurol 46: 765–767PubMedGoogle Scholar
  58. 58.
    Lowe J, Errington DR, Lennox G, Pike I, Spendlove I, Landon M, Mayer RJ (1992) Ballooned neurons in several neurodegenerative diseases and stroke contain alpha B crystallin. Neuropathol Appl Neurobiol 18: 341–50PubMedCrossRefGoogle Scholar
  59. 59.
    Maher ER, Smith EM, Lees AJ (1985) Cognitive deficits in the Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). J Neurol Neurosurg Psychiatry 48: 1234–1239PubMedCrossRefGoogle Scholar
  60. 60.
    Mizusawa H, Yen S-H, Hirano A, Llena J (1989) Pathology of the dentate nucleus in progressive supranuclear palsy: a histological immunohistochemical and ultrastructural study. Acta Neuropathol 78: 419–428PubMedCrossRefGoogle Scholar
  61. 61.
    Mori H, Nishimura M, Namba Y, Oda M (1994) Corticobasal degeneration: a disease with widespread appearance of abnormal tau and neurofibrillary tangles and its relation to progressive supranuclear palsy. Acta Neuropathol 88: 113–121PubMedCrossRefGoogle Scholar
  62. 62.
    Nishimura M, Namba Y, Ideda K, Oda M (1992) Glial fibrillary tangles with straight tubules in the brains of patients with progressive supranuclear palsy. Neurosci Lett 143: 35–38PubMedCrossRefGoogle Scholar
  63. 63.
    Oyanagi K, Takahashi H, Wakabayashi K, Ikuta F (1988) Large neurons in the neostriatum in Alzheimer’s disease and progressive supranuclear palsy: a topographic, histologic and ultrastructural investigation. Brain Res 544(2): 221–226CrossRefGoogle Scholar
  64. 64.
    Paulus W, Selim M (1990) Corticonigral degeneration with neuronal achromasia and basal neurofibrillary tangles. Acta Neuropathol 81: 89–94PubMedCrossRefGoogle Scholar
  65. 65.
    Powell HC, London GW, Lampert PW (1974) Neurofibrillary tangles in progressive supranuclear palsy: electron microscopic observations. J Neuropathol Exp Neurol 33: 98–106PubMedCrossRefGoogle Scholar
  66. 66.
    Probst A, Langui D, Lautenschlager C, Ulrich J, Brion JP, Anderton, BH (1988) Progressive supranuclear palsy: extensive neuropil threads in addition to neurofibrillary tangles. Acta Neuropathol 77: 61–68PubMedCrossRefGoogle Scholar
  67. 67.
    Rajput AH, Offord KP, Beard CM, Kurland LT (1984) Epidemiology of parkinsonism: Incidence classification and mortality. Ann Neurol 16: 278–282PubMedCrossRefGoogle Scholar
  68. 68.
    Rebeiz JJ, Kolodny EH, Richardson EP (1968) Corticodentatonigral degeneration with neuronal achromasia. Arch Neurol 18: 20–33PubMedGoogle Scholar
  69. 69.
    Roy S, Datta CK, Hirano A, Ghatak NR, Zimmerman HM (1974) Electron microscopic study of neurofibrillary tangles in Steele-Richardson-Olszewski syndrome. Acta Neuropathol 29: 175–179PubMedCrossRefGoogle Scholar
  70. 70.
    Sawle GV, Brooks DJ, Marsden CD, Frackowiak RSJ (1991) Corticobasal degeneration. A unique pattern of regional cortical oxygen hypometabolism and striatal fluorodopa uptake demonstrated by positron emission tomography. Brain 114: 541–556PubMedCrossRefGoogle Scholar
  71. 71.
    Schmidt ML, Huang R, Martin JA, Henley J, Mawal-Dewan M, Hurtig HI, Lee VM, Trojanowski JQ (1996) Neurofibrillary tangles in progressive supranuclear palsy contain the same tau epitopes identified in Alzheimer’s disease PHF-tau. J Neuropathol Exp Neurol 55: 534–539PubMedCrossRefGoogle Scholar
  72. 72.
    Schmidt ML, Lee VM-Y, Hurtig H, Trojanowski JQ (1988) Properties of antigenic determinants that distinguish neurofibrillary tangles in progressive supranuclear palsy and Alzheimer’s disease. 59: 460–466Google Scholar
  73. 73.
    Smith TW, Lippa CF, de Girolami U (1992) Immunocytochemical study of ballooned neurons in cortical degeneration with neuronal achromasia. Clin Neuropathol 11: 28–35PubMedGoogle Scholar
  74. 74.
    Spillantini MG, Murrell JR, Goedert M, Farlow MR, Klug A, Ghetti B (1998) Mutation in the tau gene in familial multisystem tauopathy with presenile dementia. Proc Natl Acad Sci (USA) 95: 7737–7741CrossRefGoogle Scholar
  75. 75.
    Spillantini MG, Bird TD, Ghetti B (1998) Frontotemporal dementia and Parkinsonism linked to chromosome 17: A new group of tauopathies. Brain Pathol 8: 387–402PubMedCrossRefGoogle Scholar
  76. 76.
    Steele JC, Richardson JC, Olszewski J (1964) Progressive supranuclear palsy: a heterogenous degeneration involving the brain stem basal ganglia and cerebellum with vertical gaze and pseudobulbar palsy nuchal dystonia and dementia. Arch Neurol 10: 333–339PubMedGoogle Scholar
  77. 77.
    Tagliavini F, Pilleri G, Bouras C, Constantinidis J (1984) The basal nucleus of Meynert in patients with progressive supranuclear palsy. Neurosci Lett 44: 37–42PubMedCrossRefGoogle Scholar
  78. 78.
    Tellez-Nagel I, Wisniewski HM (1973) Ultrastructure of neurofibrillary tangles in Steele-Richardson-Olszewski syndrome. Arch Neurol 29: 324–327PubMedGoogle Scholar
  79. 79.
    Terry RD (1963) The fine structure of neurofibrillary tangles in Alzheimer’s disease. J Neuropathol Exp Neurol 22: 629–642PubMedCrossRefGoogle Scholar
  80. 80.
    Tetrud JW, Golbe LI, Forno LS, Farmer PM (1996) Autopsy-proven progressive supranuclear palsy in two siblings. Neurology 46: 931–934PubMedGoogle Scholar
  81. 81.
    Vermersch P, Robitaille Y, Berneir L, Wattez A, Gauvreau D, Delacourte A (1994) Biochemical mapping of neurofibrillary degeneration in a case of progressive supranuclear palsy: evidence for general cortical involvement. Acta Neuropathol 87: 572–577PubMedCrossRefGoogle Scholar
  82. 82.
    Wakabayashi K, Oyanagi K, Makifuchi T, Ikuta F, Honna A, Honna Y, Horikawa Y, Tokiguche S (1994) Corticobasal degeneration: etiopathological significance of the cytoskeletal alterations. Acta Neuropathol 87: 545–553PubMedCrossRefGoogle Scholar
  83. 83.
    Yagishita S, Itoh Y, Amano N, Nakano T, Saitoh A (1979) Ultrastructure of neurofibrillary tangles in progressive supranuclear palsy. Acta Neuropathol 48: 27–30PubMedCrossRefGoogle Scholar
  84. 84.
    Yamada T, Calne DB, Akiyama H, McGeer EG, McGeer PL (1993) Further observations on tau-positive glia in the brains with progressive supranuclear palsy. Acta Neuropathol 85: 308–315PubMedCrossRefGoogle Scholar
  85. 85.
    Yamada T, McGeer PL, McGeer EG (1992) Appearance of paired nucleated tau-positive glia in patients with progressive supranuclear palsy brain tissue. Neurosci Lett 135: 99–102PubMedCrossRefGoogle Scholar

Copyright information

© Steinkopff Verlag 1999

Authors and Affiliations

  1. 1.Department of PathologyMayo Clinic JacksonvilleJacksonvilleUSA

Personalised recommendations