Review article Progressive supranuclear palsy revisited
I. Litvan,
Corresponding Author
I. Litvan
Neuropharmacology Unit, Defense & Veteran Head Injury Program, Henry M. Jackson Foundation; Medical Neurology Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
I. Litvan, Federal Building, Room 714, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 2089Z-913D, USASearch for more papers by this authorI. Litvan,
Corresponding Author
I. Litvan
Neuropharmacology Unit, Defense & Veteran Head Injury Program, Henry M. Jackson Foundation; Medical Neurology Branch, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland, USA
I. Litvan, Federal Building, Room 714, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 2089Z-913D, USASearch for more papers by this authorAbstract
Current understanding on the historic, epidemiologic, genetic, clinical, neuropathologic, neurochemical, diagnostic and therapeutic aspects of progressive supranuclear palsy (PSP) are revisited. In addition, new research directions are described.
References
- 1 STEELE JC, RICHARDSON JC, OLSZEWSKI J. Progressive supranuclear palsy. Arch Neurol 1964: 10: 333–59.
- 2 KRISTENSEN MO. Progressive supranuclear palsy - 20 years later. Acta Neurol Scand 1985: 71: 177–89.
- 3 POSEY WC. Analysis of the upward movements of the eyes. Ann Ophthalmol 1904: 13: 523–9.
- 4 SPILLER W. The importance in clinical diagnosis of paralysis of associated movements of the eyeballs (Blick-Laehmung) especially of upward and downward associated movements. J Nerv Ment Dis 1905: 32: 417–48, 497-530.
- 5 JANISCHEWSKY A. Un cas de maladie de Parkinson avec syndrome pseudobulbaire et pseudo-ophthalmoplegique: quelque considerations sur la pathogenie de cette maladie. Rev Neurol (Paris) 1909: 17: 831–2.
- 6 ALAJOUANINE T, DELAFONTAINE P, LACAN J. Fixite du regard par hypertonie, predominant dans le sens vertical, avec conservation des mouvements automatico-reflexes, aspect special de syndrome de Parinaud par hypertonie associee a un syndrome extrapyramidal avec troubles pseudo-bulbaires. Rev Neurol (Paris) 1926: 33: 410–18.
- 7 CORNIL L, KISSEL P. Syndrome extrapyramidal avec para-lysie vertical du regard et conservation des mouvements automatico-reflexes. Remarques sur les synergies oculo-palpebrales du syndrome de Parinaud. Rev Neurol (Paris) 1929: 36: 1189–91.
- 8 FRANCAIS H, VERNOTTE S. Syndrome de Parinaud associe a un syndrome de rigidite extrapyramidale. Rev Otol Neurol Ophthalmol 1932: 10: 739–41.
- 9 CHAVANY JA, VAN BOGAERT L, GODLEWSKI S. Sur un syndrome de rigidite a predominance axiale, avec perturbation des automatismes oculo-palbebraux D'origine encephalitique. La Presse Medicale 1951: 59: 958–62.
- 10 SIDEROWF AD, GALETTA SL, HURTIG HI, Liu GT. Posey, Spiller and progressive supranuclear palsy: an incorrect attribution. Mov Disord 1998: 13: 170–4.
- 11 STACY M, JANKOVIC J. Differential diagnosis of Parkinson's disease and the parkinsonism plus syndromes. Neurol Clin 1992: 10: 341–59.
- 12 BOWER JH, MARAGANORE DM, MCDONNELL SK, ROCCA WA. Incidence of progressive supranuclear palsy and multiple system atrophy in Olmstead County, Minnesota, 1976 to 1990. Neurology 1997: 49: 1284–8.
- 13 GOLBE LI, DAVIS PH, SCHOENBERG BS, DUVOISIN RC. Prevalence and natural history of progressive supranuclear palsy. Neurology 1988: 38: 1031–4.
- 14 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.
- 15 LITVAN I, MANGONE CA, MCKEE A et al. Natural history of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) and clinical predictors of survival: a clinicopathological study. J Neurol Neurosurg Psychiatry 1996: 60: 615–20.
- 16 LITVAN I, AOID Y, JANKOVIC J et al. Accuracy of clinical criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome). Neurology 1996: 46: 922–30.
- 17 LEES AJ. The Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Mov Disord 1987: 2: 272–87.
- 18 BLIN J, BARON JC, DUBOIS B et al. Positron emission tomography study in progressive supranuclear palsy. Brain hypometabolic pattern and clinicometabolic correlations. Arch Neurol 1990: 47: 747–52.
- 19 GOLBE LI, DAVIS PH. Progressive supranuclear palsy. In: J JANKOVIC, E TOLOSA, eds. Parkinson's disease and movement disorders. Baltimore : Williams and Wilkins, 1993: 145–61.
- 20 SANTACRUZ P, UTTL B, LITVAN I, GRAFMAN J. Progressive supranuclear palsy: A survey of disease course. Neurology 1998: 50: 1637–47.
- 21 DANIEL SE, DE BRUIN VMS, LEES AJ. The clinical and pathological spectrum of Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy): a reappraisal. Brain 1995: 118: 759–70.
- 22 BEN-SHLOMO Y, MARMOT MG. Survival and cause of death in a cohort of patients with parkinsonism: possible clues to aetiology J Neurol Neurosurg Psychiatry 1995: 58: 293–9.
- 23 OHARA S, KONDO K, MORITA H, MARUYAMA K, IKEDA S, YANAGISAWA N. Progressive supranuclear palsy-like syndrome in two siblings of a consanguineous marriage. Neurology 1992: 42: 1009–14.
- 24 BROWN J, LANTOS P, STRATTON M, ROQUES P, ROSSOR M. Familial progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 1993: 56: 473–6.
- 25 GAZELY S, MAGLTRE J. Familial progressive supranuclear palsy [abstract]. Brain Pathol 1994: 4: 534.
- 26 DE YEBENES JG, SARASA JL, DANIEL SE, LEES AJ. Familial progressive supranuclear palsy: description of a pedigree and review of the literature. Brain 1995: 118: 1095–103.
- 27 TETRUD JW, GOLBE LI, FORNO LS, FARMER PM. Autopsy-proven progressive supranuclear palsy in two siblings. Neurology 1996: 46: 931–4.
- 28 HIGGINS JJ, LITVAN I, PHO LT, LI W, NEE LE. Progressive supranuclear palsy is a recessive disorder in linkage disequilibrium with the tau and not the alpha-synuclein gene. Neurology 1998: 50: 270–3.
- 29 CONRAD C, ANDREADIS A, TROJANOWSKI JQ et al. Genetic evidence for the involvement of tau in progressive supranuclear palsy. Ann Neurol 1997: 41: 277–81.
- 30 TABATON M, ROLLERI M, MASTURZO P et al. Apolipoprotein E epsilon 4 allele frequency is not increased in progressive supranuclear palsy. Neurology 1995: 45: 1764–5.
- 31 ARAI H, HIGUCHI S, MURAMATSU T, MATSUSHITA S, ITABASHI S, SASAKI H. Lack of association of apolipoprotein E epsilon 4 allele with progressive supranuclear palsy [letter]. Neurodegeneration 1996: 5: 194–5.
- 32 LITVAN I, SAUNDERS AM. Apolipoprotein E epsilon 4 allele does not affect the onset or symptom severity in progressive supranuclear palsy [letter]. Arch Neurol 1998: 52: 752–4.
- 33 SAUNDERS AM, HULETTE O, WELSH-BOHMER KA et al. Specificity, sensitivity, and predictive value of apolipo-protein-E genotyping for sporadic Alzheimer's disease. Lancet 1996: 348: 90–3.
- 34 DAVIS PH, GOLBE LI, DUVOISIN RC, SCHOENBERG BS. Risk factors for progressive supranuclear palsy. Neurology 1988: 38: 1546–52.
- 35 GOLBE LI, RUBIN RS, CODY RP et al. Follow-up study of risk factors in progressive supranuclear palsy. Neurology 1996: 47: 148–54.
- 36 JELLINGER KA, BANCHER C. Neuropathology. In: I LITVAN, Y AGID, eds. Progressive supranuclear palsy: Clinical and research approaches. New York : Oxford University Press, 1992: 44–88.
- 37 AGID Y. Conclusions. In: I LITVAN, Y AGID, eds. Progressive supranuclear palsy: Clinical and research approaches. New York : Oxford University Press, 1992: 270–3.
- 38 LITVAN I, CHASE TN. Traditional and experimental therapeutic approaches. In: I LITVAN, Y AGID, ed. Progressive supranuclear palsy: Clinical and research approaches. New York : Oxford University Press, 1992: 254–69.
- 39 VII.LARES J, STRADA O, FAUCHEUX B, JAVOY-AGID F, AGID Y, HIRSCH EC. Loss of striatal high affinity NGF binding sites in progressive supranuclear palsy but not in Parkinson's disease. Neurosci Lett 1994: 182: 59–62.
- 40 YAMADA T, MCGEER P, MCGEER E. Appearance of paired nucleated, tau-positive glia in patients with progressive supranuclear palsy brain tissue. Neurosci Lett 1992: 135: 99–102.
- 41 YAMADA T, CALNE DB, AKIYAMA H, MCGEER EG, MCGEER PL. Further observations on tau-positive glia in the brains with progressive supranuclear palsy. Acta Neuropathol (Berl) 1993: 85: 308–15.
- 42 FEANY MB, DICKSON DW. Neurodegenerative disorders with extensive tau pathology: a comparative study and review. Ann Neurol 1996: 40: 139–48.
- 43 Di MONTE DA, HARATI Y, JANKOVTC J, SANDY MS, JEWELL SA, LANGSTON JW. Muscle mitochondrial ATP production in progressive supranuclear palsy. J Neurochem 1994: 62: 1631–4.
- 44 TEDESCHI G, LITVAN I, BONAVITA S et al. Proton magnetic resonance spectroscopic imaging in progressive supranuclear palsy, Parkinson's disease and corticobasal degeneration. Brain 1997: 120: 1541–52.
- 45 DAVIE CA, BARKER GJ, MACHADO C, MILLER DH, LEES AJ. H Magnetic resonance spectroscopy in Steele-Richardson-Olszewski syndrome. Mov Disord [Abstract] 1997: 12: 270.
- 46 FEDERICO F, SIMONE IL, LUCIVERO V et al. Proton magnetic resonance spectroscopy in Parkinson's disease and progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 1997: 62: 239–42.
- 47 MAHER ER, LEES AJ. The clinical features and natural history of the Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology 1986: 36: 1005–8.
- 48 VIDAILHET M, RIVAUD S, GOUIDER-KHOUJA N et al. Eye movements in parkinsonian syndromes. Ann Neurol 1994: 35: 420–6.
- 49 LITVAN I, AGID Y, CALNE D et al. Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome). Report of the NINDS-SPSP International Workshop. Neurology 1996: 47: 1–9.
- 50 DUBAS F, GRAY F, ESCOUROLLE R. Steele-Richardson-Olszewski disease without ophthalmoplegia. Six clinico-anatomic cases. Rev Neurol (Paris) 1983: 139: 407–16.
- 51 DE BRUIN VM, LEES AJ, DANIEL SE. Diffuse Lewy body disease presenting with supranuclear gaze palsy, parkinsonism, and dementia: a case report. Mov Disord 1992: 7: 355–8.
- 52 AMARENCO P, ROULLET E, HANNOUN L, MARTEAU R. Progressive supranuclear palsy as the sole manifestation of systemic Whipple's disease treated with pefloxacine [letter]. J Neurol Neurosurg Psychiatry 1991: 54: 1121–2.
- 53 DE BRUIN VM, LEES AJ. Subcortical neurofibrillary degeneration presenting as Steele-Richardson-Olszewski and other related syndromes: a review of 90 pathologically verified cases. Mov Disord 1994: 9: 381–9.
- 54 TANIGAWA A, KOMIYAMA A, HASEGAWA O. Truncal muscle tonus in progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 1998: 64: 190–6.
- 55 KLUIN KJ, FOSTER NL, BERENT S, GILMAN S. Perceptual analysis of speech disorders in progressive supranuclear palsy. Neurology 1993: 43: 563–6.
- 56 LITVAN I, SASTRY N, SONIES BC. Characterizing swallowing abnormalities in progressive supranuclear palsy. Neurology 1997: 48: 1654–62.
- 57 GRAFMAN J, LITVAN I, GOMEZ C, CHASE TN. Frontal lobe function in progressive supranuclear palsy. Arch Neurol 1990: 47: 553–8.
- 58 PILLON B, DUBOIS B, LHERMITTE F, AGID Y Heterogeneity of cognitive impairment in progressive supranuclear palsy, Parkinson's disease, and Alzheimer's disease. Neurology 1986: 36: 1179–85.
- 59 PILLON B, DUBOIS B, PLOSKA A, AGID Y. Severity and specificity of cognitive impairment in Alzheimer's, Huntington's, and Parkinson's diseases and progressive supranuclear palsy. Neurology 1991: 41: 634–43.
- 60 PILLON B, BLIN J, VIDAILHET M et al. The neuropsychological pattern of corticobasal degeneration: comparison with progressive supranuclear palsy and Alzheimer's disease. Neurology 1995: 45: 1477–83.
- 61 LITVAN I, MEGA MS, CUMMINGS JL, FAIRBANKS L. Neuro-psychiatric aspects of progressive supranuclear palsy. Neurology 1997: 47: 1184–9.
- 62 CAMBIER J, MASSON M, VIADER F, LIMODIN J, STRUBE A. Frontal syndrome of progressive supranuclear palsy. Rev Neurol (Paris) 1985: 141: 528–36.
- 63 MAHER ER, SMITH EM, LEES AJ. Cognitive deficits in the Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). J Neurol Neurosurg Psychiatry 1985: 48: 1234–9.
- 64 PILLON B, GOUIDER-KHOUJA N, DEWEER B et al. Neuropsychological pattern of striatonigral degeneration: comparison with Parkinson's disease and progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 1995: 58: 174–9.
- 65 ROBBINS TW, JAMES M, OWEN AM et al. Cognitive deficits in progressive supranuclear palsy, Parkinson's disease, and multiple system atrophy in tests sensitive to frontal lobe dysfunction. J Neurol Neurosurg Psychiatry 1994: 57: 79–88.
- 66 COLLINS SJ, AHLSKOG JE, PARISI JE, MARAGANORE DM. Progressive supranuclear palsy: neuropathologically based diagnostic criteria. J Neurol Neurosurg Psychiatry 1995: 58: 167–73.
- 67 LITVAN I, CAMPBELL G, MANGONE CA et al. Which clinical features differentiate progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome) from related disorders? A clinicopathological study. Brain 1997: 120: 65–74.
- 68 HOEHN MM, YAHR MD. Parkinsonism: onset, progression, and mortality. Neurology 1967: 17: 427–42.
- 69 LEIGUARDA RC, PRAMSTALLER PP, MERELLO M, STARKSTEIN S, LEES AJ, MARSDEN CD. Apraxia in Parkinson's disease, progressive supranuclear palsy, multiple system atrophy and neuroleptic-induced parkinsonism. Brain 1997: 120: 75–90.
- 70 SAKAKIBARA R, HATTORI T, TOJO M, YAMANISHI T, YASUDA K, HIRAYAMA K. Micturitional disturbance in progressive supranuclear palsy. J Auton Nerv Syst 1993: 45: 101–6.
- 71 WAKATSUKI A, TSUJIHATA M, MIYAKE O, ITO H, ITATANI H, UDAKA F. Vesicourethral function study and application of urinary alarm in progressive supranuclear palsy. Hinyokika Kiyo 1993: 39: 891–7.
- 72 NUWER M. Progressive supranuclear palsy despite normal eye movements. Arch Neurol 1981: 38: 784.
- 73 DUBAS F, GRAY F, ESCOUROLLE R. Maladie De Steele-Richardson-Olszewski Sans Ophtalmoplegie. Rev. Neurol 1983: 139: 407–16.
- 74 MASLIAH E, HANSEN L, QUIJADA S et al. Late onset dementia with argyrophilic grains and subcortical tangles or atypical progressive supranuclear palsy Ann Neurol 1991: 29: 389–96.
- 75 MATSUO H, TAKASHIMA H, KISHIKAWA M et al. Pure akinesia: an atypical manifestation of progressive supra nuclear palsy. J Neurol Neurosurg Psychiatry 1991: 54: 397–400.
- 76 MIZUSAWA H, MOCHIZUKI A, OHKOSHI N, YOSHIZAWA K, KANAZAWA I, IMAI H. Progressive supranuclear palsy presenting with pure akinesia. Adv Neurol 1993: 60: 618–21.
- 77 RILEY DE, FOGT N, LEIGH RJ. The syndrome of “pure akinesia” and its relationship to progressive supranuclear palsy. Neurology 1994: 44: 1025–9.
- 78 BERGERON C, POLLANEN MS, WEYER L, LANG AE. Cortical degeneration in progressive supranuclear palsy. A comparison with cortical-basal ganglionic degeneration. J Neuro-pathol Exp Neurol 1997: 56: 726–34.
- 79 DUVOISIN RC. Clinical Diagnosis. In: I LITVAN, Y AGID, eds. Progressive supranuclear palsy: Clinical and research approaches. New York : Oxford University Press, 1992: 15–33.
- 80 TOLOSA E, VALLDEORIOLA F, MARTI MJ. Clinical diagnosis and diagnostic criteria of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome). J Neural Transm Suppl 1994: 42: 15–31.
- 81 HAUW JJ, DANIEL SE, DICKSON D et al. Preliminary NINDS neuropathologic criteria for Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Neurology 1994: 44: 2015–19.
- 82 LITVAN I, HAUW JJ, BARTKO JJ et al. Validity and reliability of the preliminary NINDS neuropathologic criteria for progressive supranuclear palsy and .related disorders. J Neuropathol Exp Neurol 1996: 55: 97–105.
- 83 GEDDES JF, HUGHES AJ, LEES AJ, DANIEL SE. Pathological overlap in cases of parkinsonism associated with neurofibrillary tangles. A study of recent cases of postencephalitic parkinsonism and comparison with progressive supranuclear palsy and Guamanian parkinsonism-dementia complex. Brain 1993: 116: 281–302.
- 84 FEANY MB, MATTIACE LA, DICKSON DW. Neuropathologic overlap of progressive supranuclear palsy, Pick's disease and corticobasal degeneration. J Neuropathol Exp Neurol 1996: 55: 53–67.
- 85 VERMERSCH P, ROBITAILLE Y, BERNIER L, WATTEZ A, GAUVREAU D, DELACOURTE A. Biochemical mapping of neurofibrillary degeneration in a case of progressive supranuclear palsy: evidence for general cortical involvement. Acta Neuropathol (Berl) 1994: 87: 572–7.
- 86 FEANY MB, KSIEZAK-REDING H, LIU WK, VINCENT I, YEN SH, DICKSON DW. Epitope expression and hyperphosphory-lation of tau protein in corticobasal degeneration: differentiation from progressive supranuclear palsy. Acta Neuropathol (Berl) 1995: 90: 37–43.
- 87 BUEE-SCHERRER V, LEVEUGLE B, PERL DP, VERMESCH P, HOF PR, DELACOURTE A. Pathological tau proteins in postencephalitic parkinsonism: comparison with Alzheimer's disease and other degenerative disorders. Ann Neurol 1997: 42: 356–9.
- 88 KOMORI T, ARAI N, ODA M et al. Morphologic difference of neuropil threads in Alzheimer's disease, corticobasal degeneration and progressive supranuclear palsy: a morpho-metric study. Neurosci Lett 1997: 233: 89–92.
- 89 AGID Y, JAVOY-AGID F, RUBERG M et al. Progressive supranuclear palsy: anatomoclinical and biochemical considerations. Adv Neurol 1987: 45: 191–206.
- 90 MALESSA S, HIRSCH EC, CERVERA P, DUYCKAERTS C, AGID Y. Catecholaminergic systems in the medulla oblongata in parkinsonian syndromes: a quantitative immunohisto-chemical study in Parkinson's disease, progressive supranuclear palsy, and striatonigral degeneration. Neurology 1990: 40: 1739–43.
- 91 MALESSA S, HIRSCH EC, CERVERA P et al. Progressive supranuclear palsy: loss of choline-acetyltransferase-like immunoreactive neurons in the pontine reticular formation. Neurology 1991: 41: 1593–7.
- 92 MALESSA S, GAYMARD B, RIVAUD S et al. Role of pontine nuclei damage in smooth pursuit impairment of progressive supranuclear palsy: a clinical-pathologic study. Neurology 1994: 44: 716–21.
- 93 JUNCOS JL, HIRSCH EC, MALESSA S, DUYCKAERTS C, HERSH LB, AGID Y. Mesencephalic cholinergic nuclei in progressive supranuclear palsy. Neurology 1991: 41: 25–30.
- 94 LEVY R, RUBERG M, HERRERO MT et al. Alterations of GABAergic neurons in the basal ganglia of patients with progressive supranuclear palsy: an in situ hybridization study of GAD67 messenger RNA. Neurology 1995: 45: 127–34.
- 95 HOF PR, DELACOURTE A, BOURAS C. Distribution of cortical neurofibrillary tangles in progressive supranuclear palsy: a quantitative analysis of six cases. Acta Neuropathol (Berl) 1992: 84: 45–51.
- 96 VERNY M, DUYCKAERTS C, AGID Y HAUW JJ. The significance of cortical pathology in progressive supranuclear palsy - Clinicopathological data in 10 cases. Brain 1996: 119: 1123–36.
- 97 FUKUSHIMA-KUDO J, FUKUSHIMA K, TASHIRO K. Rigidity and dorsiflexion of the neck in progressive supranuclear palsy and the interstitial nucleus of Cajal. J Neurol Neurosurg Psychiatry 1987: 50: 1197–203.
- 98 DAUM I, SCHUGENS MM, SPIEKER S, POSER U, SCHONLE PW, BIRBAUMER N. Memory and skill acquisition in Parkinson's disease and frontal lobe dysfunction. Cortex 1995: 31: 413–32.
- 99 GRAFMAN J, WEINGARTNER H, NEWHOUSE PA et al. Implicit learning in patients with Alzheimer's disease. Pharmacopsychiatry 1990: 23: 94–101.
- 100 REVESZ T, SANGHA H, DANIEL SE. The nucleus raphe interpositus in the Steele-Richardson-Olszewski syndrome (progressive supranuclear palsy). Brain 1996: 119: 1137–43.
- 101 PIERROT-DESEILLIG.VY C, RIVAUD S, GAYMARD BRM, VERMERSCH A Cortical control of saccades. Ann Neurol 1995: 37: 557–67.
- 102 KARSON CN, BURNS RS, LEWITT PA, FOSTER NL, NEWMAN RP. Blink rates and disorders of movement. Neurology 1984: 34: 677–8.
- 103 GRAHAM DI, LANTOS PL. Greenfield's Neuropathology. London : Arnold, 1997.
- 104 HIRSCH EC, GRAYBIEL AM, DUYCKAERTS C, JAVOY-AGID F. Neuronal loss in the pedunculopontine tegmental nucleus in Parkinson disease and in progressive supranuclear palsy. Proc Natl Acad Sci USA 1987: 84: 5976–80.
- 105 ROGERS JD, BROGAN D, MIRRA SS. The nucleus basalis of Meynert in neurological disease: a quantitative morphological study. Ann Neurol 1985: 17: 163–70.
- 106 LITVAN I, GRAFMAN J, GOMEZ C, CHASE T. Memory impairment in patients with progressive supranuclear palsy. Arch Neurol 1989: 46: 767–767.
- 107 LITVAN I. Cognitive disturbances in progressive supranuclear palsy. J Neural Transm Suppl 1994: 42: 69–78.
- 108 PILLON B, DEWEER B, MICHON A, MALAPANI C, AGID Y, DUBOIS B. Are explicit memory disorders of progressive supranuclear palsy related to damage to striatofrontal circuits? Comparison with Alzheimer's, Parkinson's, and Huntington's diseases. Neurology 1994: 44: 1264–70.
- 109 ALBERT ML, FELDMAN RG, WILLIS AL. The “subcortical dementia” of progressive supranuclear palsy. J Neurol Neurosurg Psychiatry 1974: 37: 121–30.
- 110 BRANDEL JP, HIRSCH EC, MALESSA S, DUYCKAERTS C, CERVERA P, AGID Y Differential vulnerability of cholinergic projections to the mediodorsal nucleus of the thalamus in senile dementia of Alzheimer type and progressive supranuclear palsy. Neuroscience 1991: 41: 25–31.
- 111 BRAAK H, JELLINGER K, BRAAK E, BOHL J. Allocortical neurofibrillary changes in progressive supranuclear palsy. Acta Neuropathol (Berl) 1992: 84: 478–83.
- 112 MONTPLAISIR J, PETIT D, DECARY A et al. Sleep and quantitative EEG in patients with progressive supranuclear palsy. Neurology 1997: 49: 999–1003.
- 113 ALDRICH MS, FOSTER NL, WHITE RF, BLUEMLEIN L, PROKOPOWICZ G. Sleep abnormalities in progressive supranuclear palsy. Ann Neurol 1989: 25: 577–81.
- 114 DUBOIS B, PILLON B, LEGAULT F, AGID Y, LHERMITTE F. Slowing of cognitive processing in progressive supranuclear palsy. A comparison with Parkinson's disease. Arch Neurol 1988: 45: 1194–9.
- 115 JOHNSON RJ, LITVAN I, GRAFMAN J. Progressive supranuclear palsy: altered sensory processing leads to degraded cognition. Neurology 1991: 41: 1257–62.
- 116 JOHNSON RJ. Event-related brain potentials. In: I LITVAN, Y AGID, eds. Progressive supranuclear palsy: Clinical and Research Approaches. New York : Oxford University Press, 1992: 122–54.
- 117 LITVAN I. Progressive supranuclear palsy: staring into the past, moving into the future. The Neurologist 1998: 4: 13–20.
- 118 MASUCCI EF, BORTS FT, SMIRNIOTOPOULOS JG, KURTZKE JF, SCHELLINGER D. Thin-section CT of midbrain abnormalities in progressive supranuclear palsy. Am J Neuroradiol 1985: 6: 767–72.
- 119 SCHONFELD SM, GOLBE LI, SAGE JI, SAFER JN, DUVOISIN RC. Computed tomographic findings in progressive supranuclear palsy: correlation with clinical grade. Mov Disord 1987: 2: 263–78.
- 120 SAVOIARDO M, GIROTTI F, STRADA L, CICERI E. Magnetic resonance imaging in progressive supranuclear palsy and other parkinsonian disorders. J Neural Transm Suppl 1994: 42: 93–110.
- 121 YAMAUCHI H, FUKUYAMA H, NAGAHAMA Y et al. Atrophy of the corpus callosum, cognitive impairment, and cortical hypometabolism in progressive supranuclear palsy. Ann Neurol 1997: 41: 606–14.
- 122 D'ANTONA R, BARON JC, SAMSON Y et al. Subcortical dementia. Frontal cortex hypometabolism detected by positron tomography in patients with progressive supranuclear palsy. Brain 1985: 108: 785–99.
- 123 FOSTER NL, OILMAN 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.
- 124 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.
- 125 BLIN J, HORWITZ B, BARON J, AGID Y. Does frontal cortex hypometabolism in progressive supranuclear palsy result from subcortical dysfunction Eur J Neurol 1995: 1: 221–8.
- 126 DE VOLDER AG, FRANCARD J, LATERRE C et al. Decreased glucose utilization in the striatum and frontal lobe in probable striatonigral degeneration. Ann Neurol 1989: 26: 239–47.
- 127 FOSTER NL, GILMAN S, BERENT S et al. Progressive subcortical gliosis and progressive supranuclear palsy can have similar clinical and PET abnormalities. J Neurol Neurosurg Psychiatry 1992: 55: 707–13.
- 128 NAGAHAMA Y, FUKUYAMA H, TURJANSKI N et al. Cerebral glucose metabolism in corticobasal degeneration: comparison with progressive supranuclear palsy and normal controls. Mov Disord 1997: 12: 691–6.
- 129 BARON JC, MAZIERE B, LOC'H C et al. Loss of striatal [76Br] bromospiperone binding sites demonstrated by positron tomography in progressive supranuclear palsy. J Cereb Blood Flow Metab 1986: 6: 131–6.
- 130 LEENDERS KL, FRACKOWIAK RS, LEES AJ. Steele -Richardson-Olszewski syndrome. Brain energy metabolism, blood flow and fluorodopa uptake measured by positron emission tomography. Brain 1988: 111: 615–30.
- 131 BROOKS DJ, IBANEZ V, SAWLE GV et al. Striatal D2 receptor status in patients with Parkinson's disease, striatonigral degeneration, and progressive supranuclear palsy, measured with 11 C-raclopride and positron emission tomography. Ann Neurol 1992: 31: 184–92.
- 132 BROOKS DJ. PET studies in progressive supranuclear palsy. J Neural Transm Suppl 1994: 42: 119–34.
- 133 CALNE DB, LANGSTON JW, MARTIN WR et al. Positron emission tomography after MPTP: observations relating to the cause of Parkinson's disease. Nature 1985: 317: 246–8.
- 134 BURN DJ, RINNE JO, QUINN NP, LEES AJ, MARSDEN CD, BROOKS DJ. Striatal opioid receptor binding in Parkinson's disease, striatonigral degeneration and Steele-Richardson-Olszewski syndrome, A [u C]diprenorphine PET study. Brain 1995: 118: 951–8.
- 135 KOMPOLITI K, GOETZ CG, LITVAN I, JELLINGER K, VERNY M. Pharmacological therapy in progressive supranuclear palsy. Arch Neurol 1998, in press.
- 136 LITVAN I, GOMEZ C, ATACK JR et al. Physostigmine treatment of progressive supranuclear palsy. Ann Neurol 1989: 26: 404–7.
- 137 FOSTER NL, ALDRICH MS, BLUEMLEIN L, WHITE RF, BERENT S. Failure of cholinergic agonist RS-86 to improve cognition and movement in PSP despite effects on sleep. Neurology 1989: 39: 257–61.
- 138 LITVAN I, BLESA R, CLARK K et al. Pharmacological evaluation of the cholinergic system in progressive supranuclear palsy. Ann Neurol 1994: 36: 55–61.
- 139 HYMAN C, HOFER M, BARDE Y-A et al. BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 1991: 350: 230–2.
- 140 TOMAC A, LINDOVIST E, LIN L-F et al. Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 1995: 373: 335–9.
- 141 LINDVALL O, KOKAIA Z, BENGZON J, ELMER E, KOKAIA M. Neurotrophins and brain insults. TINS 1994: 17: 490–6.
- 142 SIUCIAK JA, BOYLAN C, FRITSCHE M, ALTAR CA, LINDSAY RM. BDNF increases monoaminergic activity in rat brain following intracerebroventricular or intra-parenchymal administration. Brain Res 1996: 710: 11–20.
- 143 ABIRU Y, NISHIO C, HATANAKA H. The survival of striatal cholinergic neurons cultured from postnatal 2-week-old rats is promoted by neurotrophins. Dev Brain Res 1996: 91: 260–7.
- 144 GASH DM, ZHANG Z, OVADIA A et al. Functional recovery in parkinsonian monkeys treated with GDNF. Nature 1996: 380: 252–5.
