Entorhinal verrucae geometry is coincident and correlates with Alzheimer's lesions: A combined neuropathology and high-resolution ex vivo MRI analysis

Acta Neuropathologica

Volumn 123, Issue 1, 2012, Pages 85-96

  Augustinack, Jean C ^a   Huber, Kristen E ^a   Postelnicu, Gheorghe M ^b   Kakunoori, Sita ^a   Wang, Ruopeng ^a   Van Der Kouwe, André J W ^a   Wald, Lawrence L ^a   Stein, Thor D ^a   Frosch, Matthew P ^a   Fischl, Bruce ^a,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b GOOGLE   (Switzerland)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Cortex; Ex vivo; Modularity; Neuroimaging; Surface reconstruction

Indexed keywords

ADULT; AGE; AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN SIZE; CONTROLLED STUDY; DISEASE ASSOCIATION; ENTORHINAL CORTEX; ENTORHINAL VERRUCAE; EX VIVO STUDY; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; MALE; NEUROANATOMY; NEUROPATHOLOGY; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SEX DIFFERENCE;

ADULT; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; ENTORHINAL CORTEX; FEMALE; HIPPOCAMPUS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; NEUROFIBRILLARY TANGLES; TEMPORAL LOBE;

EID: 84857030760     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-011-0929-5     Document Type: Article

References (56)

1. T Arendt 2009 Synaptic degeneration in Alzheimer's disease Acta Neuropathol 118 167 179 19390859 10.1007/s00401-009-0536-x
2. PV Arriagada JH Growdon ET Hedley-Whyte BT Hyman 1992 Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease Neurology 42 631 639 1549228 1:STN:280:DyaK387psFCktw%3D%3D
3. PV Arriagada K Marzloff BT Hyman 1992 Distribution of Alzheimer-type pathologic changes in nondemented elderly individuals matches the pattern in Alzheimer's disease Neurology 42 1681 1688 1307688 1:STN:280: DyaK38zot1Omuw%3D%3D
4. JC Augustinack AJ van der Kouwe ML Blackwell DH Salat CJ Wiggins MP Frosch GC Wiggins A Potthast LL Wald BR Fischl 2005 Detection of entorhinal layer II using 7 Tesla magnetic resonance imaging Ann Neurol 57 489 494 15786476 10.1002/ana.20426 (Pubitemid 40471157)
5. MJ Ball 1977 Neuronal loss, neurofibrillary tangles and granulovacuolar degeneration in the hippocampus with ageing and dementia. A quantitative study Acta Neuropathol 37 111 118 848276 10.1007/BF00692056 1:STN:280: DyaE2s7ltl2rug%3D%3D (Pubitemid 8047060)
6. C Bancher K Jellinger H Lassmann P Fischer F Leblhuber 1996 Correlations between mental state and quantitative neuropathology in the Vienna Longitudinal Study on Dementia Eur Arch Psychiatry Clin Neurosci 246 137 146 8739399 10.1007/BF02189115 1:STN:280:DyaK28zhslSrtA%3D%3D (Pubitemid 26130273)
7. EL Barbier S Marrett A Danek A Vortmeyer P van Gelderen J Duyn P Bandettini J Grafman AP Koretsky 2002 Imaging cortical anatomy by high-resolution MR at 3.0 T: detection of the stripe of Gennari in visual area 17 Magn Reson Med 48 735 738 12353293 10.1002/mrm.10255
8. DA Bennett JA Schneider Z Arvanitakis JF Kelly NT Aggarwal RC Shah RS Wilson 2006 Neuropathology of older persons without cognitive impairment from two community-based studies Neurology 66 1837 1844 16801647 10.1212/01.wnl. 0000219668.47116.e6 1:STN:280:DC%2BD28zosFKjsg%3D%3D (Pubitemid 44049813)
9. DA Bennett JA Schneider JL Bienias DA Evans RS Wilson 2005 Mild cognitive impairment is related to Alzheimer disease pathology and cerebral infarctions Neurology 64 834 841 15753419 10.1212/01.WNL.0000152982.47274.9E 1:STN:280:DC%2BD2M7itlWrtg%3D%3D (Pubitemid 40316322)
10. H Braak E Braak 1991 Neuropathological staging of Alzheimer-related changes Acta Neuropathol 82 239 259 1759558 10.1007/BF00308809 1:STN:280:DyaK387gtFOiug%3D%3D
11. LM Cabalka BT Hyman CR Goodlett TC Ritchie GW Van Hoesen 1992 Alteration in the pattern of nerve terminal protein immunoreactivity in the perforant pathway in Alzheimer's disease and in rats after entorhinal lesions Neurobiol Aging 13 283 291 1522944 10.1016/0197-4580(92)90041-U 1:STN:280: DyaK38zps1aqtA%3D%3D
12. Cajal SR (1955) Studies on the cerebral cortex (translated from Spanish by Kraft LM). Yearbook Publishers, Chicago
13. VP Clark E Courchesne M Grafe 1992 In vivo myeloarchitectonic analysis of human striate and extrastriate cortex using magnetic resonance imaging Cereb Cortex 2 417 424 1422094 10.1093/cercor/2.5.417 1:STN:280:DyaK3s%2FksVamsQ%3D%3D
14. HE Cline CL Dumoulin HR Hart Jr WE Lorensen S Ludke 1987 3D reconstruction of the brain from magnetic resonance images using a connectivity algorithm Magn Reson Imaging 5 345 352 3695821 10.1016/0730-725X(87)90124-X 1:STN:280:DyaL1c%2FptlGmtQ%3D%3D (Pubitemid 17167623)
15. DG Davis FA Schmitt DR Wekstein WR Markesbery 1999 Alzheimer neuropathologic alterations in aged cognitively normal subjects J Neuropathol Exp Neurol 58 376 388 10218633 10.1097/00005072-199904000-00008 1:STN:280:DyaK1M3jtlSjsw%3D%3D (Pubitemid 29187900)
16. JH Duyn P van Gelderen TQ Li JA de Zwart AP Koretsky M Fukunaga 2007 High-field MRI of brain cortical substructure based on signal phase Proc Natl Acad Sci USA 104 11796 11801 17586684 10.1073/pnas.0610821104 1:CAS:528:DC%2BD2sXotVSntbk%3D (Pubitemid 47175092)
17. DC Ewbank SE Arnold 2009 Cool with plaques and tangles N Engl J Med 360 2357 2359 19474435 10.1056/NEJMe0901965 1:CAS:528:DC%2BD1MXmsFShtL4%3D
18. B Fischl AA Stevens N Rajendran BT Yeo DN Greve K Van Leemput JR Polimeni S Kakunoori RL Buckner J Pacheco DH Salat J Melcher MP Frosch BT Hyman PE Grant BR Rosen AJ van der Kouwe GC Wiggins LL Wald JC Augustinack 2009 Predicting the location of entorhinal cortex from MRI Neuroimage 47 8 17 19376238 10.1016/j.neuroimage.2009.04.033
19. P Giannakopoulos FR Herrmann T Bussiere C Bouras E Kovari DP Perl JH Morrison G Gold PR Hof 2003 Tangle and neuron numbers, but not amyloid load, predict cognitive status in Alzheimer's disease Neurology 60 1495 1500 12743238 1:STN:280:DC%2BD3s3it1Sqtg%3D%3D (Pubitemid 36559525)
20. T Gomez-Isla R Hollister H West S Mui JH Growdon RC Petersen JE Parisi BT Hyman 1997 Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease Ann Neurol 41 17 24 9005861 10.1002/ana.410410106 1:STN:280:DyaK2s7lvVGjsw%3D%3D (Pubitemid 27057088)
21. T Gomez-Isla JL Price DW McKeel Jr JC Morris JH Growdon BT Hyman 1996 Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease J Neurosci 16 4491 4500 8699259 1:CAS:528:DyaK28XktlamsLs%3D (Pubitemid 26243044)
22. J Hanke DM Yilmazer-Hanke 1997 Variabilities in the distribution of neurofibrillary tangles in the anterior parahippocampal gyrus at initial stages of Alzheimer's disease Clin Neuropathol 16 299 302 9401795 1:STN:280: DyaK1c%2FmsFehtQ%3D%3D (Pubitemid 27483779)
23. V Haroutunian DP Purohit DP Perl D Marin K Khan M Lantz KL Davis RC Mohs 1999 Neurofibrillary tangles in nondemented elderly subjects and mild Alzheimer disease Arch Neurol 56 713 718 10369312 10.1001/archneur.56.6.713 1:STN:280:DyaK1M3psF2rtA%3D%3D (Pubitemid 29266472)
24. O Heinonen H Soininen H Sorvari O Kosunen L Paljarvi E Koivisto PJ Riekkinen Sr 1995 Loss of synaptophysin-like immunoreactivity in the hippocampal formation is an early phenomenon in Alzheimer's disease Neuroscience 64 375 384 7700527 10.1016/0306-4522(94)00422-2 1:CAS:528:DyaK2MXjtF2gsrw%3D
25. H Heinsen R Henn W Eisenmenger M Gotz J Bohl B Bethke U Lockemann K Puschel 1994 Quantitative investigations on the human entorhinal area: left-right asymmetry and age-related changes Anat Embryol 190 181 194 7818090 10.1007/BF00193414 1:STN:280:DyaK2M7hslymug%3D%3D (Pubitemid 24277078)
26. PR Hof T Bussiere G Gold E Kovari P Giannakopoulos C Bouras DP Perl JH Morrison 2003 Stereologic evidence for persistence of viable neurons in layer II of the entorhinal cortex and the CA1 field in Alzheimer disease J Neuropathol Exp Neurol 62 55 67 12528818 (Pubitemid 36068893)
27. BT Hyman GW Van Hoesen AR Damasio CL Barnes 1984 Alzheimer's disease: cell-specific pathology isolates the hippocampal formation Science 225 1168 1170 6474172 10.1126/science.6474172 1:STN:280:DyaL2czgtVejsg%3D%3D (Pubitemid 14029099)
28. Iqbal K, Wisniewski HM, Grundke-Iqbal I, Terry RD (1977) Neurofibrillary pathology: an update. In: Nandy K, Sherwin I (eds) The aging brain and senile dementia. Plenum, New York, pp 209-227
29. Kemper T (1984) Neuroanatomical and Neuropathological changes in normal aging and in dementia kemper. In: Albert ML, Knopefel JE (eds) Clinical neurology of aging. Oxford University Press, New York, pp 9-52
30. Klinger J. (1948) Die makroskopische Anatomie der Ammonsformation. Denkschr. Schweiz. Naturforsch 78
31. DS Knopman JE Parisi A Salviati M Floriach-Robert BF Boeve RJ Ivnik GE Smith DW Dickson KA Johnson LE Petersen WC McDonald H Braak RC Petersen 2003 Neuropathology of cognitively normal elderly J Neuropathol Exp Neurol 62 1087 1095 14656067 1:STN:280:DC%2BD3srnsVWqsg%3D%3D (Pubitemid 37413820)
32. JH Kordower Y Chu GT Stebbins ST DeKosky EJ Cochran D Bennett EJ Mufson 2001 Loss and atrophy of layer II entorhinal cortex neurons in elderly people with mild cognitive impairment Ann Neurol 49 202 213 11220740 10.1002/1531-8249(20010201)49:2<202::AID-ANA40>3.0.CO;2-3 1:STN:280:DC%2BD3M7otFOgug%3D%3D (Pubitemid 32157996)
33. DM Mann D Neary PO Yates J Lincoln JS Snowden P Stanworth 1981 Alterations in protein synthetic capability of nerve cells in Alzheimer's disease J Neurol Neurosurg Psychiatry 44 97 102 6163842 10.1136/jnnp.44.2.97 1:STN:280:DyaL3M7mvFygsw%3D%3D (Pubitemid 11137899)
34. DM Mann D Neary PO Yates J Lincoln JS Snowden P Stanworth 1981 Neurofibrillary pathology and protein synthetic capability in nerve cells in Alzheimer's disease Neuropathol Appl Neurobiol 7 37 47 7231636 10.1111/j.1365-2990.1981.tb00230.x 1:CAS:528:DyaL3MXhtVWjsrY%3D (Pubitemid 12233343)
35. DM Mann PO Yates 1981 The relationship between formation of senile plaques and neurofibrillary tangles and changes in nerve cell metabolism in Alzheimer type dementia Mech Ageing Dev 17 395 401 7329104 10.1016/0047-6374(81) 90056-7 1:STN:280:DyaL387itlOlsw%3D%3D (Pubitemid 12191145)
36. WR Markesbery 2010 Neuropathologic alterations in mild cognitive impairment: a review J Alzheimers Dis 19 221 228 20061641
37. J Marksteiner WA Kaufmann P Gurka C Humpel 2002 Synaptic proteins in Alzheimer's disease J Mol Neurosci 18 53 63 11931350 10.1385/JMN:18:1-2:53 1:CAS:528:DC%2BD38XisVShsL8%3D (Pubitemid 34252624)
38. E Masliah L Crews L Hansen 2006 Synaptic remodeling during aging and in Alzheimer's disease J Alzheimers Dis 9 91 99 16914848 1:CAS:528: DC%2BD28XotFKktLg%3D (Pubitemid 44253302)
39. PT Nelson WA Kukull MP Frosch 2010 Thinking outside the box: Alzheimer-type neuropathology that does not map directly onto current consensus recommendations J Neuropathol Exp Neurol 69 449 454 20418781 10.1097/NEN.0b013e3181d8db07
40. Retzius G (1896) Das Menschenhirn. Norstedt and Sonhe, Stockholm
41. GM Savva SB Wharton PG Ince G Forster FE Matthews C Brayne 2009 Age, neuropathology, and dementia N Engl J Med 360 2302 2309 19474427 10.1056/NEJMoa0806142 1:CAS:528:DC%2BD1MXmsFSjsb8%3D
42. MH Silver K Newell C Brady ET Hedley-White TT Perls 2002 Distinguishing between neurodegenerative disease and disease-free aging: correlating neuropsychological evaluations and neuropathological studies in centenarians Psychosom Med 64 493 501 12021423 (Pubitemid 34556415)
43. G Simic S Bexheti Z Kelovic M Kos K Grbic PR Hof I Kostovic 2005 Hemispheric asymmetry, modular variability and age-related changes in the human entorhinal cortex Neuroscience 130 911 925 15652989 10.1016/j.neuroscience.2004. 09.040 1:CAS:528:DC%2BD2MXksVeqtA%3D%3D (Pubitemid 40094624)
44. A Solodkin GW Van Hoesen 1996 Entorhinal cortex modules of the human brain J Comp Neurol 365 610 617 8742306 10.1002/(SICI)1096-9861(19960219)365: 4<610::AID-CNE8>3.0.CO;2-7 1:STN:280:DyaK28zlt1Cqsw%3D%3D (Pubitemid 26069260)
45. CI Sze JC Troncoso C Kawas P Mouton DL Price LJ Martin 1997 Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease J Neuropathol Exp Neurol 56 933 944 9258263 10.1097/00005072-199708000-00011 1:STN:280:DyaK2svgt1yrtw%3D%3D (Pubitemid 27329114)
46. Terry RD. (1995) Biologic differences between early- and late-onset Alzheimer disease. Alzheimer Dis Assoc Dis 9(Suppl 1): S26-S27
47. RD Terry 2000 Cell death or synaptic loss in Alzheimer disease J Neuropathol Exp Neurol 59 1118 1119 11138931 1:STN:280:DC%2BD3M%2FotVyitw%3D%3D (Pubitemid 32006314)
48. RD Terry R DeTeresa LA Hansen 1987 Neocortical cell counts in normal human adult aging Ann Neurol 21 530 539 3606042 10.1002/ana.410210603 1:STN:280:DyaL2s3mvFChtg%3D%3D (Pubitemid 17081187)
49. JA van de Nes R Nafe W Schlote 2008 Non-tau based neuronal degeneration in Alzheimer's disease-an immunocytochemical and quantitative study in the supragranular layers of the middle temporal neocortex Brain Res 1213 152 165 18455153 10.1016/j.brainres.2008.03.043
50. AJ van der Kouwe T Benner AM Dale 2006 Real-time rigid body motion correction and shimming using cloverleaf navigators Magn Reson Med 56 1019 1032 17029223 10.1002/mrm.21038 (Pubitemid 44691344)
51. G Van Hoesen DN Pandya 1975 Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents Brain Res 95 1 24 1156859 10.1016/0006-8993(75)90204-8
52. GW Van Hoesen 1995 Anatomy of the medial temporal lobe Magn Reson Imaging 13 1047 1055 8750316 10.1016/0730-725X(95)02012-I
53. GW Van Hoesen JC Augustinack J Dierking SJ Redman R Thangavel 2000 The parahippocampal gyrus in Alzheimer's disease. Clinical and preclinical neuroanatomical correlates Ann N Y Acad Sci 911 254 274 10911879 10.1111/j.1749-6632.2000.tb06731.x (Pubitemid 30462087)
54. GW Van Hoesen BT Hyman AR Damasio 1991 Entorhinal cortex pathology in Alzheimer's disease Hippocampus 1 1 8 1669339 10.1002/hipo.450010102
55. GW Van Hoesen A Solodkin 1993 Some modular features of temporal cortex in humans as revealed by pathological changes in Alzheimer's disease Cereb Cortex 3 465 475 7505138 10.1093/cercor/3.5.465 (Pubitemid 23303423)
56. HM Wisniewski D Soifer 1979 Neurofibrillary pathology: current status and research perspectives Mech Ageing Dev 9 119 142 108483 10.1016/0047-6374(79) 90125-8 1:CAS:528:DyaE1MXhtVWhu7w%3D