Skip to main content

Advertisement

Log in

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

  • Translational Neurosciences - Original Article
  • Published:
Journal of Neural Transmission Aims and scope Submit manuscript

An Erratum to this article was published on 11 June 2015

Abstract

The hippocampus (HC) and adjacent gyri are implicated in dementia in several neurodegenerative disorders. To compare HC pathology among disorders, densities of ‘signature’ pathological lesions were measured at a standard location in eight brain regions of 12 disorders. Principal components analysis of the data suggested that the disorders could be divided into three groups: (1) Alzheimer’s disease (AD), Down’s syndrome (DS), sporadic Creutzfeldt–Jakob disease, and variant Creutzfeldt–Jakob disease in which either β-amyloid (Aβ) or prion protein deposits were distributed in all sectors of the HC and adjacent gyri, with high densities being recorded in the parahippocampal gyrus and subiculum; (2) Pick’s disease, sporadic frontotemporal lobar degeneration with TDP-43 immunoreactive inclusions, and neuronal intermediate filament inclusion disease in which relatively high densities of neuronal cytoplasmic inclusions were present in the dentate gyrus (DG) granule cells; and (3) Parkinson’s disease dementia, dementia with Lewy bodies, progressive supranuclear palsy, corticobasal degeneration, and multiple system atrophy in which densities of signature lesions were relatively low. Variation in density of signature lesions in DG granule cells and CA1 were the most important sources of neuropathological variation among disorders. Hence, HC and adjacent gyri are differentially affected in dementia reflecting either variation in vulnerability of hippocampal neurons to specific molecular pathologies or in the spread of pathological proteins to the HC. Information regarding the distribution of pathology could ultimately help to explain variations in different cognitive domains, such as memory, observed in various disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abeti R, Abramov AY, Duchen MR (2011) Beta-amyloid activates PARP causing astrocytic failure and neuronal death. Brain 134:1658–1672

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Armstrong RA (2003) Quantifying the pathology of neurodegenerative disorders: quantitative measurements, sampling strategies and data analysis. Histopathology 42:521–529

    Article  CAS  PubMed  Google Scholar 

  • Armstrong RA, Hilton AC (2011) Statnotes: Statistical Analysis in Microbiology. Wiley-Blackwell, Hoboken

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Armstrong RA, Lantos PL, Cairns NJ (2008) What determines the molecular composition of abnormal protein aggregates in neurodegenerative disease? Neuropathology 28:351–365

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Braak H, Braak E (1992) The human entorhinal cortex: normal morphology and lamina-specific pathology in various diseases. Neurosci Res 15:6–31

    Article  CAS  PubMed  Google Scholar 

  • Braak H, Jellinger K, Braak E, Bohl J (1992) Allocortical neurofibrillary changes in progressive supranuclear palsy. Acta Neuropathol 84:478–483

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cairns NJ, Jaros E, Perry RH, Armstrong RA (2004b) Temporal lobe pathology of human patients with neurofilament inclusion disease. Neurosci Lett 354:245–247

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Davis DG, Schmitt FA, Wekstein DR, Markesbery WR (1999) Alzheimer neuropathology alterations in aged cognitively normal subjects. J Neuropath Exp Neurol 58:376–388

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Filey CM, Kleinschimidtdemasters BJK, Gross KF (1994) Non-Alzheimer frontotemporal degenerative dementia: a neurobehavioural and pathological study. Clin Neuropathol 13:109–116

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Goedert M, Clavaguera F, Tolnay M (2010) The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci 33:317–325

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Gray JA (1987) The Neuropsychology of Anxiety. Oxford University Press, New York, pp 1–548

    Google Scholar 

  • Gray JA, McNaughton N (2000) The neuropsychology of anxiety: an enquiry into the functions of the septo-hippocampal system. Oxford University Press, New York

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ironside JW, Head MW, Bell JE, McCardle L, Will RG (2000) Laboratory diagnosis of variant Creutzfeldt-Jakob disease. Histopathology 37:1–9

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Jackson M, Lowe J (1996) The new neuropathology of degenerative fronto-temporal dementias. Acta Neuropathol 91:127–134

    Article  CAS  PubMed  Google Scholar 

  • Josephs KA, Dickson DW (2007) Hippocampal sclerosis in tau-negtative frontotemporal lobar degeneration. Neurobiol Aging 28:1718–1722

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Masullo C, Macchi G (1997) Resistance of the hippocampus in Creutzfeldt–Jakob disease. Clin Neuropathol 16:37–44

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Meiner Z, Newman JP, Rosenman H, Soffer D, Steiner I (2005) Frontotemporal dementia with ubiquinated neuronal inclusions and visuospatial impairment. Neurology 65:478–480

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Nauta WJH, Feirtag M (1986) Fundamental neuroanatomy. WH Freeman, New York

    Google Scholar 

  • O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, Oxford

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Pike CJ, Cotman CW (1995) Calretinin-immunoreactive neurons are resistant to b-amyloid toxicity in vitro. Brain Res 671:293–298

    Article  CAS  PubMed  Google Scholar 

  • Poon MA, Stuckey S, Storey E (2001) MRI evidence of cerebellar and hippocampal involvement in Creutzfeldt–Jakob disease. Neuroradiol 43:746–749

    Article  CAS  Google Scholar 

  • Probst A, Taylor KI, Tolnay M (2007) Hippocampal sclerosis dementia: a reappraisal. Acta Neuropathol 114:335–345

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Reyes E, Gamboa A, Masliah E (1993) Atypical diffuse Lewy body disease with neuritic abnormalities. Clin Neuropathol 12:330–334

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Schmidt R (1992) Comparison of magnetic-resonance-imaging in Alzheimer’s disease, vascular dementia and normal aging. Eur Neurol 32:164–169

    Article  CAS  PubMed  Google Scholar 

  • Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol 20:11–21

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Steiner JA, Angot E, Brunden P (2011) A deadly spread: cellular mechanisms of α-synuclein transfer. Cell Death Differ 18:1425–1433

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Woulfe J, Kertesz A, Munoz DG (2001) Frontotemporal dementia with ubiquinated cytoplasmic and intranuclear inclusions. Acta Neuropathol 102:94–102

    CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

Download references

Acknowledgments

We thank the following for making tissue sections available for this study: Brain Bank, Institute of Psychiatry, London, UK; William Ellis (Department of Pathology, University of California, Davis, Sacramento, CA, USA), Ronald L. Hamilton (Department of Pathology, University of Pittsburgh, Pittsburgh, PA, USA), Ian R. A. Mackenzie (Department of Pathology, Vancouver General Hospital, Vancouver, Canada), E. Tessa Hedley-Whyte (Massachusetts General Hospital and Harvard Brain Tissue Resource Center, Belmont, MA, USA), Marla Gearing (Center for Neurodegenerative Disease, Emory University, Atlanta, GA, USA), R. H. Perry (Department of Neuropathology, Newcastle General Hospital, Newcastle-upon-Tyne, NE4 6BE, UK), C. Duyckaerts (Laboratoire de Neuropathologie, Hôpital de la Salpêtrière, Paris, France), F. Cruz-Sanchez (Institute of Neurological and Gerontological Sciences, International University of Catalonia, Barcelona, Spain), K. Skullerud (Department of Pathology, Rikshospitalet, Oslo, Norway), E. Bigio (Department of Pathology, Northwestern University Medical School, Chicago, IL, USA), and H. Yokoo (Department of Pathology, Gunma University School of Medicine, Maebashi, Japan).

Compliance with ethical standards

Informed consent was given for the removal of all brain tissue subject to local ethical committee approval and the 1996 Declaration of Helsinki (as modified Edinburgh 2000). The authors report no conflicts of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Richard A. Armstrong.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Armstrong, R.A., Cairns, N.J. Comparative quantitative study of ‘signature’ pathological lesions in the hippocampus and adjacent gyri of 12 neurodegenerative disorders. J Neural Transm 122, 1355–1367 (2015). https://doi.org/10.1007/s00702-015-1402-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00702-015-1402-8

Keywords

Navigation