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Published in: Journal of Neural Transmission 10/2015

01-10-2015 | Translational Neurosciences - Original Article

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

Authors: Richard A. Armstrong, Nigel J. Cairns

Published in: Journal of Neural Transmission | Issue 10/2015

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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.
Literature
go back to reference Abeti R, Abramov AY, Duchen MR (2011) Beta-amyloid activates PARP causing astrocytic failure and neuronal death. Brain 134:1658–1672PubMedCrossRef Abeti R, Abramov AY, Duchen MR (2011) Beta-amyloid activates PARP causing astrocytic failure and neuronal death. Brain 134:1658–1672PubMedCrossRef
go back to reference 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 342:41–44PubMedCrossRef 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 342:41–44PubMedCrossRef
go back to reference 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 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
go back to reference Armstrong RA (1994) Differences in β-amyloid (Aβ) deposition in human patients with Down’s syndrome and sporadic Alzheimer’s disease. Neurosci Lett 169:133–136PubMedCrossRef Armstrong RA (1994) Differences in β-amyloid (Aβ) deposition in human patients with Down’s syndrome and sporadic Alzheimer’s disease. Neurosci Lett 169:133–136PubMedCrossRef
go back to reference Armstrong R (1995) Beta-amyloid deposition in the medial temporal lobe in elderly non-demented brains and in Alzheimer’s disease. Dementia 6:121–125PubMed Armstrong R (1995) Beta-amyloid deposition in the medial temporal lobe in elderly non-demented brains and in Alzheimer’s disease. Dementia 6:121–125PubMed
go back to reference 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 18:19–28CrossRef 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 18:19–28CrossRef
go back to reference Armstrong RA (2003) Quantifying the pathology of neurodegenerative disorders: quantitative measurements, sampling strategies and data analysis. Histopathology 42:521–529PubMedCrossRef Armstrong RA (2003) Quantifying the pathology of neurodegenerative disorders: quantitative measurements, sampling strategies and data analysis. Histopathology 42:521–529PubMedCrossRef
go back to reference Armstrong RA, Hilton AC (2011) Statnotes: Statistical Analysis in Microbiology. Wiley-Blackwell, Hoboken Armstrong RA, Hilton AC (2011) Statnotes: Statistical Analysis in Microbiology. Wiley-Blackwell, Hoboken
go back to reference 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 1:139–144PubMedCrossRef 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 1:139–144PubMedCrossRef
go back to reference 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 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
go back to reference Armstrong RA, Cairns NJ, Lantos PL (1997) Laminar distribution of cortical Lewy bodies and neurofibrillary tangles in dementia with Lewy bodies. Neurosci Res Commun 21:145–152CrossRef Armstrong RA, Cairns NJ, Lantos PL (1997) Laminar distribution of cortical Lewy bodies and neurofibrillary tangles in dementia with Lewy bodies. Neurosci Res Commun 21:145–152CrossRef
go back to reference 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 25:266–271PubMedCrossRef 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 25:266–271PubMedCrossRef
go back to reference 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 27:85–93CrossRef 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 27:85–93CrossRef
go back to reference 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 111:485–495PubMedCrossRef 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 111:485–495PubMedCrossRef
go back to reference Armstrong RA, Lantos PL, Cairns NJ (2005) Multiple system atrophy: laminar distribution of the pathological changes in frontal and temporal neocortex. Clin Neuropathol 24:230–235PubMed Armstrong RA, Lantos PL, Cairns NJ (2005) Multiple system atrophy: laminar distribution of the pathological changes in frontal and temporal neocortex. Clin Neuropathol 24:230–235PubMed
go back to reference 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 113:1207–1215PubMedCrossRef 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 113:1207–1215PubMedCrossRef
go back to reference Armstrong RA, Lantos PL, Cairns NJ (2008) What determines the molecular composition of abnormal protein aggregates in neurodegenerative disease? Neuropathology 28:351–365PubMedCrossRef Armstrong RA, Lantos PL, Cairns NJ (2008) What determines the molecular composition of abnormal protein aggregates in neurodegenerative disease? Neuropathology 28:351–365PubMedCrossRef
go back to reference Armstrong RA, Lantos PL, Cairns NJ (2009) Hippocampal pathology in progressive supranuclear palsy (PSP): a quantitative study of 8 cases. Clin Neuropathol 28:46–53PubMedCrossRef Armstrong RA, Lantos PL, Cairns NJ (2009) Hippocampal pathology in progressive supranuclear palsy (PSP): a quantitative study of 8 cases. Clin Neuropathol 28:46–53PubMedCrossRef
go back to reference 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 117:227–239PubMedCentralPubMedCrossRef 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 117:227–239PubMedCentralPubMedCrossRef
go back to reference 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 121:171–181PubMedCentralPubMedCrossRef 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 121:171–181PubMedCentralPubMedCrossRef
go back to reference 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 129:81–94PubMedCrossRef 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 129:81–94PubMedCrossRef
go back to reference Bancher C, Jellinger KA (1994) Neurofibrillary tangle predominant form of senile dementia type: a rare subtype in very old subjects. Acta Neuropathol 88:565–570PubMedCrossRef Bancher C, Jellinger KA (1994) Neurofibrillary tangle predominant form of senile dementia type: a rare subtype in very old subjects. Acta Neuropathol 88:565–570PubMedCrossRef
go back to reference 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 12:198–205CrossRef 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 12:198–205CrossRef
go back to reference Braak H, Braak E (1992) The human entorhinal cortex: normal morphology and lamina-specific pathology in various diseases. Neurosci Res 15:6–31PubMedCrossRef Braak H, Braak E (1992) The human entorhinal cortex: normal morphology and lamina-specific pathology in various diseases. Neurosci Res 15:6–31PubMedCrossRef
go back to reference Braak H, Jellinger K, Braak E, Bohl J (1992) Allocortical neurofibrillary changes in progressive supranuclear palsy. Acta Neuropathol 84:478–483PubMedCrossRef Braak H, Jellinger K, Braak E, Bohl J (1992) Allocortical neurofibrillary changes in progressive supranuclear palsy. Acta Neuropathol 84:478–483PubMedCrossRef
go back to reference 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 5:459–466PubMedCrossRef 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 5:459–466PubMedCrossRef
go back to reference 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 164:2153–2161PubMedCentralPubMedCrossRef 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 164:2153–2161PubMedCentralPubMedCrossRef
go back to reference Cairns NJ, Jaros E, Perry RH, Armstrong RA (2004b) Temporal lobe pathology of human patients with neurofilament inclusion disease. Neurosci Lett 354:245–247PubMedCrossRef Cairns NJ, Jaros E, Perry RH, Armstrong RA (2004b) Temporal lobe pathology of human patients with neurofilament inclusion disease. Neurosci Lett 354:245–247PubMedCrossRef
go back to reference 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 63:1376–1384PubMedCentralPubMedCrossRef 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 63:1376–1384PubMedCentralPubMedCrossRef
go back to reference 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 114:5–22PubMedCentralPubMedCrossRef 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 114:5–22PubMedCentralPubMedCrossRef
go back to reference Chow TW, Hynan LS, Lipton AM (2006) MMSE scores decline at a greater rate in frontotemporal degeneration than in AD. Dement Geriatr Cogn Dis 22:194–199CrossRef Chow TW, Hynan LS, Lipton AM (2006) MMSE scores decline at a greater rate in frontotemporal degeneration than in AD. Dement Geriatr Cogn Dis 22:194–199CrossRef
go back to reference 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 35:851–864PubMedCrossRef 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 35:851–864PubMedCrossRef
go back to reference 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 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
go back to reference Davis DG, Schmitt FA, Wekstein DR, Markesbery WR (1999) Alzheimer neuropathology alterations in aged cognitively normal subjects. J Neuropath Exp Neurol 58:376–388PubMedCrossRef Davis DG, Schmitt FA, Wekstein DR, Markesbery WR (1999) Alzheimer neuropathology alterations in aged cognitively normal subjects. J Neuropath Exp Neurol 58:376–388PubMedCrossRef
go back to reference 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 69:1113–1121CrossRef 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 69:1113–1121CrossRef
go back to reference 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 18:1–11PubMedCrossRef 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 18:1–11PubMedCrossRef
go back to reference 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 97:113–118PubMedCrossRef 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 97:113–118PubMedCrossRef
go back to reference Filey CM, Kleinschimidtdemasters BJK, Gross KF (1994) Non-Alzheimer frontotemporal degenerative dementia: a neurobehavioural and pathological study. Clin Neuropathol 13:109–116 Filey CM, Kleinschimidtdemasters BJK, Gross KF (1994) Non-Alzheimer frontotemporal degenerative dementia: a neurobehavioural and pathological study. Clin Neuropathol 13:109–116
go back to reference 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 65:571–581PubMedCrossRef 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 65:571–581PubMedCrossRef
go back to reference 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 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
go back to reference 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 100:29–35PubMedCrossRef 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 100:29–35PubMedCrossRef
go back to reference 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 74:189–192PubMed 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 74:189–192PubMed
go back to reference Glenner GG, Wong CW (1984) Alzheimer’s disease and Down’s syndrome: sharing of a unique cerebrovascular amyloid fibril protein. Biochem Biophys Res Commun 122:1131–1135PubMedCrossRef Glenner GG, Wong CW (1984) Alzheimer’s disease and Down’s syndrome: sharing of a unique cerebrovascular amyloid fibril protein. Biochem Biophys Res Commun 122:1131–1135PubMedCrossRef
go back to reference Goedert M, Clavaguera F, Tolnay M (2010) The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci 33:317–325PubMedCrossRef Goedert M, Clavaguera F, Tolnay M (2010) The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci 33:317–325PubMedCrossRef
go back to reference 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 53:1284–1291PubMedCrossRef 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 53:1284–1291PubMedCrossRef
go back to reference Gray JA (1987) The Neuropsychology of Anxiety. Oxford University Press, New York, pp 1–548 Gray JA (1987) The Neuropsychology of Anxiety. Oxford University Press, New York, pp 1–548
go back to reference Gray JA, McNaughton N (2000) The neuropsychology of anxiety: an enquiry into the functions of the septo-hippocampal system. Oxford University Press, New York Gray JA, McNaughton N (2000) The neuropsychology of anxiety: an enquiry into the functions of the septo-hippocampal system. Oxford University Press, New York
go back to reference 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 56:1119–1124PubMedCrossRef 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 56:1119–1124PubMedCrossRef
go back to reference Guillozet AL, Weintraub S, Mash DC, Mesulam MM (2003) Neurofibrillary tangles, amyloid, and memory in aging and mild cognitive deficit. Arch Neurol Chic 60:729–736CrossRef Guillozet AL, Weintraub S, Mash DC, Mesulam MM (2003) Neurofibrillary tangles, amyloid, and memory in aging and mild cognitive deficit. Arch Neurol Chic 60:729–736CrossRef
go back to reference 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 44:2015–2019PubMedCrossRef 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 44:2015–2019PubMedCrossRef
go back to reference Head D, Snyder AZ, Girton LE, Morris JC, Buckner RL (2005) Fronto-hippocampal double dissociation between normal aging and Alzheimer’s disease. Cereb Cortex 15:732–739PubMedCrossRef Head D, Snyder AZ, Girton LE, Morris JC, Buckner RL (2005) Fronto-hippocampal double dissociation between normal aging and Alzheimer’s disease. Cereb Cortex 15:732–739PubMedCrossRef
go back to reference 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 1184:284–294PubMedCrossRef 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 1184:284–294PubMedCrossRef
go back to reference Hoesen GW, Solodkin A (1993) Some modular features of temporal cortex in humans as revealed by pathological changes in Alzheimer’s disease. Cereb Cortex 3:465–475PubMedCrossRef Hoesen GW, Solodkin A (1993) Some modular features of temporal cortex in humans as revealed by pathological changes in Alzheimer’s disease. Cereb Cortex 3:465–475PubMedCrossRef
go back to reference Hof PR, Delacourte A, Bouras C (1992) Distribution of cortical neurofibrillary tangles in progressive supranuclear palsy: a quantitative analysis of six cases. Acta Neuropathol 84:45–51PubMedCrossRef Hof PR, Delacourte A, Bouras C (1992) Distribution of cortical neurofibrillary tangles in progressive supranuclear palsy: a quantitative analysis of six cases. Acta Neuropathol 84:45–51PubMedCrossRef
go back to reference 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 87:115–124PubMedCrossRef 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 87:115–124PubMedCrossRef
go back to reference 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 52:379–391PubMedCrossRef 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 52:379–391PubMedCrossRef
go back to reference Hoke A, Canning DR, Malemud CJ, Silver J (1994) Regional differences in reactive gliosis induced by substrate-bound β-amyloid. Exp Neurol 130:56–66PubMedCrossRef Hoke A, Canning DR, Malemud CJ, Silver J (1994) Regional differences in reactive gliosis induced by substrate-bound β-amyloid. Exp Neurol 130:56–66PubMedCrossRef
go back to reference 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 52:373–378PubMedCrossRef 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 52:373–378PubMedCrossRef
go back to reference Ironside JW, Head MW, Bell JE, McCardle L, Will RG (2000) Laboratory diagnosis of variant Creutzfeldt-Jakob disease. Histopathology 37:1–9PubMedCrossRef Ironside JW, Head MW, Bell JE, McCardle L, Will RG (2000) Laboratory diagnosis of variant Creutzfeldt-Jakob disease. Histopathology 37:1–9PubMedCrossRef
go back to reference 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 49:786–794PubMedCentralPubMedCrossRef 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 49:786–794PubMedCentralPubMedCrossRef
go back to reference 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 51:993–999PubMedCentralPubMedCrossRef 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 51:993–999PubMedCentralPubMedCrossRef
go back to reference Jackson M, Lowe J (1996) The new neuropathology of degenerative fronto-temporal dementias. Acta Neuropathol 91:127–134PubMedCrossRef Jackson M, Lowe J (1996) The new neuropathology of degenerative fronto-temporal dementias. Acta Neuropathol 91:127–134PubMedCrossRef
go back to reference Josephs KA, Dickson DW (2007) Hippocampal sclerosis in tau-negtative frontotemporal lobar degeneration. Neurobiol Aging 28:1718–1722PubMedCrossRef Josephs KA, Dickson DW (2007) Hippocampal sclerosis in tau-negtative frontotemporal lobar degeneration. Neurobiol Aging 28:1718–1722PubMedCrossRef
go back to reference 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 108:515–523PubMedCrossRef 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 108:515–523PubMedCrossRef
go back to reference 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 19:488–493PubMedCentralPubMedCrossRef 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 19:488–493PubMedCentralPubMedCrossRef
go back to reference 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 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
go back to reference 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 108:207–212PubMedCrossRef 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 108:207–212PubMedCrossRef
go back to reference 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 45:2135–2146PubMedCrossRef 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 45:2135–2146PubMedCrossRef
go back to reference 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 54:581–586PubMedCrossRef 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 54:581–586PubMedCrossRef
go back to reference 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 15:106–114CrossRef 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 15:106–114CrossRef
go back to reference 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 47:1–9PubMedCrossRef 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 47:1–9PubMedCrossRef
go back to reference 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 55:97–105PubMedCrossRef 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 55:97–105PubMedCrossRef
go back to reference 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 112:539–549PubMedCentralPubMedCrossRef 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 112:539–549PubMedCentralPubMedCrossRef
go back to reference 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 10:179–187CrossRef 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 10:179–187CrossRef
go back to reference Masullo C, Macchi G (1997) Resistance of the hippocampus in Creutzfeldt–Jakob disease. Clin Neuropathol 16:37–44PubMed Masullo C, Macchi G (1997) Resistance of the hippocampus in Creutzfeldt–Jakob disease. Clin Neuropathol 16:37–44PubMed
go back to reference 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 3:212–217PubMedCentralPubMedCrossRef 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 3:212–217PubMedCentralPubMedCrossRef
go back to reference 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 47:1113–1124PubMedCrossRef 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 47:1113–1124PubMedCrossRef
go back to reference 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 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
go back to reference Meiner Z, Newman JP, Rosenman H, Soffer D, Steiner I (2005) Frontotemporal dementia with ubiquinated neuronal inclusions and visuospatial impairment. Neurology 65:478–480PubMedCrossRef Meiner Z, Newman JP, Rosenman H, Soffer D, Steiner I (2005) Frontotemporal dementia with ubiquinated neuronal inclusions and visuospatial impairment. Neurology 65:478–480PubMedCrossRef
go back to reference 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 41:479–486PubMedCrossRef 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 41:479–486PubMedCrossRef
go back to reference 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 104:455–461PubMed 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 104:455–461PubMed
go back to reference Nauta WJH, Feirtag M (1986) Fundamental neuroanatomy. WH Freeman, New York Nauta WJH, Feirtag M (1986) Fundamental neuroanatomy. WH Freeman, New York
go back to reference O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, Oxford O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, Oxford
go back to reference 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 32:1296–1303PubMedCrossRef 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 32:1296–1303PubMedCrossRef
go back to reference Pike CJ, Cotman CW (1995) Calretinin-immunoreactive neurons are resistant to b-amyloid toxicity in vitro. Brain Res 671:293–298PubMedCrossRef Pike CJ, Cotman CW (1995) Calretinin-immunoreactive neurons are resistant to b-amyloid toxicity in vitro. Brain Res 671:293–298PubMedCrossRef
go back to reference Poon MA, Stuckey S, Storey E (2001) MRI evidence of cerebellar and hippocampal involvement in Creutzfeldt–Jakob disease. Neuroradiol 43:746–749CrossRef Poon MA, Stuckey S, Storey E (2001) MRI evidence of cerebellar and hippocampal involvement in Creutzfeldt–Jakob disease. Neuroradiol 43:746–749CrossRef
go back to reference Probst A, Taylor KI, Tolnay M (2007) Hippocampal sclerosis dementia: a reappraisal. Acta Neuropathol 114:335–345PubMedCrossRef Probst A, Taylor KI, Tolnay M (2007) Hippocampal sclerosis dementia: a reappraisal. Acta Neuropathol 114:335–345PubMedCrossRef
go back to reference 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:e85595PubMedCentralPubMedCrossRef 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:e85595PubMedCentralPubMedCrossRef
go back to reference Reyes E, Gamboa A, Masliah E (1993) Atypical diffuse Lewy body disease with neuritic abnormalities. Clin Neuropathol 12:330–334PubMed Reyes E, Gamboa A, Masliah E (1993) Atypical diffuse Lewy body disease with neuritic abnormalities. Clin Neuropathol 12:330–334PubMed
go back to reference 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 124:1948–1957PubMedCrossRef 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 124:1948–1957PubMedCrossRef
go back to reference 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 63:643–656PubMedCrossRef 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 63:643–656PubMedCrossRef
go back to reference 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 20:493–501PubMedCrossRef 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 20:493–501PubMedCrossRef
go back to reference 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 23:389–398PubMedCrossRef 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 23:389–398PubMedCrossRef
go back to reference Schmidt R (1992) Comparison of magnetic-resonance-imaging in Alzheimer’s disease, vascular dementia and normal aging. Eur Neurol 32:164–169PubMedCrossRef Schmidt R (1992) Comparison of magnetic-resonance-imaging in Alzheimer’s disease, vascular dementia and normal aging. Eur Neurol 32:164–169PubMedCrossRef
go back to reference Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol 20:11–21 Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol 20:11–21
go back to reference Seritan AL, Mendez MF, Silverman DHS, Hurley RA, Taber KH (2004) Functional imaging as a window to dementia: corticobasal degeneration. J Neuropsych Clin Neurol 16:393–399CrossRef Seritan AL, Mendez MF, Silverman DHS, Hurley RA, Taber KH (2004) Functional imaging as a window to dementia: corticobasal degeneration. J Neuropsych Clin Neurol 16:393–399CrossRef
go back to reference 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 25:439–444CrossRef 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 25:439–444CrossRef
go back to reference 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 46:62–69PubMedCrossRef 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 46:62–69PubMedCrossRef
go back to reference 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 130:911–925PubMedCrossRef 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 130:911–925PubMedCrossRef
go back to reference 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 227:157–160PubMedCrossRef 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 227:157–160PubMedCrossRef
go back to reference 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 38:359–364PubMedCrossRef 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 38:359–364PubMedCrossRef
go back to reference 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 11:578–598PubMedCrossRef 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 11:578–598PubMedCrossRef
go back to reference 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 93:7–12CrossRef 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 93:7–12CrossRef
go back to reference 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 96:445–452PubMedCrossRef 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 96:445–452PubMedCrossRef
go back to reference 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 105:797–806PubMedCrossRef 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 105:797–806PubMedCrossRef
go back to reference 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 130:1777–1786PubMedCentralPubMedCrossRef 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 130:1777–1786PubMedCentralPubMedCrossRef
go back to reference 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 347:921–925PubMedCrossRef 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 347:921–925PubMedCrossRef
go back to reference Woulfe J, Kertesz A, Munoz DG (2001) Frontotemporal dementia with ubiquinated cytoplasmic and intranuclear inclusions. Acta Neuropathol 102:94–102PubMed Woulfe J, Kertesz A, Munoz DG (2001) Frontotemporal dementia with ubiquinated cytoplasmic and intranuclear inclusions. Acta Neuropathol 102:94–102PubMed
go back to reference 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 100:2333–2340PubMedCentralPubMedCrossRef 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 100:2333–2340PubMedCentralPubMedCrossRef
go back to reference 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 24:296–301PubMedCrossRef 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 24:296–301PubMedCrossRef
go back to reference 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 101:256–270PubMed 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 101:256–270PubMed
go back to reference 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 120:55–66CrossRef 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 120:55–66CrossRef
Metadata
Title
Comparative quantitative study of ‘signature’ pathological lesions in the hippocampus and adjacent gyri of 12 neurodegenerative disorders
Authors
Richard A. Armstrong
Nigel J. Cairns
Publication date
01-10-2015
Publisher
Springer Vienna
Published in
Journal of Neural Transmission / Issue 10/2015
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI
https://doi.org/10.1007/s00702-015-1402-8

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