Morphometric analysis of medial temporal lobe subregions in Alzheimer's disease using high-resolution MRI.
Alzheimer's disease
Amygdala nuclei
Hippocampal subfields
Magnetic resonance imaging
Morphometric analysis
Journal
Brain structure & function
ISSN: 1863-2661
Titre abrégé: Brain Struct Funct
Pays: Germany
ID NLM: 101282001
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
received:
16
01
2023
accepted:
07
07
2023
medline:
25
9
2023
pubmed:
24
7
2023
entrez:
24
7
2023
Statut:
ppublish
Résumé
The spread pattern of progressive degeneration seen in Alzheimer's disease (AD) to small-scale medial temporal lobe subregions is critical for early diagnosis. In this context, it was aimed to examine the morphometric changes of the hippocampal subfields, amygdala nuclei, entorhinal cortex (ERC), and parahippocampal cortex (PHC) using MRI. MRI data of patients diagnosed with 20 Alzheimer's disease dementia (ADD), 30 amnestic mild cognitive impairment (aMCI), and 30 subjective cognitive impairment (SCI) without demographic differences were used. Segmentation and parcellation were performed using FreeSurfer. The segmentation process obtained volume values of 12 hippocampal subfields and 9 amygdala nuclei. Thickness values of ERC and PHC were calculated with the parcellation process. ANCOVA was performed using age, education and gender as covariates to evaluate the intergroup differences. Linear discriminant analysis was used to investigate whether atrophy predicted groups at an early stage. ERC and PHC thickness decreased significantly throughout the disease continuum, while only ERC was affected in the early stage. When the hippocampal and amygdala subfields were compared volumetrically, significant differences were found in the amygdala between the SCI and aMCI groups. In the early period, only volume reduction in the anterior amygdaloid area of the amygdala nuclei exceeded the significance threshold. Research on AD primarily focuses on original hippocampocentric structures and their main function which is episodic memory. Our results emphasized the significance of so far relatively neglected olfactocentric structures and their functions, such as smell and social cognition in the pre-dementia stages of the AD process.
Identifiants
pubmed: 37486408
doi: 10.1007/s00429-023-02683-2
pii: 10.1007/s00429-023-02683-2
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1885-1899Subventions
Organisme : Istanbul University Research Projects Unit
ID : TSA-2022-39128
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Arriagada PV, Growdon JH, Hedley-Whyte ET, Hyman BT (1992) Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 42(3):631. https://doi.org/10.1212/WNL.42.3.631
doi: 10.1212/WNL.42.3.631
pubmed: 1549228
Beacher F, Daly E, Simmons A, Prasher V, Morris R, Robinson C, Murphy DGM (2009) Alzheimer’s disease and down’s syndrome: an in vivo MRI study. Psychol Med 39(4):675–684. https://doi.org/10.1017/S0033291708004054
doi: 10.1017/S0033291708004054
pubmed: 18667098
Betthauser TJ, Koscik RL, Jonaitis EM, Allison SL, Cody KA, Erickson CM, Clark LR (2020) Amyloid and tau imaging biomarkers explain cognitive decline from late middle-age. Brain 143(1):320–335. https://doi.org/10.1093/brain/awz378
doi: 10.1093/brain/awz378
pubmed: 31886494
Braak H, Braak E (1991) Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 82(4):239–259. https://doi.org/10.1007/BF00308809
doi: 10.1007/BF00308809
pubmed: 1759558
Braak H, Braak E (1995) Staging of Alzheimer’s disease-related neurofibrillary changes. Neurobiol Aging 16(3):271–284. https://doi.org/10.1016/0197-4580(95)00021-6
doi: 10.1016/0197-4580(95)00021-6
pubmed: 7566337
Buschke H (1984) Cued recall in amnesia. J Clin Neuropsychol 6(4):433–440. https://doi.org/10.1080/01688638408401233
doi: 10.1080/01688638408401233
pubmed: 6501581
Cherubini A, Péran P, Spoletini I, Di Paola M, Di Iulio F, Hagberg GE, Caltagirone C (2010) Combined volumetry and DTI in subcortical structures of mild cognitive impairment and Alzheimer’s disease patients. J Alzheimer’s Dis 19(4):1273–1282. https://doi.org/10.3233/JAD-2010-091186
doi: 10.3233/JAD-2010-091186
Cuénod C-A, Denys A, Michot J-L, Jehenson P, Forette F, Kaplan D, Boller F (1993) Amygdala atrophy in Alzheimer’s disease: an in vivo magnetic resonance imaging study. Archiv Neurol 50(9):941–945. https://doi.org/10.1001/archneur.1993.00540090046009
doi: 10.1001/archneur.1993.00540090046009
Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis I segmentation and surface reconstruction. Neuroimage 9(2):179–194. https://doi.org/10.1006/nimg.1998.0395
doi: 10.1006/nimg.1998.0395
pubmed: 9931268
De Flores R, La Joie R, Chételat G (2015) Structural imaging of hippocampal subfields in healthy aging and Alzheimer’s disease. Neuroscience 309:29–50. https://doi.org/10.1016/j.neuroscience.2015.08.033
doi: 10.1016/j.neuroscience.2015.08.033
pubmed: 26306871
de Vasconcelos LG, Jackowski AP, de Oliveira MO, Flor YMR, Bueno OFA, Brucki SMD (2011) Voxel-based morphometry findings in Alzheimer’s disease: neuropsychiatric symptoms and disability correlations-preliminary results. Clinics 66(6):1045–1050. https://doi.org/10.1590/S1807-59322011000600021
doi: 10.1590/S1807-59322011000600021
pubmed: 21808873
Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Hyman BT (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31(3):968–980. https://doi.org/10.1016/j.neuroimage.2006.01.021
doi: 10.1016/j.neuroimage.2006.01.021
pubmed: 16530430
DeTure MA, Dickson DW (2019) The neuropathological diagnosis of Alzheimer’s disease. Mol Neurodegener 14(1):32. https://doi.org/10.1186/s13024-019-0333-5
doi: 10.1186/s13024-019-0333-5
pubmed: 31375134
pmcid: 6679484
Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33(3):341–355. https://doi.org/10.1016/s0896-6273(02)00569-x
doi: 10.1016/s0896-6273(02)00569-x
pubmed: 11832223
Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatric Res 12(3):189–198. https://doi.org/10.1016/0022-3956(75)90026-6
doi: 10.1016/0022-3956(75)90026-6
Förster S, Vaitl A, Teipel SJ, Yakushev I, Mustafa M, la Fougère C, Hampel H (2010) Functional representation of olfactory impairment in early Alzheimer’s disease. J Alzheimer’s Dis 22(2):581–591. https://doi.org/10.3233/JAD-2010-091549
doi: 10.3233/JAD-2010-091549
Fox NC, Warrington EK, Freeborough PA, Hartikainen P, Kennedy AM, Stevens JM, Rossor MN (1996) Presymptomatic hippocampal atrophy in Alzheimer’s disease: a longitudinal MRI study. Brain 119(6):2001–2007. https://doi.org/10.1093/brain/119.6.2001
doi: 10.1093/brain/119.6.2001
pubmed: 9010004
Giaccio RG (2006) The dual origin hypothesis: An evolutionary brain-behavior framework for analyzing psychiatric disorders. Neurosci Biobehav Rev 30(4):526–550. https://doi.org/10.1016/j.neubiorev.2005.04.021
doi: 10.1016/j.neubiorev.2005.04.021
pubmed: 16356547
Golebiowski M, Barcikowska M, Pfeffer A (1999) Magnetic resonance imaging-based hippocampal volumetry in patients with dementia of the Alzheimer type. Dement Geriatr Cogn Disord 10(4):284–288. https://doi.org/10.1159/000017133
doi: 10.1159/000017133
pubmed: 10364646
Grober E, Sanders AE, Hall C, Lipton RB (2010) Free and cued selective reminding identifies very mild dementia in primary care. Alzheimer Dis Assoc Disord 24(3):284–290. https://doi.org/10.1097/WAD.0b013e3181cfc78b
doi: 10.1097/WAD.0b013e3181cfc78b
pubmed: 20683186
pmcid: 2929322
Herzog AG, Kemper TL (1980) Amygdaloid changes in aging and dementia. Arch Neurol 37(10):625–629. https://doi.org/10.1001/archneur.1980.00500590049006
doi: 10.1001/archneur.1980.00500590049006
pubmed: 7425886
Heun R, Mazanek M, Atzor K-R, Tintera J, Gawehn J, Burkart M, Stoeter P (1997) Amygdala-hippocampal atrophy and memory performance in dementia of Alzheimer type. Dementia Geriatric Cognit Disord 8(6):329–336. https://doi.org/10.1159/000106651
doi: 10.1159/000106651
Horínek D, Varjassyová A, Hort J (2007) Magnetic resonance analysis of amygdalar volume in Alzheimer’s disease. Curr Opin Psychiatry 20(3):273–277. https://doi.org/10.1097/YCO.0b013e3280ebb613
doi: 10.1097/YCO.0b013e3280ebb613
pubmed: 17415082
Iglesias JE, Augustinack JC, Nguyen K, Player CM, Player A, Wright M, Van Leemput K (2015) A computational atlas of the hippocampal formation using ex vivo, ultra-high resolution MRI: application to adaptive segmentation of in vivo MRI. Neuroimage 115:117–137. https://doi.org/10.1016/j.neuroimage.2015.04.042
doi: 10.1016/j.neuroimage.2015.04.042
pubmed: 25936807
Insel PS, Young CB, Johnson KA, Sperling RA, Mormino EC, Donohue MC (2023) Tau positron emission tomography in preclinical Alzheimer’s disease. Brain 146(2):700–711. https://doi.org/10.1093/brain/awac299
doi: 10.1093/brain/awac299
pubmed: 35962782
Ivnik RJ, Smith GE, Lucas JA, Tangalos EG, Kokmen E, Petersen RC (1997) Free and cued selective reminding test: MOANS norms. J Clin Exp Neuropsychol 19(5):676–691. https://doi.org/10.1080/01688639708403753
doi: 10.1080/01688639708403753
pubmed: 9408798
Jack CRJ, Knopman DS, Jagust WJ, Shaw LM, Aisen PS, Weiner MW, Trojanowski JQ (2010) Hypothetical model of dynamic biomarkers of the Alzheimer’s pathological cascade. Lancet Neurol 9(1):119–128. https://doi.org/10.1016/S1474-4422(09)70299-6
doi: 10.1016/S1474-4422(09)70299-6
pubmed: 20083042
pmcid: 2819840
Jack CR, Barkhof F, Bernstein MA, Cantillon M, Cole PE, DeCarli C, Frisoni GB (2011) Steps to standardization and validation of hippocampal volumetry as a biomarker in clinical trials and diagnostic criterion for Alzheimer’s disease. Alzheimer Dementia 7(4):474–485. https://doi.org/10.1016/j.jalz.2011.04.007
doi: 10.1016/j.jalz.2011.04.007
Jessen F, Wolfsgruber S, Wiese B, Bickel H, Mösch E, Kaduszkiewicz H, Wagner M (2014) AD dementia risk in late MCI, in early MCI, and in subjective memory impairment Alzheimer’s & Dementia. J Alzheimer’s Assoc 10(1):76–83. https://doi.org/10.1016/j.jalz.2012.09.017
doi: 10.1016/j.jalz.2012.09.017
Kotecha AM, Corrêa ADC, Fisher KM, Rushworth JV (2018) Olfactory dysfunction as a global biomarker for sniffing out Alzheimer’s disease: a meta-analysis. Biosensors 8(2):41. https://doi.org/10.3390/bios8020041
doi: 10.3390/bios8020041
pubmed: 29652815
pmcid: 6023101
Lehmann M, Douiri A, Kim LG, Modat M, Chan D, Ourselin S, Fox NC (2010) Atrophy patterns in Alzheimer’s disease and semantic dementia: a comparison of FreeSurfer and manual volumetric measurements. Neuroimage 49(3):2264–2274. https://doi.org/10.1016/j.neuroimage.2009.10.056
doi: 10.1016/j.neuroimage.2009.10.056
pubmed: 19874902
Liu Y, Paajanen T, Zhang Y, Westman E, Wahlund L-O, Simmons A, Tsolaki M (2010) Analysis of regional MRI volumes and thicknesses as predictors of conversion from mild cognitive impairment to Alzheimer’s disease. Neurobiol Aging 31(8):1375–1385. https://doi.org/10.1016/j.neurobiolaging.2010.01.022
doi: 10.1016/j.neurobiolaging.2010.01.022
pubmed: 20447732
Lockhart SN, Schöll M, Baker SL, Ayakta N, Swinnerton KN, Bell RK, Janabi M (2017) Amyloid and tau PET demonstrate region-specific associations in normal older people. Neuroimage 150:191–199. https://doi.org/10.1016/j.neuroimage.2017.02.051
doi: 10.1016/j.neuroimage.2017.02.051
pubmed: 28232190
Mai JK, Paxinos G (2011) The human nervous system. Academic Press. https://doi.org/10.1016/C2009-0-02721-4
doi: 10.1016/C2009-0-02721-4
McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CRJ, Kawas CH, Phelps CH (2011) The diagnosis of dementia due to Alzheimer’s disease: recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease Alzheimer’s & dementia. J Alzheimer’s Assoc 7(3):263–269. https://doi.org/10.1016/j.jalz.2011.03.005
doi: 10.1016/j.jalz.2011.03.005
Molinuevo JL, Rabin LA, Amariglio R, Buckley R, Dubois B, Ellis KA, Group, S. C. D. I. (SCD-I. W) (2017) Implementation of subjective cognitive decline criteria in research studies Alzheimer’s and dementia. J Alzheimer’s Assoc 13(3):296–311. https://doi.org/10.1016/j.jalz.2016.09.012
doi: 10.1016/j.jalz.2016.09.012
Morris JC (1991) The clinical dementia rating (cdr): current version and. Young 41:1588–1592. https://doi.org/10.1212/WNL.43.11.2412-a
doi: 10.1212/WNL.43.11.2412-a
Pandya D, Petrides M, Cipolloni PB (2015) Cerebral cortex: architecture, connections, and the dual origin concept. Oxford University Press. https://doi.org/10.1093/med/9780195385151.001.0001
doi: 10.1093/med/9780195385151.001.0001
Petersen RC (2004) Mild cognitive impairment as a diagnostic entity. J Intern Med 256(3):183–194. https://doi.org/10.1111/j.1365-2796.2004.01388.x
doi: 10.1111/j.1365-2796.2004.01388.x
pubmed: 15324362
Poulin SP, Dautoff R, Morris JC, Barrett LF, Dickerson BC, Initiative ADN (2011) Amygdala atrophy is prominent in early Alzheimer’s disease and relates to symptom severity. Psychiatry Res Neuroimaging 194(1):7–13. https://doi.org/10.1016/j.pscychresns.2011.06.014
doi: 10.1016/j.pscychresns.2011.06.014
Price JL, Morris JC (1999) Tangles and plaques in nondemented aging and “preclinical” Alzheimer’s disease. Ann Neurol 45(3):358–368. https://doi.org/10.1002/1531-8249(199903)45:3%3c358::AID-ANA12%3e3.0.CO;2-X
doi: 10.1002/1531-8249(199903)45:3<358::AID-ANA12>3.0.CO;2-X
pubmed: 10072051
Price JL, Davis PB, Morris JC, White DL (1991) The distribution of tangles, plaques and related immunohistochemical markers in healthy aging and Alzheimer’s disease. Neurobiol Aging 12(4):295–312. https://doi.org/10.1016/0197-4580(91)90006-6
doi: 10.1016/0197-4580(91)90006-6
pubmed: 1961359
Quarmley M, Moberg PJ, Mechanic-Hamilton D, Kabadi S, Arnold SE, Wolk DA, Roalf DR (2017) Odor identification screening improves diagnostic classification in incipient Alzheimer’s disease. J Alzheimer’s Dis 55(4):1497–1507. https://doi.org/10.3233/JAD-160842
doi: 10.3233/JAD-160842
Roberts RO, Geda YE, Knopman DS, Cha RH, Pankratz VS, Boeve BF, Rocca WA (2008) The mayo clinic study of aging: design and sampling, participation, baseline measures and sample characteristics. Neuroepidemiology 30(1):58–69. https://doi.org/10.1159/000115751
doi: 10.1159/000115751
pubmed: 18259084
pmcid: 2821441
Sanabria-Castro A, Alvarado-Echeverría I, Monge-Bonilla C (2017) Molecular pathogenesis of Alzheimer’s disease: an update. Ann Neurosci 24(1):46–54. https://doi.org/10.1159/000464422
doi: 10.1159/000464422
pubmed: 28588356
pmcid: 5448443
Saygin ZM, Kliemann D, Iglesias JE, van der Kouwe AJW, Boyd E, Reuter M, Frosch MP (2017) High-resolution magnetic resonance imaging reveals nuclei of the human amygdala: manual segmentation to automatic atlas. Neuroimage 155:370–382. https://doi.org/10.1016/j.neuroimage.2017.04.046
doi: 10.1016/j.neuroimage.2017.04.046
pubmed: 28479476
Scheltens P, Leys D, Barkhof F, Huglo D, Weinstein HC, Vermersch P, Valk J (1992) Atrophy of medial temporal lobes on MRI in “probable” Alzheimer’s disease and normal ageing: diagnostic value and neuropsychological correlates. J Neurol Neurosurg Psychiatry 55(10):967–972. https://doi.org/10.1136/jnnp.55.10.967
doi: 10.1136/jnnp.55.10.967
pubmed: 1431963
pmcid: 1015202
Schöll M, Lockhart SN, Schonhaut DR, O’Neil JP, Janabi M, Ossenkoppele R, Schwimmer HD (2016) PET imaging of tau deposition in the aging human brain. Neuron 89(5):971–982. https://doi.org/10.1016/j.neuron.2016.01.028
doi: 10.1016/j.neuron.2016.01.028
pubmed: 26938442
pmcid: 4779187
Schultz C, Engelhardt M (2014) Anatomy of the hippocampal formation. Front Neurol Neurosci 34:6–17. https://doi.org/10.1159/000360925
doi: 10.1159/000360925
pubmed: 24777126
Scott SA, Sparks DL, Scheff SW, Dekosky ST, Knox CA (1992) Amygdala cell loss and atrophy in Alzheimer’s disease. Ann Neurol 32(4):555–563. https://doi.org/10.1002/ana.410320412
doi: 10.1002/ana.410320412
pubmed: 1456740
Seligman SC, Kamath V, Giovannetti T, Arnold SE, Moberg PJ (2013) Olfaction and apathy in Alzheimer’s disease, mild cognitive impairment, and healthy older adults. Aging Ment Health 17(5):564–570. https://doi.org/10.1080/13607863.2013.768208
doi: 10.1080/13607863.2013.768208
pubmed: 23398350
pmcid: 3664659
Small SA, Schobel SA, Buxton RB, Witter MP, Barnes CA (2011) A pathophysiological framework of hippocampal dysfunction in ageing and disease. Nat Rev Neurosci 12(10):585–601. https://doi.org/10.1038/nrn3085
doi: 10.1038/nrn3085
pubmed: 21897434
pmcid: 3312472
Sperling RA, Mormino EC, Schultz AP, Betensky RA, Papp KV, Amariglio RE, Hedden T (2019) The impact of amyloid-beta and tau on prospective cognitive decline in older individuals. Ann Neurol 85(2):181–193. https://doi.org/10.1002/ana.25395
doi: 10.1002/ana.25395
pubmed: 30549303
pmcid: 6402593
Squire LR, Stark CEL, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279–306. https://doi.org/10.1146/annurev.neuro.27.070203.144130
doi: 10.1146/annurev.neuro.27.070203.144130
pubmed: 15217334
van Strien NM, Cappaert NLM, Witter MP (2009) The anatomy of memory: an interactive overview of the parahippocampal-hippocampal network. Nat Rev Neurosci 10(4):272–282. https://doi.org/10.1038/nrn2614
doi: 10.1038/nrn2614
pubmed: 19300446
Velayudhan L, Gasper A, Pritchard M, Baillon S, Messer C, Proitsi P (2015) Pattern of smell identification impairment in Alzheimer’s disease. J Alzheimer’s Dis 46(2):381–387. https://doi.org/10.3233/JAD-142838
doi: 10.3233/JAD-142838
Vemuri P, Lowe VJ, Knopman DS, Senjem ML, Kemp BJ, Schwarz CG, Jack CR Jr (2017) Tau-PET uptake: regional variation in average SUVR and impact of amyloid deposition. Alzheimer’s Dement 6:21–30. https://doi.org/10.1016/j.dadm.2016.12.010
doi: 10.1016/j.dadm.2016.12.010
Vogt LJK, Hyman BT, Van Hoesen GW, Damasio AR (1990) Pathological alterations in the amygdala in Alzheimer’s disease. Neuroscience 37(2):377–385. https://doi.org/10.1016/0306-4522(90)90408-V
doi: 10.1016/0306-4522(90)90408-V
Wang J, Eslinger PJ, Doty RL, Zimmerman EK, Grunfeld R, Sun X, Smith MB (2010) Olfactory deficit detected by fMRI in early Alzheimer’s disease. Brain Res 1357:184–194. https://doi.org/10.1016/j.brainres.2010.08.018
doi: 10.1016/j.brainres.2010.08.018
pubmed: 20709038
pmcid: 3515873
Ward AM, Calamia M, Thiemann E, Dunlap J, Tranel D (2017) Association between olfaction and higher cortical functions in Alzheimer’s disease, mild cognitive impairment, and healthy older adults. J Clin Exp Neuropsychol 39(7):646–658. https://doi.org/10.1080/13803395.2016.1253667
doi: 10.1080/13803395.2016.1253667
pubmed: 27868477
Wilson RS, Li Y, Aggarwal NT, McCann JJ, Gilley DW, Bienias JL, Evans DA (2006) Cognitive decline and survival in Alzheimer’s disease. Int J Geriatr Psychiatry 21(4):356–362. https://doi.org/10.1002/gps.1472
doi: 10.1002/gps.1472
pubmed: 16534773
Wolk DA, Das SR, Mueller SG, Weiner MW, Yushkevich PA, Initiative ADN (2017) Medial temporal lobe subregional morphometry using high resolution MRI in Alzheimer’s disease. Neurobiol Aging 49:204–213. https://doi.org/10.1016/j.neurobiolaging.2016.09.011
doi: 10.1016/j.neurobiolaging.2016.09.011
pubmed: 27836336
Yilmazer-Hanke DM (2012) Amygdala. In: Mai JK (ed) Third E. Paxinos. Academic Press, San Diego, pp 759–834. https://doi.org/10.1016/B978-0-12-374236-0.10022-7
doi: 10.1016/B978-0-12-374236-0.10022-7
Yushkevich PA, Pluta JB, Wang H, Xie L, Ding S, Gertje EC, Wolk DA (2015) Automated volumetry and regional thickness analysis of hippocampal subfields and medial temporal cortical structures in mild cognitive impairment. Hum Brain Mapp 36(1):258–287. https://doi.org/10.1002/hbm.22627
doi: 10.1002/hbm.22627
pubmed: 25181316
Yushkevich PA, Muñoz López M, de Onzoño I, Martin MM, Ittyerah R, Lim S, Ravikumar S, Wang J (2021) Three-dimensional mapping of neurofibrillary tangle burden in the human medial temporal lobe. Brain 144(9):2784–2797. https://doi.org/10.1093/brain/awab262
doi: 10.1093/brain/awab262
pubmed: 34259858
pmcid: 8783607