Advertisement

Journal of Genetics

, 98:95 | Cite as

Language impairment in primary progressive aphasia and other neurodegenerative diseases

  • D. R. Rahul
  • R. Joseph PonniahEmail author
Review Article
First Online:

Abstract

Primary progressive aphasia (PPA) is a progressive neurodegenerative disease that disrupts the language capacity of an individual by selectively affecting the language network of brain. Although aphasic literature is replete with reports of brain damage responsible for various types of PPA, it does not provide a comprehensive understanding of whether PPA is an independent pathological condition or an atypical syndrome of neurodegenerative diseases (NDD). To address this ambiguity, we provide a detailed description of PPA, its variants and their brain anatomy. Subsequently, we unravel the relationship between PPA and NDDs like Alzheimer’s, Parkinson’s and Dyslexia. To substantiate the relationship further, we also provide a brief account of their genetic aetiology. In the final section, we offer an exhaustive approach towards the treatment of PPA by combining the existing language therapies with clinical and pharmacological interventions.

Keywords

primary progressive aphasia aphasia Alzheimer Parkinson dyslexia GRN gene 
This is a preview of subscription content, log in to check access.

References

  1. Adlam A. L. R., Bozeat S., Arnold R., Watson P. and Hodges J. R. 2006 Semantic knowledge in mild cognitive impairment and mild Alzheimer’s disease. Cortex 42, 675–684.PubMedGoogle Scholar
  2. Alladi S., Xuereb J., Bak T., Nestor P., Knibb J., Patterson K. et al. 2007 Focal cortical presentations of Alzheimer’s disease. Brain 130, 2636–2645.PubMedGoogle Scholar
  3. Auclair-Ouellet N., Lieberman P. and Monchi O. 2017 Contribution of language studies to the understanding of cognitive impairment and its progression over time in Parkinson’s disease. Neurosci. Biobehav. Rev. 80, 657–672.PubMedGoogle Scholar
  4. Barnish M. S., Horton S. M. C., Butterfint Z. R., Clark A. B., Atkinson R. A. and Deane K. H. O. 2017 Speech and communication in Parkinson’s disease: a cross-sectional exploratory study in the UK. BMJ Open 7, e014642.PubMedPubMedCentralGoogle Scholar
  5. Berndt R., Haendiges A. and Mitchum C. 2005 Orthographic effects in the word substitutions of aphasic patients: an epidemic of right neglect dyslexia? Brain Lang. 93, 55–63.PubMedGoogle Scholar
  6. Binney R. J., Henry M. L., Babiak M., Pressman P. S., Santos-Santos M. A., Narvid J. et al. 2016 Reading words and other people: a comparison of exception word, familiar face and affect processing in the left and right temporal variants of primary progressive aphasia. Cortex 82, 147–163.PubMedPubMedCentralGoogle Scholar
  7. Blair M., Marczinski C. A., Davis-Faroque N. and Kertesz A. 2007 A longitudinal study of language decline in Alzheimer’s disease and frontotemporal dementia. J. Int. Neuropsychol. Soc. 13, 237–245.PubMedGoogle Scholar
  8. Boeve B. F. and Hutton M. 2008 Refining frontotemporal dementia with parkinsonism linked to chromosome 17: introducing FTDP-17 (MAPT) and FTDP-17 (PGRN). Arch. Neurol. 65, 460–464.PubMedPubMedCentralGoogle Scholar
  9. Boggio P. S., Khoury L. P., Martins D. C. S., Martins O. E. M. S., de Macedo E. C. and Fregni F. 2009 Temporal cortex direct current stimulation enhances performance on a visual recognition memory task in Alzheimer disease. J. Neurol. Neurosurg. Psychiatry 80, 444–447.PubMedGoogle Scholar
  10. Boggio P. S., Valasek C. A., Campanhã C., Giglio A. C. A., Baptista N. I., Lapenta O. M. et al. 2011 Non-invasive brain stimulation to assess and modulate neuroplasticity in Alzheimer’s disease. Neuropsychol. Rehabil. 21, 703–716.PubMedGoogle Scholar
  11. Brambati S. M., Ogar J., Neuhaus J., Miller B. L. and Gorno-Tempini M. L. 2009. Reading disorders in primary progressive aphasia: a behavioral and neuroimaging study. Neuropsychologia 47, 1893–1900.PubMedPubMedCentralGoogle Scholar
  12. Chartier-Harlin M.-C., Dachsel J. C., Vilariño-Güell C., Lincoln S. J., Leprêtre F., Hulihan M. M. et al. 2011 Translation initiator EIF4G1 mutations in familial Parkinson disease. Am. J. Hum. Genet. 89, 398–406.PubMedPubMedCentralGoogle Scholar
  13. Chertkow H., Whatmough C., Saumier D. and Duong A. 2008 Cognitive neuroscience studies of semantic memory in Alzheimer’s disease. Prog. Brain Res. 169, 393–407.PubMedGoogle Scholar
  14. Chiacchio L., Grossi D., Stanzione M. and Trojano L. 1993 Slowly progressive aphasia associated with surface dyslexia. Cortex 29, 145–152.PubMedGoogle Scholar
  15. Clark D. G., Mendez M. F., Farag E. and Vinters H. V. 2003 Clinicopathologic case report: progressive aphasia in a 77-Year-Old Man. J. Neuropsychiatry Clin. Neurosci. 15, 231–238.PubMedGoogle Scholar
  16. Coppola G., Chinnathambi S., Lee J. J., Dombroski B. A., Baker M. C., Soto-Ortolaza. et al. 2012 Evidence for a role of the rare p.A152T variant in MAPT in increasing the risk for FTD-spectrum and Alzheimer’s diseases. Hum. Mol. Genet. 21, 3500–3512.PubMedPubMedCentralGoogle Scholar
  17. Cotelli M., Manenti R., Brambilla M., Petesi M., Rosini S., Ferrari C. et al. 2014 Anodal tDCS during face-name associations memory training in Alzheimer’s patients. Front. Aging Neurosci. 6, 38.PubMedPubMedCentralGoogle Scholar
  18. Croot K., Hodges J. R., Xuereb J. and Patterson K. 2000 Phonological and articulatory impairment in Alzheimer’s disease: a case series. Brain Lang. 75, 277–309.PubMedGoogle Scholar
  19. de Jong S., Chepelev I., Janson E., Strengman E., van den Berg L. H., Veldink J. H. and Ophoff R. A. 2012 Common inversion polymorphism at 17q21.31 affects expression of multiple genes in tissue-specific manner. BMC Genomics 13, 458.PubMedPubMedCentralGoogle Scholar
  20. Deffenbacher K. E., Kenyon J. B., Hoover D. M., Olson R. K., Pennington B. F., DeFries J. C. et al. 2004 Refinement of the 6p21.3 quantitative trait locus influencing dyslexia: linkage and association analyses. Hum. Genet. 115, 128–138.PubMedGoogle Scholar
  21. Deramecourt V., Lebert F., Debachy B., Mackowiak-Cordoliani M. A., Bombois S., Kerdraon O. et al. 2010 Prediction of pathology in primary progressive language and speech disorders. Neurology 74, 42–49.PubMedGoogle Scholar
  22. Desikan R. S., Witoelar A., Sharma M., McEvoy L. K., Holland D., Brewer J. B. et al. 2015 Genetic overlap between Alzheimer’s disease and Parkinson’s disease at the MAPT locus. Mol. Psychiatry 20, 1588–1595.PubMedPubMedCentralGoogle Scholar
  23. Deters K. D., Nho K., Risacher S. L., Kim S., Ramanan V. K., Crane P. K. et al. 2017 Genome-wide association study of language performance in Alzheimer’s disease. Brain Lang. 172, 22–29.PubMedPubMedCentralGoogle Scholar
  24. Doherty K. M., Rohrer J. D., Lees A. J., Holton J. L. and Warren J. 2013 Primary progressive aphasia with parkinsonism. Mov. Disord. 28, 741–746.PubMedPubMedCentralGoogle Scholar
  25. Fang Y. Q., Mao F., Zhu M. J. and Li X. H. 2019 Compound heterozygous mutations in PARK2 causing early-onset Parkinson disease: a case report. Medicine 98, e14228.PubMedPubMedCentralGoogle Scholar
  26. Ferrucci R., Mameli F., Guidi I., Mrakic-Sposta S., Vergari M., Marceglia S. et al. 2008 Transcranial direct current stimulation improves recognition memory in Alzheimer disease. Neurology 71, 493–498.PubMedGoogle Scholar
  27. Fridriksson J., Richardson J. D., Baker J. M. and Rorden C. 2011 Transcranial direct current stimulation improves naming reaction time in fluent aphasia:a double-blind, sham-controlled study. Stroke 42, 819–821.PubMedGoogle Scholar
  28. Galante E., Tralli A., Zuffi M. and Avanzi S. 2000 Primary progressive aphasia: a patient with stress assignment impairment in reading aloud. Neurol. Sci. 21, 39–48.PubMedGoogle Scholar
  29. Garrard P., Ralph M. A. L., Watson P. C., Powis J., Patterson K. and Hodges J. R. 2001 Longitudinal profiles of semantic impairment for living and nonliving concepts in dementia of Alzheimer’s type. J. Cogn. Neurosci. 13, 892–909.PubMedGoogle Scholar
  30. Gordon E., Rohrer J. D. and Fox N. C. 2016 Advances in neuroimaging in frontotemporal dementia. J. Neurochem. 138, 193–210.PubMedGoogle Scholar
  31. Gorno-Tempini M. L., Dronkers N. F., Rankin K. P., Ogar J. M., Phengrasamy L., Rosen H. J. et al. 2004 Cognition and anatomy in three variants of primary progressive aphasia. Ann. Neurol. 55, 335–346.PubMedPubMedCentralGoogle Scholar
  32. Gorno-Tempini M. L., Brambati S. M., Ginex V., Ogar J., Dronkers N. F., Marcone A. et al. 2008 The logopenic/phonological variant of primary progressive aphasia. Neurology 71, 1227–1234.PubMedPubMedCentralGoogle Scholar
  33. Gorno-Tempini M. L., Hillis A. E., Weintraub S., Kertesz A., Mendez M., Cappa S. F. et al. 2011 Classification of primary progressive aphasia and its variants. Neurology 76, 1006–1014.PubMedPubMedCentralGoogle Scholar
  34. Greene J. D. W., Patterson K., Xuereb J. and Hodges J. R. 1996 Alzheimer disease and nonfluent progressive aphasia. Arch Neurol. 53, 1072–1078.PubMedGoogle Scholar
  35. Henry M. L., Meese M. V., Truong S., Babiak M. C., Miller B. L. and Gorno-Tempini M. L. 2013 Treatment for apraxia of speech in nonfluent variant primary progressive aphasia. Behav. Neurol. 26, 77–88.PubMedPubMedCentralGoogle Scholar
  36. Hillis A. E., Tuffiash E., Wityk R. J. and Barker P. B. 2002 Regions of neural dysfunction associated with impaired naming of actions and objects in acute stroke. Cogn. Neuropsychol. 19, 523–534.PubMedGoogle Scholar
  37. Hillis A. E., Kleinman J. T., Newhart M., Heidler-Gary J., Gottesman R., Barker P. B. et al. 2006 Restoring cerebral blood flow reveals neural regions critical for naming. J. Neurosci. 26, 8069–8073.PubMedPubMedCentralGoogle Scholar
  38. Hu W. T., McMillan C., Libon D., Leight S., Forman M., Lee V. M. Y. et al. 2010 Multimodal predictors for Alzheimer disease in nonfluent primary progressive aphasia. Neurology 75, 595–602.PubMedPubMedCentralGoogle Scholar
  39. Ichimi N., Hashimoto M., Matsushita M., Yano H., Yatabe Y. and Ikeda M. 2013 The relationship between primary progressive aphasia and neurodegenerative dementia. East Asian Arch. Psychiatry 23, 120–125.PubMedGoogle Scholar
  40. Kertesz A., Martinez-Lage P., Davidson W. and Munoz D. G. 2000 The corticobasal degeneration syndrome overlaps progressive aphasia and frontotemporal dementia. Neurology 55, 1368–1375.PubMedGoogle Scholar
  41. Kim E. J., Park Y. E., Kim D. S., Ahn B. Y., Kim H. S., Chang Y. H. et al. 2011 Inclusion body myopathy with paget disease of bone and frontotemporal dementia linked to VCP p.Arg155Cys in a Korean family. Arch. Neurol. 68, 787–796.PubMedGoogle Scholar
  42. Lai C. S., Fisher S. E., Hurst J. A., Vargha-Khadem F. and Monaco A. P. 2001 A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413 519–523.PubMedGoogle Scholar
  43. Lanoiselée H. M., Nicolas G., Wallon D., Rovelet-Lecrux A., Lacour M., Rousseau S. et al. 2017 APP, PSEN1, and PSEN2 mutations in early-onset Alzheimer disease: a genetic screening study of familial and sporadic cases. PLoS Med. 14, e1002270.PubMedPubMedCentralGoogle Scholar
  44. Lewis F. M., Lapointe L. L., Murdoch B. E. and Chenery H. J. 1998 Language impairment in Parkinson’s disease. Aphasiology 12, 193–206.Google Scholar
  45. Liu L., Luo X. G., Dy C. L., Ren Y., Feng Y., Yu H. M. et al. 2015 Characteristics of language impairment in Parkinson’s disease and its influencing factors. Transl. Neurodegener. 4, 2.PubMedPubMedCentralGoogle Scholar
  46. Louwersheimer E., Keulen M. A., Steenwijk M. D., Wattjes M. P., Jiskoot L. C., Vrenken H. et al. 2016 Heterogeneous language profiles in patients with primary progressive aphasia due to Alzheimer’s disease. J. Alzheimer’s Dis. 51, 581–590.Google Scholar
  47. Machado T. H., Campanha A. C., Caramelli P. and Carthery-Goulart M. T. 2014 Brief intervention for agrammatism in primary progressive nonfluent aphasia: a case report. Dement. Neuropsychol. 8, 291–296.PubMedPubMedCentralGoogle Scholar
  48. Mahoney C. J., Beck J., Rohrer J. D., Lashley T., Mok K., Shakespeare T. et al. 2012 Frontotemporal dementia with the C9ORF72 hexanucleotide repeat expansion: clinical, neuroanatomical and neuropathological features. Brain 135, 736–750.PubMedPubMedCentralGoogle Scholar
  49. Mandelli M. L., Vitali P., Santos M., Henry M., Gola K., Rosenberg L. et al. 2016 Two insular regions are differentially involved in behavioral variant FTD and nonfluent/agrammatic variant PPA. Cortex 74, 149–157.PubMedGoogle Scholar
  50. Marshall J., Pring T. and Chiat S. 1998 Verb retrieval and sentence production in aphasia. Brain Lang. 63, 159–183.PubMedGoogle Scholar
  51. Matías-Guiu J. A., Cuetos F., Cabrera-Martín M. N., Valles-Salgado M., Moreno-Ramos T., Carreras J. L. et al. 2017 Reading difficulties in primary progressive aphasia in a regular language-speaking cohort of patients. Neuropsychologia 101, 132–140.PubMedGoogle Scholar
  52. McMonagle P., Blair M. and Kertesz A. 2006 Corticobasal degeneration and progressive aphasia. Neurology 67, 1444–1451.PubMedGoogle Scholar
  53. Meinzer M., Jähnigen S., Copland D. A., Darkow R., Grittner U., Avirame K. et al. 2014 Transcranial direct current stimulation over multiple days improves learning and maintenance of a novel vocabulary. Cortex 50, 137–147.PubMedGoogle Scholar
  54. Mesulam M., Wicklund A., Johnson N., Rogalski E., Léger G. C., Rademaker A. et al. 2008 Alzheimer and frontotemporal pathology in subsets of primary progressive aphasia. Ann. Neurol. 63, 709–719.PubMedPubMedCentralGoogle Scholar
  55. Mesulam M. M. 2001 Primary progressive aphasia. Ann. Neurol. 49, 425–432. PubMedGoogle Scholar
  56. Mesulam M. M. 2013 Primary progressive aphasia and the language network: The 2013 H. Houston Merritt Lecture. Neurology 81, 456–462.Google Scholar
  57. Mesulam M. M., Lalehzari N., Rahmani F., Ohm D., Shahidehpour R., Kim G. et al. 2019 Cortical cholinergic denervation in primary progressive aphasia with Alzheimer pathology. Neurology 92, e1580–e1588.PubMedGoogle Scholar
  58. Montembeault M., Brambati S. M., Joubert S., Boukadi M., Chapleau M., Laforce R. et al. 2017 Naming unique entities in the semantic variant of primary progressive aphasia and Alzheimer’s disease: towards a better understanding of the semantic impairment. Neuropsychologia 95, 11–20.PubMedGoogle Scholar
  59. Monte-Silva K., Kuo M. F., Hessenthaler S., Fresnoza S., Liebetanz D., Paulus W. et al. 2013 Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimul. 6, 424–432.PubMedGoogle Scholar
  60. Mummery C. J., Patterson K., Price C. J., Ashburner J., Frackowiak R. S. J. and Hodges J. R. 2000 A voxel-based morphometry study of semantic dementia: relationship between temporal lobe atrophy and semantic memory. Ann. Neurol. 47, 36–45.PubMedGoogle Scholar
  61. Obeso I., Casabona E., Bringas M. L., Álvarez L. and Jahanshahi M. 2012 Semantic and phonemic verbal fluency in Parkinson’s disease: influence of clinical and demographic variables. Behav. Neurol. 25, 111–118.PubMedPubMedCentralGoogle Scholar
  62. Owens T. E., Machulda M. M., Duffy J. R., Strand E. A., Clark H. M., Boland S. et al. 2018 Patterns of neuropsychological dysfunction and cortical volume changes in logopenic aphasia. J. Alzheimer’s Dis. 66, 1015–1025.Google Scholar
  63. Padovani A., Cosseddu M., Premi E., Archetti S., Papetti A., Agosti C. et al. 2010 The speech and language FOXP2 gene modulates the phenotype of frontotemporal lobar degeneration. J. Alzheimer’s Dis. 22, 923–931.Google Scholar
  64. Paternicó D., Premi E., Alberici A., Archetti S., Bonomi E., Gualeni V. et al. 2015 Dyslexia susceptibility genes influence brain atrophy in frontotemporal dementia. Neurol. Genet. 1, e24.PubMedPubMedCentralGoogle Scholar
  65. Peters F., Majerus S., Collette F., Degueldre C., Fiore G. D., Laureys S. et al. 2009 Neural substrates of phonological and lexicosemantic representations in Alzheimer’s disease. Hum. Brain Mapp. 30, 185–199.PubMedGoogle Scholar
  66. Pick A. Girling D. M. and Berrios G. E. 1994 On the relationship between senile cerebral atrophy and aphasia. Hist. Psychiatry 5, 542–547.Google Scholar
  67. Price C. J. and Mechelli A. 2005 Reading and reading disturbance. Curr. Opin. Neurobiol. 15, 231–238.PubMedGoogle Scholar
  68. Rahul D. R. and Ponniah R. J. 2019 Decoding the biology of language and its implications in language acquisition. J. Biosci. 44, 25.PubMedGoogle Scholar
  69. Reis J., Schambra H. M., Cohen L. G., Buch E. R., Fritsch B., Zarahn E. et al. 2009 Noninvasive cortical stimulation enhances motor skill acquisition over multiple days through an effect on consolidation. Proc. Natl. Acad. Sci.USA 106, 1590–1595.PubMedGoogle Scholar
  70. Renton A. E., Majounie E., Waite A., Simón-Sánchez J., Rollinson S., Gibbs J. R. et al. 2011 A hexanucleotide repeat expansion in C9ORF72 is the cause of chromosome 9p21-linked ALS-FTD. Neuron 72, 257–268.PubMedPubMedCentralGoogle Scholar
  71. Rogalski E., Cobia D., Harrison T. M., Wieneke C., Weintraub S. and Mesulam M. M. 2011 Progression of language decline and cortical atrophy in subtypes of primary progressive aphasia. Neurology 76, 1804–1810. PubMedPubMedCentralGoogle Scholar
  72. Rohrer J. D., Rossor M. N. and Warren J. D. 2012 Alzheimer’s pathology in primary progressive aphasia. Neurobiol. Aging 33, 744–752.PubMedPubMedCentralGoogle Scholar
  73. Rohrer J. D., Beck J., Plagnol V., Gordon E., Lashley T., Revesz T. et al. 2013 Exome sequencing reveals a novel partial deletion in the progranulin gene causing primary progressive aphasia. J. Neurol. Neurosurg. Psychiatry 84, 1411–1412.PubMedPubMedCentralGoogle Scholar
  74. Saunders A. M., Strittmatter W. J., Schemechel D., George-Hyslop P. H., Pericak-Vance M. A., Joo S. H. et al. 1993 Association of apolipoprotein E allele epsilon 4 with late-onset familial and sporadic Alzheimer’s disease. Neurology 43, 1467–1472.PubMedGoogle Scholar
  75. Scahill R. I., Schott J. M., Stevens J. M., Rossor M. N. and Fox N. C. 2002 Mapping the evolution of regional atrophy in Alzheimer’s disease: unbiased analysis of fluid-registered serial MRI. Proc. Natl. Acad. Sci. USA 99, 4703–4707.PubMedGoogle Scholar
  76. Schaeverbeke J., Evenepoel C., Bruffaerts R., Van Laere K., Bormans G., Dries E. et al. 2017 Cholinergic depletion and basal forebrain volume in primary progressive aphasia. NeuroImage Clin. 13, 271–279.PubMedGoogle Scholar
  77. Schliebs R. and Arendt T. 2006 The significance of the cholinergic system in the brain during aging and in Alzheimer’s disease. J. Neural. Transm. 113, 1625–1644.PubMedGoogle Scholar
  78. Schneider S. L., Thompson C. K. and Luring B. 1996 Effects of verbal plus gestural matrix training on sentence production in a patient with primary progressive aphasia. Aphasiology 10, 297–317.Google Scholar
  79. Singleton A. B., Farrer M., Johnson J., Singleton A., Hague S., Kachergus J. et al. 2003 \(\alpha \)-synuclein locus triplication causes Parkinson’s disease. Science 302, 841.PubMedGoogle Scholar
  80. Snowden J. S., Goulding P. J. and Neary D. 1989 Semantic dementia: a form of circumscribed cerebral atrophy. Behav. Neurol. 2, 167–182.Google Scholar
  81. Snowden J. S., Kindell J., Thompson J. C., Richardson A. M. T. and Neary D. 2012 Progressive aphasia presenting with deep dyslexia and dysgraphia. Cortex 48, 1234–1239.PubMedGoogle Scholar
  82. Sriganesh R. and Ponniah R. J. 2018 Genetics of language and its implications on language interventions. J. Genet. 97, 1485–1491.PubMedGoogle Scholar
  83. Stagg C. J. and Nitsche M. A. 2011 Physiological basis of transcranial direct current stimulation. Neuroscientist 17, 37–53.PubMedGoogle Scholar
  84. Tippett D. C., Hillis A. E. and Tsapkini K. 2015 Treatment of primary progressive aphasia. Curr. Treat Options Neurol. 17, 362.PubMedPubMedCentralGoogle Scholar
  85. Tomasino B., Marin D., Maieron M., D’Agostini S., Fabbro F., Skrap M. et al. 2015 Double-letter processing in surface dyslexia and dysgraphia following a left temporal lesion: a multimodal neuroimaging study. Cortex 73, 112–130.PubMedGoogle Scholar
  86. Troche M. S. and Altmann L. J. P. 2012 Sentence production in Parkinson disease: effects of conceptual and task complexity. Appl. Psycholinguist 33, 225–251.Google Scholar
  87. Tsapkini K., Frangakis C., Gomez Y., Davis C. and Hillis A. E. 2014 Augmentation of spelling therapy with transcranial direct current stimulation in primary progressive aphasia: preliminary results and challenges. Aphasiology 28, 1112–1130.PubMedPubMedCentralGoogle Scholar
  88. Valente E. M., Abou-Sleiman P. M., Caputo V., Harvey K., Gispert S. and Ali Z. 2004 Hereditary early-onset Parkinson’s disease caused by mutations in PINK1. Science 304, 1158–1160.PubMedPubMedCentralGoogle Scholar
  89. Van Langenhove T., van der Zee J., Gijselinck I., Engelborghs S., Vandenberghe R., Vandenbulcke M. et al. 2013 Distinct clinical characteristics of C9orf72 expansion carriers compared with GRN, MAPT, and nonmutation carriers in a flanders-belgian FTLD cohort. JAMA Neurol. 70, 365–373.PubMedGoogle Scholar
  90. Vilariño-Güell C., Wider C., Ross O. A., Dachsel J. C., Kachergus J. M., Lincoln S. J. et al 2011 VPS35 Mutations in Parkinson disease. Am. J. Hum. Genet. 89, 162–167.PubMedPubMedCentralGoogle Scholar
  91. Watt S., Jokel R. and Behrmann M. 1997 Surface Dyslexia in nonfluent progressive aphasia. Brain Lang. 56, 211–233.PubMedGoogle Scholar
  92. Zimprich A., Biskup S., Leitner P., Lichtner P., Farrer M., Lincoln S. et al. 2004 Mutations in LRRK2 cause autosomal-dominant parkinsonism with pleomorphic pathology. Neuron 44, 601–607.Google Scholar

Copyright information

© Indian Academy of Sciences 2019

Authors and Affiliations

  1. 1.National Institute of TechnologyTiruchirappalliIndia

Personalised recommendations

Cite article

Buy options