Comparative quantitative study of ‘signature’ pathological lesions in the hippocampus and adjacent gyri of 12 neurodegenerative disorders

Journal of Neural Transmission

Volumn 122, Issue 10, 2015, Pages 1355-1367

  Armstrong, Richard A ^a   Cairns, Nigel J ^b  

^a ASTON UNIVERSITY   (United Kingdom)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cellular inclusions; Dentate gyrus (DG); Hippocampus (HC); Neurodegenerative disease; Synucleinopathies; Tauopathies

Indexed keywords

AMYLOID BETA PROTEIN; PRION PROTEIN;

ALZHEIMER DISEASE; ARTICLE; BRAIN REGION; CELL INCLUSION; COGNITION; COMPARATIVE STUDY; CORTICOBASAL DEGENERATION; DEGENERATIVE DISEASE; DENTATE GYRUS; DIFFUSE LEWY BODY DISEASE; DOWN SYNDROME; FRONTOTEMPORAL DEMENTIA; GRANULE CELL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA2 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; IMMUNOREACTIVITY; INTERMEDIATE FILAMENT; MEMORY; NEUROPATHOLOGY; PARAHIPPOCAMPAL GYRUS; PARKINSON DISEASE; PICK PRESENILE DEMENTIA; PRINCIPAL COMPONENT ANALYSIS; PRIORITY JOURNAL; PROGRESSIVE SUPRANUCLEAR PALSY; QUANTITATIVE STUDY; SHY DRAGER SYNDROME; SPORADIC CREUTZFELDT JAKOB DISEASE; SUBICULUM; VARIANT CREUTZFELDT JAKOB DISEASE; ADULT; AGED; FEMALE; MALE; MIDDLE AGED; PATHOLOGY;

ADULT; AGED; FEMALE; HIPPOCAMPUS; HUMANS; MALE; MIDDLE AGED; NEURODEGENERATIVE DISEASES; PARAHIPPOCAMPAL GYRUS; PRINCIPAL COMPONENT ANALYSIS;

EID: 84942990531     PISSN: 03009564     EISSN: 14351463     Source Type: Journal    
DOI: 10.1007/s00702-015-1402-8     Document Type: Article

References (113)

1. Abeti R, Abramov AY, Duchen MR (2011) Beta-amyloid activates PARP causing astrocytic failure and neuronal death. Brain 134:1658–1672
2. Arai T, Nonaka T, Hasegawa M, Akiyama H, Yoshida M, Hashizume Y, Tsuchiya K, Oda T, Ikeda K (2003) Neuronal and glial inclusions in FTD with or without MND are immunopositive for p62. Neurosci Lett 342:41–44
3. Armstrong RA (1992) Alzheimer’s disease: are cellular neurofibrillary tangles linked to β/A4 formation at the projection sites? Neurosci Res Commun 11:171–178
4. Armstrong RA (1994) Differences in β-amyloid (Aβ) deposition in human patients with Down’s syndrome and sporadic Alzheimer’s disease. Neurosci Lett 169:133–136
5. Armstrong R (1995) Beta-amyloid deposition in the medial temporal lobe in elderly non-demented brains and in Alzheimer’s disease. Dementia 6:121–125
6. Armstrong RA (1996) β-amyloid (Aβ) deposits and blood vessels: laminar distribution in the frontal cortex of patients with Alzheimer’s disease. Neurosci Res Commun 18:19–28
7. Armstrong RA (2003) Quantifying the pathology of neurodegenerative disorders: quantitative measurements, sampling strategies and data analysis. Histopathology 42:521–529
8. Armstrong RA, Hilton AC (2011) Statnotes: Statistical Analysis in Microbiology. Wiley-Blackwell, Hoboken
9. Armstrong RA, Smith CUM (1994) β-amyloid (β/A4) deposition in the medial temporal lobe in Down’s syndrome: effects of brain region and patient age. Neurobiol Dis 1:139–144
10. Armstrong RA, Myers D, Smith CUM (1992) The distribution of senile plaques, neurofibrillary tangles and β/A4 protein in the hippocampus in Alzheimer’s disease. Neurosci Res Commun 10:87–94
11. Armstrong RA, Cairns NJ, Lantos PL (1997) Laminar distribution of cortical Lewy bodies and neurofibrillary tangles in dementia with Lewy bodies. Neurosci Res Commun 21:145–152
12. Armstrong RA, Cairns NJ, Lantos P (1999) Laminar distribution of Pick bodies, Pick cells, and Alzheimer’s disease pathology in the frontal and temporal cortex in Pick’s disease. Neuropathol Appl Neurobiol 25:266–271
13. Armstrong RA, Lantos PL, Cairns NJ (2000) Laminar distribution of ballooned neurons and tau positive neurons with inclusions in patients with corticobasal degeneration. Neurosci Res Commun 27:85–93
14. Armstrong RA, Lantos PL, Cairns NJ (2004) A quantitative study of the pathological changes in ten patients with multiple system atrophy (MSA). J Neural Transm 111:485–495
15. Armstrong RA, Lantos PL, Cairns NJ (2005) Multiple system atrophy: laminar distribution of the pathological changes in frontal and temporal neocortex. Clin Neuropathol 24:230–235
16. Armstrong RA, Kerty E, Skullerud K, Cairns NJ (2006) Neuropathological changes in ten cases of neuronal intermediate filament inclusion disease (NIFID): a study using α-internexin immunohistochemistry and principal components analysis (PCA). J Neural Transm 113:1207–1215
17. Armstrong RA, Lantos PL, Cairns NJ (2008) What determines the molecular composition of abnormal protein aggregates in neurodegenerative disease? Neuropathology 28:351–365
18. Armstrong RA, Lantos PL, Cairns NJ (2009) Hippocampal pathology in progressive supranuclear palsy (PSP): a quantitative study of 8 cases. Clin Neuropathol 28:46–53
19. Armstrong RA, Ellis W, Hamilton RL, Mackenzie IRA, Hedreen J, Gearing M, Montine T, Vonsattel J-P, Head E, Lieberman AP, Cairns NJ (2010) Neuropathological heterogeneity in frontotemporal lobar degeneration with TDP-43 proteinopathy: a quantitative study of 94 cases using principal components analysis. J Neural Transm 117:227–239
20. Armstrong RA, Kotzbauer PT, Perlmutter JS, Campbell MC, Hurth KM, Schmidt RE, Cairns NJ (2014) A quantitative study of α-synuclein pathology in fifteen cases of dementia associated with Parkinson disease. J Neural Transm 121:171–181
21. Bahr BA, Abai B, Gall CM, Vanderklosk PW, Hoffman KB, Lynch G (1994) Induction of β-amyloid containing polypeptides in hippocampus: evidence for a concomitant loss of synaptic proteins and interactions with an excitotoxin. Exp Neurol 129:81–94
22. Bancher C, Jellinger KA (1994) Neurofibrillary tangle predominant form of senile dementia type: a rare subtype in very old subjects. Acta Neuropathol 88:565–570
23. Barber R, McKeith IG, Ballard C, Gholkov A, O’Brien JT (2001) A comparison of medial and lateral temporal lobe atrophy in dementia with Lewy bodies and Alzheimer’s disease: magnetic resonance imaging volumetric study. Dement Geriatr Cogn Dis 12:198–205
24. Braak H, Braak E (1992) The human entorhinal cortex: normal morphology and lamina-specific pathology in various diseases. Neurosci Res 15:6–31
25. Braak H, Jellinger K, Braak E, Bohl J (1992) Allocortical neurofibrillary changes in progressive supranuclear palsy. Acta Neuropathol 84:478–483
26. Budka H, Aguzzi A, Brown P, Brucher JM, Bugiani O, Gullotta F, Haltia M, Hauw JJ, Ironside JW, Jellinger K, Kretzschmar HA, Lantos PL, Masullo C, Schlote W, Tateishi J, Weller RO (1995) Neuropathological diagnostic criteria for Creutzfeldt–Jakob disease (CJD) and other human spongiform encephalopathies (Prion diseases). Brain Pathol 5:459–466
27. Cairns NJ, Zhukareva V, Uryu K, Zhang B, Bigio E, Mackenzie IRA, Gearing M, Duyckaerts C, Yokoo H, Nakazato Y, Jaros E, Perry RH, Lee VMY, Trojanowski JQ (2004a) α-Internexin is present in the pathological inclusions of neuronal intermediate filament inclusion disease. Am J Pathol 164:2153–2161
28. Cairns NJ, Jaros E, Perry RH, Armstrong RA (2004b) Temporal lobe pathology of human patients with neurofilament inclusion disease. Neurosci Lett 354:245–247
29. Cairns NJ, Grossman M, Arnold SE, Burn DJ, Jaros E, Perry RH, Duyckaerts C, Stankoff B, Pillon B, Skullerud K, Cruz-Sanchez FF, Bigio EH, Mackenzie IRA, Gearing M, Juncos JL, Glass JD, Yokoo H, Nakazato Y, Mosaheb S, Thorpe JR, Uryu K, Lee VM-Y, Trojanowski JQ (2004c) Clinical and neuropathologic variation in neuronal intermediate filament inclusion disease (NIFID). Neurology 63:1376–1384
30. Cairns NJ, Bigio EH, Mackenzie IRA, Neumann M, Lee VMY, Hatanpaa KJ, White CL, Schneider JA, Grinberg LT, Halliday G, Duyckaerts C, Lowe JS, Holm IE, Tolnay M, Okamoto K, Yokoo H, Murayama S, Woulfe J, Munoz DG, Dickson DW, Ince PG, Trojanowski JQ, Mann DMA (2007) Neuropathologic diagnostic and nosological criteria for frontotemporal lobar degeneration: consensus of the Consortium for Frontotemporal Lobar Degeneration. Acta Neuropathol 114:5–22
31. Chow TW, Hynan LS, Lipton AM (2006) MMSE scores decline at a greater rate in frontotemporal degeneration than in AD. Dement Geriatr Cogn Dis 22:194–199
32. Corder EH, Woodbury MA, Volkmann I, Madsen DK, Bogdanovic N, Winblad B (2000) Density profiles in Alzheimer’s disease regional brain pathology for the Huddinge brain bank: pattern recognition emulates and expands upon Braak staging. Exp Gerontol 35:851–864
33. Dalton AL, McLachlan C (1984) Incidence of memory deterioration in ageing persons with Down’s syndrome. In: Berg JM (ed) Perspectives and progress in mental retardation: biomedical aspects, vol 2. University Park Press, Baltimore, pp 55–62
34. Davis DG, Schmitt FA, Wekstein DR, Markesbery WR (1999) Alzheimer neuropathology alterations in aged cognitively normal subjects. J Neuropath Exp Neurol 58:376–388
35. Davison S, Johnson N, Weintraub MM, Engberg A, Mishra M, Baker M, Adamson J, Hutton M, Rademakers R, Bigio EH (2007) Clinicopathologic correlations in PGRN mutations. Neurology 69:1113–1121
36. De Leon MJ, George AE, Golumb J, Tarhish C, Convit A, Kluger A, DeSantis S, McRae T, Ferris SH, Reisberg B, Ince C, Rusinek H, Bobinski M, Quinn B, Miller DC, Wisniewski HM (1997) Frequency of hippocampal formation atrophy in normal aging and Alzheimer’s disease. Neurobiol Aging 18:1–11
37. Egensperger R, Weggen S, Ida N, Multhaup G, Schnabel R, Beyreuther K, Bayer TA (1999) Reverse relationship between β-amyloid precursor protein and β-amyloid plaques in Down’s syndrome versus sporadic/familial Alzheimer’s disease. Acta Neuropathol 97:113–118
38. Filey CM, Kleinschimidtdemasters BJK, Gross KF (1994) Non-Alzheimer frontotemporal degenerative dementia: a neurobehavioural and pathological study. Clin Neuropathol 13:109–116
39. Forman MS, Mackenzie IR, Cairns NJ, Swanson E, Boyer PJ, Drachman DA, Jhaveri BS, Karlawish JH, Pestronk A, Smith TW, Tu PH, Watts GDJ, Markesbery WR, Smith CD, Kimonis VE (2006) Novel ubiquitin neuropathology in frontotemporal dementia with valosin-containing protein gene mutations. J Neuropath Exp Neurol 65:571–581
40. Galimberti D, Scarpini E (2015) Frontotemporal lobar degeneration. In: Martin AR, Preedy VR (eds) Diet and nutrition in dementia and cognitive decline. Academic Press, London, pp 57–66
41. Garcia-Sierra F, Hauw JJ, Duyckaerts C, Wischik CA, Luna-Munoz J, Mena R (2000) The extent of neuropathology in performant pathway neurons is the key determinant of dementia in the very old. Acta Neuropathol 100:29–35
42. Gilman S, Low PA, Quinn N, Albanese A, Ben-Schlomo Y, Fowler CJ, Kaufmann H, Klockgether T, Lang AE, Lantos PL, Livan I, Mathias CJ, Oliver E, Robertson D, Schatz I, Wenning GK (1998) Consensus statement on the diagnosis of multiple system atrophy. J Auton Nerv Syst 74:189–192
43. Glenner GG, Wong CW (1984) Alzheimer’s disease and Down’s syndrome: sharing of a unique cerebrovascular amyloid fibril protein. Biochem Biophys Res Commun 122:1131–1135
44. Goedert M, Clavaguera F, Tolnay M (2010) The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci 33:317–325
45. Gomez-Tortosa E, Newell K, Irizairy MC, Albert M, Growdon JH, Hyman BT (1999) Clinical and quantitative pathologic correlates of dementia with Lewy bodies. Neurology 53:1284–1291
46. Gray JA (1987) The Neuropsychology of Anxiety. Oxford University Press, New York, pp 1–548
47. Gray JA, McNaughton N (2000) The neuropsychology of anxiety: an enquiry into the functions of the septo-hippocampal system. Oxford University Press, New York
48. Guentchev M, Hainfellner JA, Trabattori GR, Budka H (1997) Distribution of parvalbumin-immunoreactive neurons in brain correlates with hippocampal and temporal cortical pathology in Creutzfeldt–Jakob disease. J Neuropath Exp Neurol 56:1119–1124
49. Guillozet AL, Weintraub S, Mash DC, Mesulam MM (2003) Neurofibrillary tangles, amyloid, and memory in aging and mild cognitive deficit. Arch Neurol Chic 60:729–736
50. Hauw JJ, 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 (PSP). Neurology 44:2015–2019
51. Head D, Snyder AZ, Girton LE, Morris JC, Buckner RL (2005) Fronto-hippocampal double dissociation between normal aging and Alzheimer’s disease. Cereb Cortex 15:732–739
52. Higashi S, Iseki E, Yamamoto R, Minegashi M, Hiro H, Fizisawa K, Togo T, Katsuse O, Uchikado H, Furukawa Y, Kosaka K, Arai H (2007) Concurrence of TDP-43, tau and alpha-synuclein pathology in brains of Alzheimer’s disease and dementia with Lewy bodies. Brain Res 1184:284–294
53. Hoesen GW, Solodkin A (1993) Some modular features of temporal cortex in humans as revealed by pathological changes in Alzheimer’s disease. Cereb Cortex 3:465–475
54. Hof PR, Delacourte A, Bouras C (1992) Distribution of cortical neurofibrillary tangles in progressive supranuclear palsy: a quantitative analysis of six cases. Acta Neuropathol 84:45–51
55. Hof PR, Bouras C, Perl DP, Morrison JH (1994) Quantitative neuropathological analysis of Pick’s disease cases: cortical distribution of Pick bodies and coexistence with Alzheimer’s disease. Acta Neuropathol 87:115–124
56. Hof PR, Bouras C, Perl DP, Sparks DL, Mehta N, Morrison JH (1995) Age-related distribution of neuropathological changes in the cerebral cortex of patients with Down’s syndrome: quantitative regional analysis and comparison with Alzheimer’s disease. Arch Neurol-Chicago 52:379–391
57. Hoke A, Canning DR, Malemud CJ, Silver J (1994) Regional differences in reactive gliosis induced by substrate-bound β-amyloid. Exp Neurol 130:56–66
58. Hyman BT, West HL, Rebeck GW, Lai F, Mann DMA (1995) Neuropathological changes in Down’s syndrome hippocampal formation: affect of age and apolipoprotein E genotype. Arch Neurol-Chicago 52:373–378
59. Ironside JW, Head MW, Bell JE, McCardle L, Will RG (2000) Laboratory diagnosis of variant Creutzfeldt-Jakob disease. Histopathology 37:1–9
60. Jack CR, Petersen RC, Xu YC, Waring SC, O’Brien PC, Tangalos EG, Smith GE, Ivnick RJ, Kokmen E (1997) Medial temporal atrophy on MRI in normal aging and very mild Alzheimer’s disease. Neurology 49:786–794
61. Jack CR, Petersen RC, Xu Y, O’Brien PC, Smith GE, Ivnick RJ, Tangalos EG, Kokmen E (1998) Rate of medial temporal lobe atrophy in typical aging and Alzheimer’s disease. Neurology 51:993–999
62. Jackson M, Lowe J (1996) The new neuropathology of degenerative fronto-temporal dementias. Acta Neuropathol 91:127–134
63. Josephs KA, Dickson DW (2007) Hippocampal sclerosis in tau-negtative frontotemporal lobar degeneration. Neurobiol Aging 28:1718–1722
64. Kersaitis C, Halliday GM, Kril JJ (2004) Regional and cellular pathology in fronto-temporal dementia: relationship to stage of disease in cases with and without Pick bodies. Acta Neuropathol 108:515–523
65. Kim EJ, Cho SS, Jeong BH, Kim YS, Seo SW, Na DL, Geschwind MD, Jeong Y (2012) Glucose metabolism in sporadic Creutzfeldt-Jakob disease: a statistical parametric mapping analysis of 18F-FDG PET. Eur J Neurol 19:488–493
66. Kotzbauer PT, Cairns NJ, Campbell MC, Racette BA, Tabbal SD, Perlmutter JS (2012) Pathological accumulation of α-synuclein and Aβ in Parkinson disease patients with dementia. Arch Neurol-Chicago 23:1–6
67. Kovari E, Gold G, Giannakopoulos P, Bouras C (2004) Cortical ubiquitin positive inclusions in frontotemporal dementia without motor neuron disease: a quantitative immunocytochemical study. Acta Neuropathol 108:207–212
68. Lee ACH, Levi N, Davies RR, Hodges JR, Graham KS (2007) Differing profiles of face and scene discrimination deficits in semantic dementia and Alzheimer’s disease. Neuropsychologia 45:2135–2146
69. Lee SH, Kim SS, Tae WS, Lee SY, Lee KU, Jhoo J (2013) Brain volumetry in Parkinson’s disease with and without dementia: where are the differences? Acta Radiol 54:581–586
70. Lindau M, Jelic V, Johansson SE, Anderson C, Wahlund LO, Almkvist O (2003) Quantitative EEG abnormalities and cognitive dysfunctions in frontotemporal dementia and Alzheimer’s disease. Dement Geriatr Cogn 15:106–114
71. Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Davoisen RC, Goetz CG, Golbe LI, Grafman J, Growden JH, Hallett M, Jankovic J, Quinn NP, Tolisa E, Zee DS, Chase TW, FitzGibbon EJ, Hall Z, Juncos J, Nelson KB, Oliver E, Pramstaller P, Reich SG, Verny M (1996a) Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele–Richardson–Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 47:1–9
72. Litvan I, Hauw JJ, Bartko JJ, Lantos PL, Daniel SE, Horoupian DS, McKee A, Dickson D, Bancher C, Tabaton M, Jellinger K, Anderson DW (1996b) Validity and reliability of the preliminary NINDS neuropathological criteria for progressive supranuclear palsy and related disorders. J Neuropath Exp Neurol 55:97–105
73. Mackenzie IR, Baborie A, Pickering-Brown S, Du Plessis D, Jaros E, Perry RH, Neary D, Snowden JS, Mann DMA (2006) Heterogeneity of ubiquitin pathology in frontotemporal lobar degeneration: classification and relation to clinical phenotype. Acta Neuropathol 112:539–549
74. Markus HS, Lees AJ, Lennox G, Marsden CD, Costa DC (1995) Patterns of regional cerebral blood flow in corticobasal degeneration studied using HMPAO SPECT: comparison with Parkinson’s disease and normal controls. Move Disord 10:179–187
75. Masullo C, Macchi G (1997) Resistance of the hippocampus in Creutzfeldt–Jakob disease. Clin Neuropathol 16:37–44
76. Mazere J, Meissner WG, Sibon I, Lamare F, Tison F, Allard M, Mayo W (2013) [l-123]BVM SPECT imaging of cholinergic systems in multiple system atrophy: a specific alteration of the ponto-thalamic cholinergic pathways (Ch5-CH6). Neuroimage Clin 3:212–217
77. McKeith IG, Galasko D, Kosaka K, Perry EK, Dickson DW, Hansen LA, Salmon DP, Lowe J, Mirra SS, Byrne EJ, Lennox G, Quinn NP, Edwardson JA, Ince PG, Bergman A, Burns A, Miller BL, Lovestone S, Collerton D, Jansen ENH, Ballard C, de Vis RAI, Wilcock GK, Jellinger KA, Perry RH (1996) Consensus guidelines for the clinical and pathological diagnosis of dementia with Lewy bodies (DLB): report of the consortium on DLB international workshop. Neurology 47:1113–1124
78. Meencke HJ, Ferszt R, Gertz HJ, Cervos-Navarro J (1983) Hippocampal pathology in normal aging and dementia. In: Cervos-Navarro J, Sarkander HI (eds) Brain aging, neuropathology and neuropharmacology (aging vol 21). Raven Press, New York, pp 13–26
79. Meiner Z, Newman JP, Rosenman H, Soffer D, Steiner I (2005) Frontotemporal dementia with ubiquinated neuronal inclusions and visuospatial impairment. Neurology 65:478–480
80. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brownlee LM, Vogel FS, Hughes JP, van Belle G, Berg L (1991) The consortium to establish a registry for Alzheimer’s disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer’s disease. Neurology 41:479–486
81. Mori F, Hayashi S, Yamagishi S, Yoshimoto M, Yagihashi S, Tokahashi H, Wakabayashi K (2002) Pick’s disease: alpha- and beta-synuclein immunoreactive Pick bodies in the dentate gyrus. Acta Neuropathol 104:455–461
82. Nauta WJH, Feirtag M (1986) Fundamental neuroanatomy. WH Freeman, New York
83. O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, Oxford
84. Pham CT, de Silva R, Haik S, Verny M, Sachet A, Forette B, Lees A, Hauw JJ, Duyckaerts C (2011) Tau-positive grains are constant in centenarians’ hippocampus. Neurobiol Aging 32:1296–1303
85. Pike CJ, Cotman CW (1995) Calretinin-immunoreactive neurons are resistant to b-amyloid toxicity in vitro. Brain Res 671:293–298
86. Poon MA, Stuckey S, Storey E (2001) MRI evidence of cerebellar and hippocampal involvement in Creutzfeldt–Jakob disease. Neuroradiol 43:746–749
87. Probst A, Taylor KI, Tolnay M (2007) Hippocampal sclerosis dementia: a reappraisal. Acta Neuropathol 114:335–345
88. Rektorova I, Blundo R, Marecek R, Weis L, Aarsland D, Antonini A (2014) Grey matter changes in cognitively impaired Parkinson’s disease patients. PLoS One 9:e85595
89. Reyes E, Gamboa A, Masliah E (1993) Atypical diffuse Lewy body disease with neuritic abnormalities. Clin Neuropathol 12:330–334
90. Rosso SM, Kamphorst W, deGraf B, Willemsen R, Ravid R, Niermeyer MF, Spillantini MG, Henlink P, van Swieten JC (2001) Familial fronto-temporal dementia with ubiquitin-positive inclusions is linked to chromosome 17q21-22. Brain 124:1948–1957
91. Saab BJ, Georgiou J, Nath A, Lee FJ, Wang H, Michalon A, Liu F, Mansuy IM, Roder JC (2009) NCS-1 in the dentate gyrus promotes exploration, synapitic plasticity, and rapid acquisition of spatial memory. Neuron 63:643–656
92. Saini J, Bagepally BS, Sandhya M, Pasha SA, Yadav R, Thennarasu K, Pai PK (2013) Subcortical structures in progressive supranuclear palsy: vertex-based analysis. Eur J Neurol 20:493–501
93. Saper CB, Wainer BH, German DC (1987) Axonal and transneural transport in the transmission of neurological disease: potential role in system degenerations, including Alzheimer’s disease. Neuroscience 23:389–398
94. Schmidt R (1992) Comparison of magnetic-resonance-imaging in Alzheimer’s disease, vascular dementia and normal aging. Eur Neurol 32:164–169
95. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol 20:11–21
96. Seritan AL, Mendez MF, Silverman DHS, Hurley RA, Taber KH (2004) Functional imaging as a window to dementia: corticobasal degeneration. J Neuropsych Clin Neurol 16:393–399
97. Shinagawa S, Toyota Y, Ishikawa T, Fukuhara R, Hokoishi K, Komori K, Tanimukai S, Ikeda M (2008) Cognitive function and psychiatric symptoms in early- and late-onset frontotemporal dementia. Dement Geriatr Cogn 25:439–444
98. Shinotoh H, Namba H, Yamaguchi M, Fukushi K, Nagatsuka S, Iyo M, Asahina M, Hattori T, Tanada S, Irie T (1999) Positron emission tomographic measurement of acetylcholinesterase activity reveals differential loss of ascending cholinergic systems in Parkinson’s disease and progressive supranuclear palsy. Ann Neurol 46:62–69
99. Simic G, Becheti S, Kelovic Z, Kos M, Grbic K, Hof PR, Kostovic I (2005) Hemispheric asymmetry, modular variability and age-related changes in the human entorhinal cortex. Neuroscience 130:911–925
100. Steiner JA, Angot E, Brunden P (2011) A deadly spread: cellular mechanisms of α-synuclein transfer. Cell Death Differ 18:1425–1433
101. Takeda A, Arai N, Komori T, Kato S, Oda M (1997) Neuronal inclusions in the dentate fascia in patients with multiple system atrophy. Neurosci Lett 227:157–160
102. Tierney MC, Fisher RH, Lewis AJ, Zorzitto ML, Snow WG, Reid DW, Nieuwstraten P (1988) The NINCDS-ADRDA work group criteria for the clinical diagnosis of probable Alzheimer’s disease. Neurology 38:359–364
103. Vinogradova OS (2001) Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11:578–598
104. Wakabayashi K, Hansen LA, Vincent I, Mallory M, Masliah E (1996) Neurofibrillary tangles in the dentate granule cells of patients with Alzheimer’s disease, Lewy body dementia, and progressive supranuclear palsy. Acta Neuropathol 93:7–12
105. Wakabayashi K, Hayashi S, Kakita A, Yamada M, Toroshima Y, Yoshimoto M, Takahashi H (1998) Accumulation of alpha-synuclein.NACP is a cytopathological feature common to Lewy body disease and multiple system atrophy. Acta Neuropathol 96:445–452
106. Wang IF, Wu LS, Chang HY, Shen CJK (2008) TDP-43, the signature protein of FTLD-U is a neuronal activity-responsive factor. J Neurochem 105:797–806
107. Whitwell JL, Przybelski SA, Weigand SD, Knopman DS, Boeve BF, Petersen RC, Jack CR (2007) 3D maps from multiple MRI illustrate changing atrophy patterns as subjects progress from mild cognitive impairment to Alzheimer’s disease. Brain 130:1777–1786
108. Will RG, Ironside JW, Zeidler M, Cousens SN, Estibeiro K, Alperovitch A, Poser S, Pocchiari M, Hofman A, Smith PG (1996) A new variant of Creutzfeldt–Jakob disease in the United Kingdom. Lancet 347:921–925
109. Woulfe J, Kertesz A, Munoz DG (2001) Frontotemporal dementia with ubiquinated cytoplasmic and intranuclear inclusions. Acta Neuropathol 102:94–102
110. Yaar M, Zhai S, Pilch PF, Doyle SM, Eisenhauer PB, Fine RE, Gilchrest BA (1997) Binding of beta-amyloid to the p75 neurotrophic receptor induces apoptosis: a possible mechanism for Alzheimer’s disease. J Clin Invest 100:2333–2340
111. Yaguchi M, Fujita Y, Amari M, Takatama M, Al-Sarraj S, Leigh PN, Okamoto K (2004) Morphological differences of intraneural ubiquitin positive inclusions in the dentate gyrus and parahippocampal gyrus of motor neuron disease with dementia. Neuropathology 24:296–301
112. Yang Y, Schmitt HP (2001) Frontotemporal dementia: evidence for impairment of ascending serotinergic but not adrenergic innervation: immunocytochemical and quantitative study using a graph method. Acta Neuropathol 101:256–270
113. Yokata O, Davidson Y, Bigio EH, Ishizu H, Terada S, Arai T, Hasegawa M, Akiyama H, Sikkink S, Pickering-Brown S, Mann DMA (2010) Phosphorylated TDP-43 pathology and hippocampal sclerosis in progressive supranuclear palsy. Acta Neuropathol 120:55–66