View Item 

Show simple item record

H untington's D isease ( HD ): Degeneration of Select Nuclei, Widespread Occurrence of Neuronal Nuclear and Axonal Inclusions in the Brainstem

dc.contributor.authorRüb, Udoen_US
dc.contributor.authorHentschel, Matthiasen_US
dc.contributor.authorStratmann, Katharinaen_US
dc.contributor.authorBrunt, Ewouten_US
dc.contributor.authorHeinsen, Helmuten_US
dc.contributor.authorSeidel, Kayen_US
dc.contributor.authorBouzrou, Mohameden_US
dc.contributor.authorAuburger, Georgen_US
dc.contributor.authorPaulson, Henryen_US
dc.contributor.authorVonsattel, Jean‐paulen_US
dc.contributor.authorLange, Herwigen_US
dc.contributor.authorKorf, Horst‐werneren_US
dc.contributor.authorDunnen, Wilfreden_US
dc.date.accessioned2014-05-23T15:59:52Z
dc.date.available2015-06-01T15:48:46Zen_US
dc.date.issued2014-04en_US
dc.identifier.citationRüb, Udo ; Hentschel, Matthias; Stratmann, Katharina; Brunt, Ewout; Heinsen, Helmut; Seidel, Kay; Bouzrou, Mohamed; Auburger, Georg; Paulson, Henry; Vonsattel, Jean‐paul ; Lange, Herwig; Korf, Horst‐werner ; Dunnen, Wilfred (2014). " H untington's D isease ( HD ): Degeneration of Select Nuclei, Widespread Occurrence of Neuronal Nuclear and Axonal Inclusions in the Brainstem." Brain Pathology (3): 247-260.en_US
dc.identifier.issn1015-6305en_US
dc.identifier.issn1750-3639en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/106965
dc.description.abstractH untington's disease ( HD ) is a progressive polyglutamine disease that leads to a severe striatal and layer‐specific neuronal loss in the cerebral neo‐and allocortex. As some of the clinical symptoms (eg, oculomotor dysfunctions) suggested a degeneration of select brainstem nuclei, we performed a systematic investigation of the brainstem of eight clinically diagnosed and genetically confirmed HD patients. This post‐mortem investigation revealed a consistent neuronal loss in the substantia nigra, pontine nuclei, reticulotegmental nucleus of the pons, superior and inferior olives, in the area of the excitatory burst neurons for horizontal saccades, raphe interpositus nucleus and vestibular nuclei. Immunoreactive intranuclear neuronal inclusions were present in all degenerated and apparently spared brainstem nuclei and immunoreactive axonal inclusions were observed in all brainstem fiber tracts of the HD patients. Degeneration of brainstem nuclei can account for a number of less well‐understood clinical HD symptoms (ie, cerebellar, oculomotor and vestibular symptoms), while the formation of axonal aggregates may represent a crucial event in the cascades of pathological events leading to neurodegeneration in HD .en_US
dc.publisherWiley Periodicals, Inc.en_US
dc.publisherElsevieren_US
dc.subject.otherPolyglutamine Diseasesen_US
dc.subject.otherNeurodegenerationen_US
dc.subject.otherH Untington's Diseaseen_US
dc.subject.otherBrainstemen_US
dc.subject.otherAxonal Inclusionsen_US
dc.subject.otherPathoanatomyen_US
dc.titleH untington's D isease ( HD ): Degeneration of Select Nuclei, Widespread Occurrence of Neuronal Nuclear and Axonal Inclusions in the Brainstemen_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelNeurosciencesen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.description.peerreviewedPeer Revieweden_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/106965/1/bpa12115.pdf
dc.identifier.doi10.1111/bpa.12115en_US
dc.identifier.sourceBrain Pathologyen_US
dc.identifier.citedreferenceRüb U, Brunt ER, de Vos RA, Del Turco D, Del Tredici K, Gierga K et al ( 2004 ) Degeneration of the central vestibular system in spinocerebellar ataxia type 3 (SCA3) patients and its possible clinical significance. Neuropathol Appl Neurobiol 30: 402 – 414.en_US
dc.identifier.citedreferenceRiess O, Rüb U, Pastore A, Bauer P, Schöls L ( 2008 ) SCA3: neurological features, pathogenesis and animal models. Cerebellum 7: 125 – 137.en_US
dc.identifier.citedreferenceRubinsztein DC ( 2006 ) The roles of intracellular protein‐degradation pathways in neurodegeneration. Nature 443: 780 – 786.en_US
dc.identifier.citedreferenceRubinsztein DC, Carmichael J ( 2003 ) Huntington's disease: molecular basis of neurodegeneration. Expert Rev Mol Med 5: 1 – 21.en_US
dc.identifier.citedreferenceRüb U, Brunt ER, Deller T ( 2008 ) New insights into the pathoanatomy of spinocerebellar ataxia type 3 (Machado‐Joseph disease). Curr Opin Neurol 21: 111 – 116.en_US
dc.identifier.citedreferenceRüb U, Brunt ER, Gierga K, Schultz C, Paulson H, de Vos RA, Braak H ( 2003 ) The nucleus raphe interpositus in spinocerebellar ataxia type 3 (Machado‐Joseph disease). J Chem Neuroanat 25: 115 – 127.en_US
dc.identifier.citedreferenceRüb U, Brunt ER, Gierga K, Seidel K, Schultz C, Schöls L et al ( 2005 ) Spinocerebellar ataxia type 7 (SCA7): first report of a systematic neuropathological study of the brain of a patient with a very short expanded CAG‐repeat. Brain Pathol 15: 287 – 295.en_US
dc.identifier.citedreferenceRüb U, Bürk K, Timmann D, den Dunnen W, Seidel K, Brunt E et al ( 2012 ) Spinocerebellar ataxia type 1 (SCA1): new pathoanatomical and clinico‐pathological insights. Neuropathol Appl Neurobiol 38: 665 – 680.en_US
dc.identifier.citedreferenceRüb U, Heinsen H, Brunt ER, Landwehrmeyer B, Den Dunnen WF, Gierga K, Deller T ( 2009 ) The human premotor oculomotor brainstem system—can it help to understand oculomotor symptoms in Huntington's disease? Neuropathol Appl Neurobiol 35: 4 – 15.en_US
dc.identifier.citedreferenceRüb U, Hoche F, Brunt ER, Heinsen H, Seidel K, Del Turco D et al ( 2013 ) Degeneration of the cerebellum in Huntington's Disease (HD): possible relevance for the clinical picture and potential gateway to pathological mechanisms of the disease process. Brain Pathol 23: 165 – 177.en_US
dc.identifier.citedreferenceRüb U, Jen JC, Braak H, Deller T ( 2008 ) Functional neuroanatomy of the human premotor oculomotor brainstem nuclei: insights from postmortem and advanced in vivo imaging studies. Exp Brain Res 187: 167 – 180.en_US
dc.identifier.citedreferenceSapp E, Penney J, Young A, Aronin N, Vonsattel JP, Difiglia M ( 1999 ) Axonal transport of N‐terminal huntingtin suggests early pathology of corticostriatal projections in Huntington disease. J Neuropathol Exp Neurol 58: 165 – 173.en_US
dc.identifier.citedreferenceSchulte J, Littleton JT ( 2011 ) The biological function of the Huntingtin protein and its relevance to Huntington's disease pathology. Curr Trends Neurol 5: 65 – 78.en_US
dc.identifier.citedreferenceSeibenhener ML, Babu JR, Geetha T, Wong HC, Krishna NR, Wooten MW ( 2004 ) Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol Cell Biol 24: 8055 – 8068.en_US
dc.identifier.citedreferenceSeidel K, Brunt ER, de Vos RA, Dijk F, van der Want HJ, Rüb U, Den Dunnen WF ( 2009 ) The p62 antibody reveals various cytoplasmic protein aggregates in spinocerebellar ataxia type 6. Clin Neuropathol 28: 344 – 349.en_US
dc.identifier.citedreferenceSeidel K, Den Dunnen WF, Schultz C, Paulson H, Frank S, de Vos RA et al ( 2010 ) Axonal inclusions in spinocerebellar ataxia type 3. Acta Neuropathol 120: 449 – 460.en_US
dc.identifier.citedreferenceSeidel K, Siswanto S, Brunt ER, den Dunnen W, Korf HW, Rüb U ( 2012 ) Brain pathology of spinocerebellar ataxias. Acta Neuropathol 124: 1 – 21.en_US
dc.identifier.citedreferenceShaw G, Osborn M, Weber K ( 1981 ) An immunofluorescence microscopical study of the neurofilament triplet proteins, vimentin and glial fibrillary acidic protein within the adult rat brain. Eur J Cell Biol 26: 68 – 82.en_US
dc.identifier.citedreferenceShoulson I, Young AB ( 2011 ) Milestones in Huntington disease. Mov Disord 26: 1127 – 1133.en_US
dc.identifier.citedreferenceSieradzan KA, Mann DM ( 2001 ) The selective vulnerability of nerve cells in Huntington's disease. Neuropathol Appl Neurobiol 27: 1 – 21.en_US
dc.identifier.citedreferenceSieradzan KA, Mechan AO, Jones L, Wanker EE, Nukina N, Mann DM ( 1999 ) Huntington's disease intranuclear inclusions contain truncated, ubiquitinated huntingtin protein. Exp Neurol 156: 92 – 99.en_US
dc.identifier.citedreferenceSmithson KG, MacVicar BA, Hatton GI ( 1983 ) Polyethylene glycol embedding: a technique compatible with immunocytochemistry, enzyme histochemistry, histofluorescence and intracellular staining. J Neurosci Methods 7: 27 – 41.en_US
dc.identifier.citedreferenceThe Huntington's disease Collaborative Research Group ( 1993 ) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72: 971 – 983.en_US
dc.identifier.citedreferenceTrottier Y, Devys D, Imbert G, Saudou F, An I, Lutz Y et al ( 1995 ) Cellular localization of the Huntington's disease protein and discrimination of the normal and mutated form. Nat Genet 10: 104 – 110.en_US
dc.identifier.citedreferenceTrottier Y, Lutz Y, Stevanin G, Imbert G, Devys D, Cancel G et al ( 1995 ) Polyglutamine expansion as a pathological epitope in Huntington's disease and four dominant cerebellar ataxias. Nature 378: 403 – 406.en_US
dc.identifier.citedreferenceTruant R, Atwal R, Burtnik A ( 2006 ) Hypothesis: Huntingtin may function in membrane association and vesicular trafficking. Biochem Cell Biol 84: 912 – 917.en_US
dc.identifier.citedreferenceValera AG, Diaz‐Hernandez M, Hernandez F, Ortega Z, Lucas JJ ( 2005 ) The ubiquitin‐proteasome system in Huntington's disease. Neuroscientist 11: 583 – 594.en_US
dc.identifier.citedreferenceVonsattel JP ( 2008 ) Huntington disease models and human neuropathology: similarities and differences. Acta Neuropathol 115: 55 – 69.en_US
dc.identifier.citedreferenceVonsattel JP, Difiglia M ( 1998 ) Huntington disease. J Neuropathol Exp Neurol 57: 369 – 384.en_US
dc.identifier.citedreferenceVonsattel JP, Myers RH, Stevens TJ, Ferrante RJ, Bird ED, Richardson EP Jr ( 1985 ) Neuropathological classification of Huntington's disease. J Neuropathol Exp Neurol 44: 559 – 577.en_US
dc.identifier.citedreferenceVoogd J ( 2004 ) Cerebellum and precerebellar nuclei. In: The Human Nervous System, 2nd edn. G Paxinos, JK Mai (eds), pp. 321 – 392. Elsevier: San Diego.en_US
dc.identifier.citedreferenceWalker FO ( 2007a ) Huntington's disease. Semin Neurol 27: 143 – 150.en_US
dc.identifier.citedreferenceWalker FO ( 2007b ) Huntington's disease. Lancet 369: 218 – 228.en_US
dc.identifier.citedreferenceArrasate M, Finkbeiner S ( 2012 ) Protein aggregates in Huntington's disease. Exp Neurol 238: 1 – 11.en_US
dc.identifier.citedreferenceBecher MW, Kotzuk JA, Sharp AH, Davies SW, Bates GP, Price DL, Ross CA ( 1998 ) Intranuclear neuronal inclusions in Huntington's disease and dentatorubral and pallidoluysian atrophy: correlation between the density of inclusions and IT15 CAG triplet repeat length. Neurobiol Dis 4: 387 – 397.en_US
dc.identifier.citedreferenceBraak H, Braak E ( 1992 ) Allocortical involvement in Huntington's disease. Neuropathol Appl Neurobiol 18: 539 – 547.en_US
dc.identifier.citedreferenceBraak H, Rüb U, Del Tredici K ( 2003 ) Involvement of precerebellar nuclei in multiple system atrophy. Neuropathol Appl Neurobiol 29: 60 – 76.en_US
dc.identifier.citedreferenceBruyn GW, Bots GTAM, Dom R ( 1979 ) Huntington's chorea: current neuropathological status. Adv Neurol 23: 83 – 93.en_US
dc.identifier.citedreferenceBusse ME, Wiles CM, Rosser AE ( 2009 ) Mobility and falls in people with Huntington's disease. J Neurol Neurosurg Psychiatry 80: 88 – 90.en_US
dc.identifier.citedreferenceBüttner‐Ennever JA ( 2006 ) The extraocular motor nuclei: organization and functional neuroanatomy. Prog Brain Res 151: 95 – 125.en_US
dc.identifier.citedreferenceBüttner‐Ennever JA, Gerrits NM ( 2004 ) Vestibular system. In: The Human Nervous System, 2nd edn. G Paxinos, JK Mai (eds), pp. 1213 – 1240. Elsevier: San Diego.en_US
dc.identifier.citedreferenceBüttner‐Ennever JA, Horn AKE ( 2004 ) Reticular formation: eye movements, gaze, and blinks. In: The Human Nervous System, 2nd edn. G Paxinos, JK Mai (eds), pp. 479 – 510. Elsevier: San Diego.en_US
dc.identifier.citedreferenceDavies JE, Sarkar S, Rubinsztein DC ( 2007 ) The ubiquitin proteasome system in Huntington's disease and the spinocerebellar ataxias. BMC Biochem 8 ( Suppl. 1 ): S2.en_US
dc.identifier.citedreferenceDe Vos KJ, Grierson AJ, Ackerley S, Miller CC ( 2008 ) Role of axonal transport in neurodegenerative diseases. Annu Rev Neurosci 31: 151 – 173.en_US
dc.identifier.citedreferenceDen Dunnen WF ( 2013 ) Neuropathological diagnostic considerations in hyperkinetic movement disorders. Front Neurol 4: 7.en_US
dc.identifier.citedreferenceDickson DW, Braak H, Duda JE, Duyckaerts C, Gasser T, Halliday GM et al ( 2009 ) Neuropathological assessment of Parkinson's disease: refining the diagnostic criteria. Lancet Neurol 8: 1150 – 1157.en_US
dc.identifier.citedreferenceDifiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel JP, Aronin N ( 1997 ) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 277: 1990 – 1993.en_US
dc.identifier.citedreferenceDom R, Malfroid M, Baro F ( 1976 ) Neuropathology of Huntington's chorea. Studies of the ventrobasal complex of the thalamus. Neurology 26: 64 – 68.en_US
dc.identifier.citedreferenceDuyao M, Ambrose C, Myers R, Novelletto A, Persichetti F, Frontali M et al ( 1993 ) Trinucleotide repeat length instability and age of onset in Huntington's disease. Nat Genet 4: 387 – 392.en_US
dc.identifier.citedreferenceGil JM, Rego AC ( 2008 ) Mechanisms of neurodegeneration in Huntington's disease. Eur J Neurosci 27: 2803 – 2820.en_US
dc.identifier.citedreferenceGoedert M, Jakes R, Crowther RA, Cohen P, Vanmechelen E, Vandermeeren M, Cras P ( 1994 ) Epitope mapping of monoclonal antibodies to the paired helical filaments of Alzheimer's disease: identification of phosphorylation sites in tau protein. Biochem J 301 ( Pt 3 ): 871 – 877.en_US
dc.identifier.citedreferenceGourfinkel‐An I, Cancel G, Duyckaerts C, Faucheux B, Hauw JJ, Trottier Y et al ( 1998 ) Neuronal distribution of intranuclear inclusions in Huntington's disease with adult onset. Neuroreport 9: 1823 – 1826.en_US
dc.identifier.citedreferenceGrimbergen YA, Knol MJ, Bloem BR, Kremer BP, Roos RA, Munneke M ( 2008 ) Falls and gait disturbances in Huntington's disease. Mov Disord 23: 970 – 976.en_US
dc.identifier.citedreferenceGunawardena S, Goldstein LS ( 2005 ) Polyglutamine diseases and transport problems: deadly traffic jams on neuronal highways. Arch Neurol 62: 46 – 51.en_US
dc.identifier.citedreferenceGutekunst CA, Li SH, Yi H, Mulroy JS, Kuemmerle S, Jones R et al ( 1999 ) Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J Neurosci 19: 2522 – 2534.en_US
dc.identifier.citedreferenceHalliday G ( 2004 ) Substantia nigra and locus coeruleus. In: The Human Nervous System, 2nd edn. G Paxinos, JK Mai (eds), pp. 449 – 463. Elsevier: San Diego.en_US
dc.identifier.citedreferenceHarper PS ( 1992 ) The epidemiology of Huntington's disease. Hum Genet 89: 365 – 376.en_US
dc.identifier.citedreferenceHeinsen H, Rüb U, Bauer M, Ulmar G, Bethke B, Schüler M et al ( 1999 ) Nerve cell loss in the thalamic mediodorsal nucleus in Huntington's disease. Acta Neuropathol 97: 613 – 622.en_US
dc.identifier.citedreferenceHeinsen H, Rüb U, Gangnus D, Jungkunz G, Bauer M, Ulmar G et al ( 1996 ) Nerve cell loss in the thalamic centromedian‐parafascicular complex in patients with Huntington's disease. Acta Neuropathol 91: 161 – 168.en_US
dc.identifier.citedreferenceHeinsen H, Strik M, Bauer M, Luther K, Ulmar G, Gangnus D et al ( 1994 ) Cortical and striatal neurone number in Huntington's disease. Acta Neuropathol 88: 320 – 333.en_US
dc.identifier.citedreferenceHoche F, Seidel K, Brunt ER, Auburger G, Schöls L, Bürk K et al ( 2008 ) Involvement of the auditory brainstem system in spinocerebellar ataxia type 2 (SCA2), type 3 (SCA3) and type 7 (SCA7). Neuropathol Appl Neurobiol 34: 479 – 491.en_US
dc.identifier.citedreferenceHorn AK ( 2006 ) The reticular formation. Prog Brain Res 151: 127 – 155.en_US
dc.identifier.citedreferenceHuang Q, Figueiredo‐Pereira ME ( 2010 ) Ubiquitin/proteasome pathway impairment in neurodegeneration: therapeutic implications. Apoptosis 15: 1292 – 1311.en_US
dc.identifier.citedreferenceImarisio S, Carmichael J, Korolchuk V, Chen CW, Saiki S, Rose C et al ( 2008 ) Huntington's disease: from pathology and genetics to potential therapies. Biochem J 412: 191 – 209.en_US
dc.identifier.citedreferenceKoeppen AH ( 1989 ) The nucleus pontis centralis caudalis in Huntington's disease. J Neurol Sci 91: 129 – 141.en_US
dc.identifier.citedreferenceKoutcherov Y, Huang XF, Halliday G, Paxinos G ( 2004 ) Organization of human brain stem nuclei. In: The Human Nervous System, 2nd edn. G Paxinos, JK Mai (eds), pp. 267 – 320. Elsevier: San Diego.en_US
dc.identifier.citedreferenceKremer B, Weber B, Hayden MR ( 1992 ) New insights into the clinical features, pathogenesis and molecular genetics of Huntington disease. Brain Pathol 2: 321 – 335.en_US
dc.identifier.citedreferenceKremer HP, Roos RA, Dingjan GM, Bots GT, Bruyn GW, Hofman MA ( 1991 ) The hypothalamic lateral tuberal nucleus and the characteristics of neuronal loss in Huntington's disease. Neurosci Lett 132: 101 – 104.en_US
dc.identifier.citedreferenceKuemmerle S, Gutekunst CA, Klein AM, Li XJ, Li SH, Beal MF et al ( 1999 ) Huntington aggregates may not predict neuronal death in Huntington's disease. Ann Neurol 46: 842 – 849.en_US
dc.identifier.citedreferenceKuusisto E, Kauppinen T, Alafuzoff I ( 2008 ) Use of p62/SQSTM1 antibodies for neuropathological diagnosis. Neuropathol Appl Neurobiol 34: 169 – 180.en_US
dc.identifier.citedreferenceKuusisto E, Salminen A, Alafuzoff I ( 2001 ) Ubiquitin‐binding protein p62 is present in neuronal and glial inclusions in human tauopathies and synucleinopathies. Neuroreport 12: 2085 – 2090.en_US
dc.identifier.citedreferenceLange H, Thorner G, Hopf A, Schroder KF ( 1976 ) Morphometric studies of the neuropathological changes in choreatic diseases. J Neurol Sci 28: 401 – 425.en_US
dc.identifier.citedreferenceLange HW ( 1981 ) Quantitative changes of telencephalon, diencephalon, and mesencephalon in Huntington's chorea, postencephalitic, and idiopathic Parkinsonism. Verh Anat Ges 73: 923 – 925.en_US
dc.identifier.citedreferenceLange HW, Aulich A ( 1986 ) Die Hirnatrophie bei der Huntingtonschen Krankheit. In: Die Huntingtonsche Krankheit, 1st edn. H Oepen (ed.), pp. 25 – 41. Hippokrates Verlag: Stuttgart.en_US
dc.identifier.citedreferenceLasker AG, Zee DS ( 1997 ) Ocular motor abnormalities in Huntington's disease. Vision Res 37: 3639 – 3645.en_US
dc.identifier.citedreferenceLastres‐Becker I, Rüb U, Auburger G ( 2008 ) Spinocerebellar ataxia 2 (SCA2). Cerebellum 7: 115 – 124.en_US
dc.identifier.citedreferenceLeigh RJ, Newman SA, Folstein SE, Lasker AG, Jensen BA ( 1983 ) Abnormal ocular motor control in Huntington's disease. Neurology 33: 1268 – 1275.en_US
dc.identifier.citedreferenceLeigh RJ, Parhad IM, Clark AW, Buettner‐Ennever JA, Folstein SE ( 1985 ) Brainstem findings in Huntington's disease. Possible mechanisms for slow vertical saccades. J Neurol Sci 71: 247 – 256.en_US
dc.identifier.citedreferenceLi JY, Conforti L ( 2012 ) Axonopathy in Huntington's disease. Exp Neurol 246: 62 – 72.en_US
dc.identifier.citedreferenceMaat‐Schieman M, Roos R, Losekoot M, Dorsman J, Welling‐Graafland C, Hegeman‐Kleinn I et al ( 2007 ) Neuronal intranuclear and neuropil inclusions for pathological assessment of Huntington's disease. Brain Pathol 17: 31 – 37.en_US
dc.identifier.citedreferenceMaat‐Schieman ML, Dorsman JC, Smoor MA, Siesling S, van Duinen SG, Verschuuren JJ et al ( 1999 ) Distribution of inclusions in neuronal nuclei and dystrophic neurites in Huntington disease brain. J Neuropathol Exp Neurol 58: 129 – 137.en_US
dc.identifier.citedreferenceMargolis RL, Ross CA ( 2003 ) Diagnosis of Huntington disease. Clin Chem 49: 1726 – 1732.en_US
dc.identifier.citedreferenceMoore JK, Linthicum FH ( 2004 ) Auditory system. In: The Human Nervous System, 2nd edn. G Paxinos, JK Mai (eds), pp. 1241 – 1279. Elsevier: San Diego.en_US
dc.identifier.citedreferenceMyers RH ( 2004 ) Huntington's disease genetics. NeuroRx 1: 255 – 262.en_US
dc.identifier.citedreferenceOyanagi K, Takeda S, Takahashi H, Ohama E, Ikuta F ( 1989 ) A quantitative investigation of the substantia nigra in Huntington's disease. Ann Neurol 26: 13 – 19.en_US
dc.identifier.citedreferencePaulus W, Jellinger K ( 1991 ) The neuropathologic basis of different clinical subgroups of Parkinson's disease. J Neuropathol Exp Neurol 50: 743 – 755.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
bpa12115.pdf
Size:
1.392MB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.