Clinical and neuroanatomical signatures of tissue pathology in frontotemporal lobar degeneration

Brain

Volumn 134, Issue 9, 2011, Pages 2565-2581

  Rohrer, Jonathan D ^a   Lashley, Tammaryn ^a   Schott, Jonathan M ^a   Warren, Jane E ^b   Mead, Simon ^a   Isaacs, Adrian M ^a   Beck, Jonathan ^a   Hardy, John ^c   De Silva, Rohan ^c   Warrington, Elizabeth ^a   Troakes, Claire ^d   Al Sarraj, Safa ^e   King, Andrew ^e   Borroni, Barbara ^f   Clarkson, Matthew J ^a,g   Ourselin, Sebastien ^a,g   Holton, Janice L ^a   Fox, Nick C ^a   Revesz, Tamas ^a   Rossor, Martin N ^a   Warren, Jason D ^a   more..

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e KING'S COLLEGE HOSPITAL NHS FOUNDATION TRUST   (United Kingdom)

^f UNIVERSITY OF BRESCIA   (Italy)

^g UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

frontotemporal dementia; frontotemporal lobar degeneration; MRI; neural network; voxel based morphometry

Indexed keywords

FUSED IN SARCOMA PROTEIN; PROGRANULIN; PROTEIN; TAR DNA BINDING PROTEIN; TAU PROTEIN; UNCLASSIFIED DRUG;

ADULT; AMYGDALOID NUCLEUS; AMYLOID PLAQUE; ANOMIA; APATHY; ARTICLE; BRAIN ASYMMETRY; BRAIN ATROPHY; BRAIN FORNIX; BRAIN SIZE; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; CORTICOBASAL DEGENERATION; DISEASE COURSE; FEMALE; FRONTAL LOBE; FRONTAL VARIANT FRONTOTEMPORAL DEMENTIA; FRONTOTEMPORAL DEMENTIA; GENE MUTATION; GRAY MATTER; HALLUCINATION; HIPPOCAMPUS; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; INSULA; MALE; MILD COGNITIVE IMPAIRMENT; MOTOR NEURON DISEASE; NUCLEAR MAGNETIC RESONANCE IMAGING; ORBITAL CORTEX; PARKINSONISM; PICK PRESENILE DEMENTIA; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; PUTAMEN; RETROSPECTIVE STUDY; SEMANTIC DEMENTIA; TAUOPATHY; TEMPORAL CORTEX; THALAMUS; UNCINATE FASCICULUS; VOLUMETRY; VOXEL BASED MORPHOMETRY; WHITE MATTER;

EID: 80052923233     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awr198     Document Type: Article

References (81)

1. Acosta-Cabronero J, Patterson K, Fryer TD, Hodges JR, Pengas G, Williams GB, et al. Atrophy, hypometabolism and white matter abnormalities in semantic dementia tell a coherent story. Brain 2011; 134 (Pt 7): 2025-35.
2. Alzheimer A. Uber eigenartige Krankheitsfalle des Spateren Alters. Z Ges Neurol Psychiatr 1911; 4: 356-85.
3. Boeve BF, Lang AE, Litvan I. Corticobasal degeneration and its relationship to progressive supranuclear palsy and frontotemporal dementia. Ann Neurol 2003; 54 (Suppl. 5): S15-9. (Pubitemid 36760148)
4. Braak H, Alafuzoff I, Arzberger T, Kretzschmar H, Del Tredici K. Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathol 2006; 112: 389-404. (Pubitemid 44469160)
5. Cairns NJ, Bigio EH, Mackenzie IR, Neumann M, Lee VM, Hatanpaa KJ, et al. Consortium for Frontotemporal Lobar Degeneration. Neuropathologic diagnostic and nosologic criteria for frontotemporal lobar degeneration: consensus of the Consortium for Frontotemporal Lobar Degeneration. Acta Neuropathol 2007; 114: 5-22. (Pubitemid 47029055)
6. Davies RR, Hodges JR, Kril JJ, Patterson K, Halliday GM, Xuereb JH. The pathological basis of semantic dementia. Brain 2005; 128 (Pt 9): 1984-95. (Pubitemid 41253266)
7. de Silva R, Lashley T, Strand C, Shiarli AM, Shi J, Tian J, et al. An immunohistochemical study of cases of sporadic and inherited fronto-temporal lobar degeneration using 3R-and 4R-specific tau monoclonal antibodies. Acta Neuropathol 2006; 111: 329-40.
8. Everitt BS, Landau S, Leese M. Cluster analysis. 4th edn. London: Hodder Arnold; 2001.
9. Fletcher PD, Warren JD. Semantic dementia: a specific network-opathy. J Mol Neurosci 2011. Advance Access published on June 29, 2011, doi:10.1007/s12031-011-9586-3.
10. Forman MS, Farmer J, Johnson JK, Clark CM, Arnold SE, Coslett HB, et al. Frontotemporal dementia: clinicopathological correlations. Ann Neurol 2006; 59: 952-62. (Pubitemid 43830927)
11. Geda YE, Boeve BF, Negash S, Graff-Radford NR, Knopman DS, Parisi JE, et al. Neuropsychiatric features in 36 pathologically confirmed cases of corticobasal degeneration. J Neuropsychiatry Clin Neurosci 2007; 19: 77-80. (Pubitemid 46294449)
12. Geser F, Martinez-Lage M, Robinson J, Uryu K, Neumann M, Brandmeir NJ, et al. Clinical and pathological continuum of multisystem TDP-43 proteinopathies. Arch Neurol 2009; 66: 180-9.
13. Gliebus G, Bigio EH, Gasho K, Mishra M, Caplan D, Mesulam MM, et al. Asymmetric TDP-43 distribution in primary progressive aphasia with progranulin mutation. Neurology 2010; 74: 1607-10.
14. Gorno-Tempini ML, Hillis AE, Weintraub S, Kertesz A, Mendez M, Cappa SF, et al. Classification of primary progressive aphasia and its variants. Neurology 2011; 76: 1006-14.
15. Hodges JR, Davies RR, Xuereb JH, Casey B, Broe M, Bak TH, et al. Clinicopathological correlates in frontotemporal dementia. Ann Neurol 2004; 56: 399-406. (Pubitemid 39166559)
16. Josephs KA, Duffy JR. Apraxia of speech and nonfluent aphasia: a new clinical marker for corticobasal degeneration and progressive supra-nuclear palsy. Curr Opin Neurol 2008a; 21: 688-92.
17. Josephs KA, Duffy JR, Strand EA, Whitwell JL, Layton KF, Parisi JE, et al. Clinicopathological and imaging correlates of progressive aphasia and apraxia of speech. Brain 2006a; 129 (Pt 6): 1385-98. (Pubitemid 43999372)
18. Josephs KA, Petersen RC, Knopman DS, Boeve BF, Whitwell JL, Duffy JR, et al. Clinicopathologic analysis of frontotemporal and corticobasal degenerations and PSP. Neurology 2006b; 66: 41-8. (Pubitemid 43739589)
19. Josephs KA, Whitwell JL, Dickson DW, Boeve BF, Knopman DS, Petersen RC, et al. Voxel-based morphometry in autopsy proven PSP and CBD. Neurobiol Aging 2008b; 29: 280-9.
20. Josephs KA, Whitwell JL, Knopman DS, Boeve BF, Vemuri P, Senjem ML, Parisi JE, Ivnik RJ, Dickson DW, Petersen RC, Jack CR Jr. Two distinct subtypes of right temporal variant frontotemporal dementia. Neurology 2009; 3: 1443-50.
21. Josephs KA, Whitwell JL, Parisi JE, Petersen RC, Boeve BF, Jack CR Jr, et al. Caudate atrophy on MRI is a characteristic feature of FTLD-FUS. Eur J Neurol 2010; 17: 969-75.
22. Kelley BJ, Haidar W, Boeve BF, Baker M, Graff-Radford NR, Krefft T, et al. Prominent phenotypic variability associated with mutations in Progranulin. Neurobiol Aging 2009; 30: 739-51.
23. Kelley BJ, Haidar W, Boeve BF, Baker M, Shiung M, Knopman DS, et al. Alzheimer disease-like phenotype associated with the c.154delA mutation in progranulin. Arch Neurol 2010; 67: 171-7.
24. Kertesz A. Frontotemporal dementia, Pick's disease. Ideggyogy Sz 2010; 63: 4-12.
25. Kertesz A, McMonagle P, Blair M, Davidson W, Munoz DG. The evolution and pathology of frontotemporal dementia. Brain 2005; 128 (Pt 9): 1996-2005. (Pubitemid 41253267)
26. Lashley T, Holton JL, Gray E, Kirkham K, O'Sullivan SS, Hilbig A, et al. Cortical alpha-synuclein load is associated with amyloid-beta plaque burden in a subset of Parkinson's disease patients. Acta Neuropathol 2008; 115: 417-25.
27. Lashley T, Rohrer JD, Bandopadhyay R, Fry C, Ahmed Z, Isaacs AM, et al. A comparative clinical, pathological and biochemical study of FUS proteinopathies. Brain 2011, in press.
28. Ling H, O'Sullivan SS, Holton JL, Revesz T, Massey LA, Williams DR, et al. Does corticobasal degeneration exist? A clinicopathological re-evaluation. Brain 2010; 133 (Pt 7): 2045-57.
29. Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, 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. (Pubitemid 26243849)
30. Lladó A, Sánchez-Valle R, Rey MJ, Ezquerra M, Tolosa E, Ferrer I, Molinuevo JL. Catalan collaborative Study Group for FTLD. Clinicopathological and genetic correlates of frontotemporal lobar degeneration and corticobasal degeneration. J Neurol 2008; 255: 488-94.
31. Mackenzie IR, Baborie A, Pickering-Brown S, Du Plessis D, Jaros E, Perry RH, et al. Heterogeneity of ubiquitin pathology in frontotem-poral lobar degeneration: classification and relation to clinical pheno-type. Acta Neuropathol 2006; 112: 539-49. (Pubitemid 44550678)
32. Mackenzie IR, Neumann M, Bigio EH, Cairns NJ, Alafuzoff I, Kril J, et al. Nomenclature for neuropathologic subtypes of frontotemporal lobar degeneration: consensus recommendations. Acta Neuropathol 2009; 117: 15-8.
33. Mackenzie IR, Neumann M, Bigio EH, Cairns NJ, Alafuzoff I, Kril J, et al. Nomenclature and nosology for neuropathologic subtypes of fronto-temporal lobar degeneration: an update. Acta Neuropathol 2010; 119: 1-4.
34. Mackenzie IR, Neumann M, Baborie A, Sampathu DM, Du Plessis D, Jaros E, et al. A harmonized classification system for FTLD-TDP pathology. Acta Neuropathol 2011. Advance Access published on June 5, 2011, doi: 10.1007/s00401-011-0845-8.
35. Mesulam MM. Slowly progressive aphasia without generalized dementia. Ann Neurol 1982; 11: 592-8.
36. Mesulam M, Wicklund A, Johnson N, Rogalski E, Léger GC, Rademaker A, et al. Alzheimer and frontotemporal pathology in subsets of primary progressive aphasia. Ann Neurol 2008; 63: 709-19. (Pubitemid 351945530)
37. Munoz DG, Neumann M, Kusaka H, Yokota O, Ishihara K, Terada S, et al. FUS pathology in basophilic inclusion body disease. Acta Neuropathol 2009; 118: 617-27.
38. Murray R, Neumann M, Forman MS, Farmer J, Massimo L, Rice A, et al. Cognitive and motor assessment in autopsy-proven corticobasal degeneration. Neurology 2007; 68: 1274-83. (Pubitemid 46625973)
39. Neary D, Snowden JS, Gustafson L, Passant U, Stuss D, Black S, et al. Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 1998; 51: 1546-54.
40. Neumann M, Rademakers R, Roeber S, Baker M, Kretzschmar HA, Mackenzie IR. A new subtype of frontotemporal lobar degeneration with FUS pathology. Brain 2009a; 132: 2922-31.
41. Neumann M, Roeber S, Kretzschmar HA, Rademakers R, Baker M, Mackenzie IR. Abundant FUS-immunoreactive pathology in neuronal intermediate filament inclusion disease. Acta Neuropathol 2009b; 118: 605-16.
42. Olichney J, Hansen L, Galasko D, Saitoh T, Hofstetter C, Katzman R, et al. The apolipoprotein e4 allele is associated with increased neuritic plaques and cerebral amyloid angiopathy in Alzheimer's disease and Lewy body variant. Neurology 1996; 47: 190-196. (Pubitemid 26243882)
43. Omar R, Sampson EL, Loy CT, Mummery CJ, Fox NC, Rossor MN, et al. Delusions in frontotemporal lobar degeneration. J Neurol 2009; 256: 600-7.
44. Pereira JM, Williams GB, Acosta-Cabronero J, Pengas G, Spillantini MG, Xuereb JH, et al. Atrophy patterns in histologic vs clinical groupings of frontotemporal lobar degeneration. Neurology 2009; 72: 1653-60.
45. Pick A. Uber die Beziehungen der senilen Hirnatrophie zur Aphasie. Prag Med Wochenschr 1892; 17: 165-7.
46. Piguet O, Halliday GM, Reid WG, Casey B, Carman R, Huang Y, et al. Clinical phenotypes in autopsy-confirmed Pick disease. Neurology 2011; 76: 253-9.
47. Rademakers R, Eriksen JL, Baker M, Robinson T, Ahmed Z, Lincoln SJ, et al. Common variation in the miR-659 binding-site of GRN is a major risk factor for TDP-43-positive frontotemporal dementia. Hum Mol Genet 2008; 17: 3631-42.
48. Rogalski E, Cobia D, Harrison TM, Wieneke C, Weintraub S, Mesulam MM. Progression of language decline and cortical atrophy in subtypes of primary progressive aphasia. Neurology 2011; 76: 1804-10.
49. Rohrer JD, Crutch SJ, Warrington EK, Warren JD. Progranulin-associated primary progressive aphasia: a distinct phenotype? Neuropsychologia 2010a; 48: 288-97.
50. Rohrer JD, Geser F, Zhou J, Gennatas ED, Sidhu M, Trojanowski JQ, et al. TDP-43 subtypes are associated with distinct atrophy patterns in frontotemporal dementia. Neurology 2010b; 75: 2204-11.
51. Rohrer JD, Guerreiro R, Vandrovcova J, Uphill J, Reiman D, Beck J, et al. The heritability and genetics of frontotemporal lobar degeneration. Neurology 2009; 73: 1451-6.
52. Rohrer JD, Lashley T, Holton J, Revesz T, Urwin H, Isaacs AM, et al. The clinical and neuroanatomical phenotype of FUS associated frontotem-poral lobar degeneration. J Neurol Neurosurg Psychiatry 2010c; Advance Access published on July 16, 2010; doi:10.1136/jnnp.2010.214437.
53. Rohrer JD, Ridgway GR, Crutch SJ, Hailstone J, Goll JC, Clarkson MJ, et al. Progressive logopenic/phonological aphasia: erosion of the language network. Neuroimage 2010d; 49: 984-93.
54. Rohrer JD, Ridgway GR, Modat M, Ourselin S, Mead S, Fox NC, et al. Distinct profiles of brain atrophy in frontotemporal lobar degeneration caused by progranulin and tau mutations. Neuroimage 2010e; 53: 1070-6.
55. Rollinson S, Rohrer JD, van der Zee J, Sleegers K, Mead S, Engelborghs S, et al. No association of PGRN 3'UTR rs5848 in frontotemporal lobar degeneration. Neurobiol Aging 2011; 32: 754-5.
56. Sampathu DM, Neumann M, Kwong LK, Chou TT, Micsenyi M, Truax A, et al. Pathological heterogeneity of frontotemporal lobar degeneration with ubiquitin-positive inclusions delineated by ubiquitin immunohisto-chemistry and novel monoclonal antibodies. Am J Pathol 2006; 169: 1343-52. (Pubitemid 351194368)
57. Sá nchez-Valle R, Forman MS, Miller BL, Gorno-Tempini ML. From progressive nonfluent aphasia to corticobasal syndrome: a case report of corticobasal degeneration. Neurocase 2006; 12: 355-9. (Pubitemid 46017720)
58. Saur D, Kreher BW, Schnell S, Kümmerer D, Kellmeyer P, Vry MS, et al. Ventral and dorsal pathways for language. Proc Natl Acad Sci USA 2008; 105: 18035-40.
59. Seelaar H, Rohrer JD, Pijnenburg YA, Fox NC, van Swieten JC. Clinical, genetic and pathological heterogeneity of frontotemporal dementia: a review. J Neurol Neurosurg Psychiatry 2011; 82: 476-86.
60. Seeley WW. Selective functional, regional, and neuronal vulnerability in frontotemporal dementia. Curr Opin Neurol 2008; 21: 701-7.
61. Seeley WW, Allman JM, Carlin DA, Crawford RK, Macedo MN, Greicius MD, et al. Divergent social functioning in behavioural variant frontotemporal dementia and Alzheimer disease: reciprocal networks and neuronal evolution. Alzheimer Dis Assoc Disord 2007; 21: S50-7. (Pubitemid 350307445)
62. Seeley WW, Carlin DA, Allman JM, Macedo MN, Bush C, Miller BL, et al. Early frontotemporal dementia targets neurons unique to apes and humans. Ann Neurol 2006; 60: 660-7. (Pubitemid 46048483)
63. Seeley WW, Crawford R, Rascovsky K, Kramer JH, Weiner M, Miller BL, et al. Frontal paralimbic network atrophy in very mild behavioural variant frontotemporal dementia. Arch Neurol 2008; 65: 249-55. (Pubitemid 351240789)
64. Seeley WW, Crawford RK, Zhou J, Miller BL, Greicius MD. Neurodegenerative diseases target large-scale human brain networks. Neuron 2009; 62: 42-52.
65. Sergeant N, Wattez A, Delacourte A. Neurofibrillary degeneration in progressive supranuclear palsy and corticobasal degeneration: tau pathologies with exclusively "exon 10" isoforms. J Neurochem 1999; 72: 1243-9. (Pubitemid 29085040)
66. Shi J, Shaw CL, Du Plessis D, Richardson AM, Bailey KL, Julien C, et al. Histopathological changes underlying frontotemporal lobar degeneration with clinicopathological correlation. Acta Neuropathol 2005; 110: 501-12. (Pubitemid 41672343)
67. Snowden J, Neary D, Mann D. Frontotemporal lobar degeneration: clinical and pathological relationships. Acta Neuropathol 2007; 114: 31-8. (Pubitemid 47029057)
68. Sporns O, Zwi JD. The small world of the cerebral cortex. Neuroinformatics 2004; 2: 145-62. (Pubitemid 41214095)
69. Tang-Wai DF, Josephs KA, Boeve BF, Dickson DW, Parisi JE, Petersen RC. Pathologically confirmed corticobasal degeneration presenting with visuospatial dysfunction. Neurology 2003; 61: 1134-5. (Pubitemid 37461954)
70. Urwin H, Josephs KA, Rohrer JD, Mackenzie IR, Neumann M, Authier A, et al. FUS pathology defines the majority of tau-and TDP-43-negative frontotemporal lobar degeneration. Acta Neuropathol 2010; 120: 33-41.
71. Vanvoorst WA, Greenaway MC, Boeve BF, Ivnik RJ, Parisi JE, Eric Ahlskog J, et al. Neuropsychological findings in clinically atypical autopsy confirmed corticobasal degeneration and progressive supra-nuclear palsy. Parkinsonism Relat Disord 2008; 14: 376-8. (Pubitemid 351726516)
72. Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S. Fiber tract-based atlas of human white matter anatomy. Radiology 2004; 230: 77-87. (Pubitemid 37549786)
73. Weintraub S, Mesulam M. With or without FUS, it is the anatomy that dictates the dementia phenotype. Brain 2009; 132 (Pt 11): 2906-8.
74. Whitwell JL, Jack CR Jr, Boeve BF, Senjem ML, Baker M, Ivnik RJ, et al. Atrophy patterns in IVS10+16, IVS10 +3, N279K, S305N, P301L, and V337M MAPT mutations. Neurology 2009a; 73: 1058-65.
75. Whitwell JL, Przybelski SA, Weigand SD, Ivnik RJ, Vemuri P, Gunter JL, et al. Distinct anatomical subtypes of the behavioural variant of fron-totemporal dementia: a cluster analysis study. Brain 2009b; 132 (Pt 11): 2932-46.
76. Whitwell JL, Jack CR Jr, Senjem ML, Parisi JE, Boeve BF, Knopman DS, et al. MRI correlates of protein deposition and disease severity in postmortem frontotemporal lobar degeneration. Neurodegen Dis 2009c; 6: 106-17.
77. Whitwell JL, Jack CR Jr, Parisi JE, Knopman DS, Boeve BF, Petersen RC, et al. Imaging signatures of molecular pathology in behavioral variant frontotemporal dementia. J Mol Neurosci 2011. Advance Access published on May 10, 2011; doi:10.1007/s12031-011-9533-3.
78. Williams DR, Holton JL, Strand C, Pittman A, de Silva R, Lees AJ, et al. Pathological tau burden and distribution distinguishes progressive supranuclear palsy-parkinsonism from Richardson's syndrome. Brain 2007; 130 (Pt 6): 1566-76. (Pubitemid 47355935)
79. Winklhofer KF, Tatzelt J, Haass C. The two faces of protein misfolding: gain-and loss-of-function in neurodegenerative diseases. EMBO J 2008; 27: 336-49. (Pubitemid 351161650)
80. Yokota O, Tsuchiya K, Arai T, Yagishita S, Matsubara O, Mochizuki A, et al. Clinicopathological characterization of Pick's disease versus fron-totemporal lobar degeneration with ubiquitin/TDP-43-positive inclusions. Acta Neuropathol 2009; 117: 429-44.
81. Zhou J, Greicius MD, Gennatas ED, Growdon ME, Jang JY, Rabinovici GD, et al. Divergent network connectivity changes in behavioural variant frontotemporal dementia and Alzheimer's disease. Brain 2010; 133 (Pt 5): 1352-67.