Unveiling the hippocampal subfield changes across the Alzheimer's disease continuum: a systematic review of neuroimaging studies.
Alzheimer’s disease continuum
Hippocampal subfields
Hippocampal volume and surface
Journal
Brain imaging and behavior
ISSN: 1931-7565
Titre abrégé: Brain Imaging Behav
Pays: United States
ID NLM: 101300405
Informations de publication
Date de publication:
23 Oct 2024
23 Oct 2024
Historique:
accepted:
10
10
2024
medline:
24
10
2024
pubmed:
24
10
2024
entrez:
23
10
2024
Statut:
aheadofprint
Résumé
Studies exploring the hippocampal subfield atrophy in Alzheimer's disease (AD) have shown contradictory results. This review aims to disentangle such heterogeneity by investigating the dynamic changes of hippocampal subfields across the AD continuum. We systematically searched the PubMed and EMBASE databases for case-control studies. Selected studies included investigations of biomarker-based amyloid status and reported data on hippocampal subfield atrophy using advanced MRI techniques. Twelve studies were included. Despite high heterogeneity, a distinguishable pattern of vulnerability of hippocampal subfields can be recognized from the cognitively unimpaired phase to the dementia stage, shedding light on hippocampal changes with disease progression. Consistent findings revealed atrophy in the subiculum and presubiculum, along with a potential increase in volume in the cornu ammonis (CA) among the cognitively unimpaired group, a feature not observed in patients experiencing subjective cognitive decline. Atrophy in the subiculum, presubiculum, CA 1-4, and the dentate gyrus characterized the mild cognitive impairment stage, with a more pronounced severity in the progression to dementia.
Identifiants
pubmed: 39443362
doi: 10.1007/s11682-024-00952-0
pii: 10.1007/s11682-024-00952-0
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Aimone, J. B., Wiles, J., & Gage, F. H. (2009). Computational influence of adult neurogenesis on memory encoding. Neuron, 61(2), 187–202. https://doi.org/10.1016/j.neuron.2008.11.026
doi: 10.1016/j.neuron.2008.11.026
pubmed: 19186162
pmcid: 2670434
Aisen, P. S., Cummings, J., Jack, C. R., Jr., Morris, J. C., Sperling, R., Frölich, L., Jones, R. W., Dowsett, S. A., Matthews, B. R., Raskin, J., Scheltens, P., & Dubois, B. (2017). On the path to 2025: understanding the Alzheimer’s disease continuum. Alzheimer’s Research & Therapy, 9(1), 60. https://doi.org/10.1186/s13195-017-0283-5
doi: 10.1186/s13195-017-0283-5
Anand, K. S., & Dhikav, V. (2012). Hippocampus in health and disease: An overview. Annals of Indian Academy of Neurology, 15(4), 239–246. https://doi.org/10.4103/0972-2327.104323
doi: 10.4103/0972-2327.104323
pubmed: 23349586
pmcid: 3548359
Baek, M. S., Lee, N., Kim, J. W., & Hong, J. Y. (2022). Association of hippocampal subfield volumes with Amyloid-Beta deposition in Alzheimer’s disease. Journal of Clinical Medicine, 11(6), 1526. https://doi.org/10.3390/jcm11061526
doi: 10.3390/jcm11061526
pubmed: 35329851
pmcid: 8955328
Baset, A., & Huang, F. (2024). Shedding light on subiculum’s role in human brain disorders. Brain Research Bulletin, 214, 110993. https://doi.org/10.1016/j.brainresbull.2024.110993
doi: 10.1016/j.brainresbull.2024.110993
pubmed: 38825254
Bejanin, A., Schonhaut, D. R., La Joie, R., Kramer, J. H., Baker, S. L., Sosa, N., Ayakta, N., Cantwell, A., Janabi, M., Lauriola, M., O’Neil, J. P., Gorno-Tempini, M. L., Miller, Z. A., Rosen, H. J., Miller, B. L., Jagust, W. J., & Rabinovici, G. D. (2017). Tau pathology and neurodegeneration contribute to cognitive impairment in Alzheimer’s disease. Brain, 140(12), 3286–3300. https://doi.org/10.1093/brain/awx243
doi: 10.1093/brain/awx243
pubmed: 29053874
pmcid: 5841139
Berron, D., Schütze, H., Maass, A., Cardenas-Blanco, A., Kuijf, H. J., Kumaran, D., & Düzel, E. (2016). Strong evidence for pattern separation in Human dentate gyrus. Journal of Neuroscience, 36(29), 7569–7579. https://doi.org/10.1523/JNEUROSCI.0518-16.2016
doi: 10.1523/JNEUROSCI.0518-16.2016
pubmed: 27445136
Berron, D., Vogel, J. W., Insel, P. S., Pereira, J. B., Xie, L., Wisse, L. E. M., Yushkevich, P. A., Palmqvist, S., Mattsson-Carlgren, N., Stomrud, E., Smith, R., Strandberg, O., & Hansson, O. (2021). Early stages of tau pathology and its associations with functional connectivity, atrophy and memory. Brain, 144(9), 2771–2783. https://doi.org/10.1093/brain/awab114
doi: 10.1093/brain/awab114
pubmed: 33725124
pmcid: 8557349
Boccardi, V., Westman, E., Pelini, L., Lindberg, O., Muehlboeck, J. S., Simmons, A., Tarducci, R., Floridi, P., Chiarini, P., Soininen, H., Kloszewska, I., Tsolaki, M., Vellas, B., Spenger, C., Wahlund, L. O., Lovestone, S., & Mecocci, P. (2019). Differential associations of IL-4 with hippocampal subfields in mild cognitive impairment and Alzheimer’s disease. Frontiers in Aging Neuroscience, 10, 439. https://doi.org/10.3389/fnagi.2018.00439
doi: 10.3389/fnagi.2018.00439
pubmed: 30705627
pmcid: 6344381
Braak, H., & Braak, E. (1991). Neuropathological stageing of Alzheimer-related changes. Acta Neuropathologica,82(4), 239–259. https://doi.org/10.1007/BF00308809
doi: 10.1007/BF00308809
pubmed: 1759558
Braak, H., & Braak, E. (1990). Morphologie des Morbus Alzheimer [Morphology of Alzheimer disease]. Fortschritte der Medizin,108(33), 621–624.
pubmed: 2289729
Caldwell, J. Z. K., Berg, J. L., Shan, G., Cummings, J. L., Banks, S. J., Alzheimer’s Disease Neuroimaging Initiative. (2018). Sex moderates the impact of diagnosis and Amyloid PET positivity on hippocampal subfield volume. Journal of Alzheimer’s Disease: JAD, 64(1), 79–89. https://doi.org/10.3233/JAD-180028
doi: 10.3233/JAD-180028
pubmed: 29865063
Carlesimo, G. A., Piras, F., Orfei, M. D., Iorio, M., Caltagirone, C., & Spalletta, G. (2015). Atrophy of presubiculum and subiculum is the earliest hippocampal anatomical marker of Alzheimer’s disease. Alzheimer’s & Dementia (Amsterdam Netherlands),1(1), 24–32. https://doi.org/10.1016/j.dadm.2014.12.001
doi: 10.1016/j.dadm.2014.12.001
Cherubini, E., & Miles, R. (2015). The CA3 region of the hippocampus: How is it? What is it for? How does it do it? Frontiers in Cellular Neuroscience, 9, 19
doi: 10.3389/fncel.2015.00019
pubmed: 25698930
pmcid: 4318343
Cong, S., Rizkalla, M., Salama, P., West, J., Risacher, S., Saykin, A., & Shen, L. (2015). Surface-Based Morphometric Analysis of Hippocampal Subfields in Mild Cognitive Impairment and Alzheimer's Disease. The ... Midwest Symposium on Circuits and Systems conference proceedings : MWSCAS. Midwest Symposium on Circuits and Systems, 2015. https://doi.org/10.1109/MWSCAS.2015.7282173
Contador, J., Pérez-Millan, A., Guillén, N., Sarto, J., Tort-Merino, A., Balasa, M., Falgàs, N., Castellví, M., Borrego-Écija, S., Juncà-Parella, J., Bosch, B., Fernández-Villullas, G., Ramos-Campoy, O., Antonell, A., Bargalló, N., Sanchez-Valle, R., Sala-Llonch, R., & Lladó, A. (2022). Sex differences in early-onset Alzheimer’s disease. European Journal of Neurology, 29(12), 3623–3632. https://doi.org/10.1111/ene.15531
doi: 10.1111/ene.15531
pubmed: 36005384
Dainauskas, J. J., Vitale, P., Moreno, S., Marie, H., Migliore, M., & Saudargiene, A. (2023). Altered synaptic plasticity at hippocampal CA1-CA3 synapses in Alzheimer’s disease: integration of amyloid precursor protein intracellular domain and amyloid beta effects into computational models. Frontiers in Computational Neuroscience,17, 1305169. https://doi.org/10.3389/fncom.2023.1305169
doi: 10.3389/fncom.2023.1305169
pubmed: 38130706
pmcid: 10733499
de Flores, R., Demeilliez-Servouin, S., Kuhn, E., Chauveau, L., Landeau, B., Delcroix, N., Gonneaud, J., Vivien, D., Chételat, G., Medit-Ageing research group. (2023). Respective influence of beta-amyloid and APOE ε4 genotype on medial temporal lobe subregions in cognitively unimpaired older adults. Neurobiology of Disease,181, 106127. https://doi.org/10.1016/j.nbd.2023.106127
doi: 10.1016/j.nbd.2023.106127
pubmed: 37061167
de Vos, R., Larivière, S., Caldairou, B., Hong, S. J., Margulies, D. S., Jefferies, E., Bernasconi, A., Smallwood, J., Bernasconi, N., & Bernhardt, B. C. (2018). Anatomical and microstructural determinants of hippocampal subfield functional connectome embedding. Proceedings of the National Academy of Sciences of the United States of America,115(40), 10154–10159. https://doi.org/10.1073/pnas.1803667115
doi: 10.1073/pnas.1803667115
Ding, S. L. (2013). Comparative anatomy of the prosubiculum, subiculum, presubiculum, postsubiculum, and parasubiculum in human, monkey, and rodent. The Journal of Comparative Neurology,521(18), 4145–4162. https://doi.org/10.1002/cne.23416
doi: 10.1002/cne.23416
pubmed: 23839777
Fixemer, S., Ameli, C., Hammer, G., Salamanca, L., Huarte, U., Schwartz, O., Gérardy, C., Mechawar, J. J., Skupin, N., Mittelbronn, A., & Bouvier, D. S. (2022). Microglia phenotypes are associated with subregional patterns of concomitant tau, amyloid-β and α-synuclein pathologies in the hippocampus of patients with Alzheimer’s disease and dementia with Lewy bodies. Acta Neuropathologica Communications, 10(1), 36. https://doi.org/10.1186/s40478-022-01342
doi: 10.1186/s40478-022-01342
pubmed: 35296366
pmcid: 8925098
Fouquet, M., Desgranges, B., La Joie, R., Rivière, D., Mangin, J. F., Landeau, B., Mézenge, F., Pélerin, A., de La Sayette, V., Viader, F., Baron, J. C., Eustache, F., & Chételat, G. (2012). Role of hippocampal CA1 atrophy in memory encoding deficits in amnestic mild cognitive impairment. NeuroImage, 59(4), 3309–3315. https://doi.org/10.1016/j.neuroimage.2011.11.036
doi: 10.1016/j.neuroimage.2011.11.036
pubmed: 22119654
Goto, M., Abe, O., Hagiwara, A., Fujita, S., Kamagata, K., Hori, M., Aoki, S., Osada, T., Konishi, S., Masutani, Y., Sakamoto, H., Sakano, Y., Kyogoku, S., & Daida, H. (2022). Advantages of using both voxel- and surface-based Morphometry in Cortical Morphology analysis: A review of various applications. Magnetic resonance in medical sciences: MRMS. : An official journal of Japan Society of Magnetic Resonance in Medicine, 21(1), 41–57. https://doi.org/10.2463/mrms.rev.2021-0096
Hsu, P. J., Shou, H., Benzinger, T., Marcus, D., Durbin, T., Morris, J. C., & Sheline, Y. I. (2015). Amyloid burden in cognitively normal elderly is associated with preferential hippocampal subfield volume loss. Journal of Alzheimer’s Disease: JAD,45(1), 27–33. https://doi.org/10.3233/JAD-141743
doi: 10.3233/JAD-141743
pubmed: 25428255
Iaccarino, L., Tammewar, G., Ayakta, N., Baker, S. L., Bejanin, A., Boxer, A. L., Gorno-Tempini, M. L., Janabi, M., Kramer, J. H., Lazaris, A., Lockhart, S. N., Miller, B. L., Miller, Z. A., O’Neil, J. P., Ossenkoppele, R., Rosen, H. J., Schonhaut, D. R., Jagust, W. J., & Rabinovici, G. D. (2017). Local and distant relationships between amyloid, tau and neurodegeneration in Alzheimer’s disease. NeuroImage Clinical, 17, 452–464. https://doi.org/10.1016/j.nicl.2017.09.016
doi: 10.1016/j.nicl.2017.09.016
pubmed: 29159058
pmcid: 5684433
Jack, C. R., Jr, Bennett, D. A., Blennow, K., Carrillo, M. C., Dunn, B., Haeberlein, S. B., Holtzman, D. M., Jagust, W., Jessen, F., Karlawish, J., Liu, E., Molinuevo, J. L., Montine, T., Phelps, C., Rankin, K. P., Rowe, C. C., Scheltens, P., Siemers, E., Snyder, H. M., & Sperling, R., …, & Contributors (2018). NIA-AA Research Framework: Toward a biological definition of Alzheimer's disease. Alzheimer's & dementia: the journal of the Alzheimer's Association, 14(4), 535–562. https://doi.org/10.1016/j.jalz.2018.02.018
Jagust, W. (2016). Is amyloid-β harmful to the brain? Insights from human imaging studies. Brain, 139(Pt, 1), 23–30. https://doi.org/10.1093/brain/awv326
doi: 10.1093/brain/awv326
pubmed: 26614753
Kalus, P., Braak, H., Braak, E., & Bohl, J. (1989). The presubicular region in Alzheimer’s disease: topography of amyloid deposits and neurofibrillary changes. Brain Research, 494(1), 198–203. https://doi.org/10.1016/0006-8993(89)90164-9
doi: 10.1016/0006-8993(89)90164-9
pubmed: 2765920
Kannappan, B., Te Nijenhuis, J., Choi, Y. Y., Lee, J. J., Choi, K. Y., Balzekas, I., Jung, H. Y., Choe, Y., Song, M. K., Chung, J. Y., Ha, J. M., Choi, S. M., Kim, H., Kim, B. C., Jo, H. J., & Lee, K. H. (2022). Can hippocampal subfield measures supply information that could be used to improve the diagnosis of Alzheimer’s disease? PloS one, 17(11), e0275233. https://doi.org/10.1371/journal.pone.0275233
doi: 10.1371/journal.pone.0275233
pubmed: 36327265
pmcid: 9632892
Khan, W., Giampietro, V., Banaschewski, T., Barker, G. J., Bokde, A. L., Büchel, C., Conrod, P., Flor, H., Frouin, V., Garavan, H., Gowland, P., Heinz, A., Ittermann, B., Lemaître, H., Nees, F., Paus, T., Pausova, Z., Rietschel, M., Smolka, M. N., & Ströhle, A. (2017). A Multi-cohort study of ApoE ɛ4 and Amyloid-β effects on the Hippocampus in Alzheimer's disease. Journal of Alzheimer's Disease: JAD, 56(3), 1159–1174. https://doi.org/10.3233/JAD-161097
Knierim, J. J. (2015). The hippocampus. Current Biology: CB,25(23), R1116–R1121. https://doi.org/10.1016/j.cub.2015.10.049
doi: 10.1016/j.cub.2015.10.049
pubmed: 26654366
Li, K., Wang, S., Luo, X., Zeng, Q., Jiaerken, Y., Xu, X., Wang, C., Liu, X., Li, Z., Zhao, S., Zhang, T., Fu, Y., Chen, Y., Liu, Z., Zhou, J., Huang, P., & Zhang, M. (2020). Progressive Memory circuit impairments along with Alzheimer’s Disease Neuropathology spread: Evidence from in vivo Neuroimaging. Cerebral Cortex (New York N Y : 1991), 30(11), 5863–5873. https://doi.org/10.1093/cercor/bhaa162
doi: 10.1093/cercor/bhaa162
pubmed: 32537637
Lindberg, O., Mårtensson, G., Stomrud, E., Palmqvist, S., Wahlund, L. O., Westman, E., & Hansson, O. (2017). Atrophy of the Posterior Subiculum Is Associated with Memory Impairment, Tau- and Aβ Pathology in Non-demented Individuals. Frontiers in Aging Neuroscience,9, 306. https://doi.org/10.3389/fnagi.2017.00306
doi: 10.3389/fnagi.2017.00306
pubmed: 28979205
pmcid: 5611434
Milner, B., Petrides, M., & Smith, M. L. (1985). Frontal lobes and the temporal organization of memory. Human Neurobiology, 4(3), 137–142.
pubmed: 4066424
Moola, S., Munn, Z., Tufanaru, C., Aromataris, E., Sears, K., Sfetcu, R., Currie, M., Lisy, K., Qureshi, R., Mattis, P., & Mu, P. (2020). Chapter 7: Systematic reviews of etiology and risk. In: Aromataris E, Munn Z (Eds.). JBI Manual for Evidence Synthesis. JBI, https://synthesismanual.jbi.global . Accessed 2023
Mueller, S. G., Chao, L. L., Berman, B., & Weiner, M. W. (2011). Evidence for functional specialization of hippocampal subfields detected by MR subfield volumetry on high resolution images at 4 T. Neuroimage,56(3), 851–857. https://doi.org/10.1016/j.neuroimage.2011.03.028
doi: 10.1016/j.neuroimage.2011.03.028
pubmed: 21419225
Mueller, S. G., Yushkevich, P. A., Das, S., Wang, L., Van Leemput, K., Iglesias, J. E., Alpert, K., Mezher, A., Ng, P., Paz, K., & Weiner, M. W. (2017). Systematic comparison of different techniques to measure hippocampal subfield volumes in ADNI2. NeuroImage. Clinical,17, 1006–1018. https://doi.org/10.1016/j.nicl.2017.12.036
doi: 10.1016/j.nicl.2017.12.036
pubmed: 29527502
pmcid: 5842756
Mufson, E. J., Mahady, L., Waters, D., Counts, S. E., Perez, S. E., DeKosky, S. T., Ginsberg, S. D., Ikonomovic, M. D., Scheff, S. W., & Binder, L. I. (2015). Hippocampal plasticity during the progression of Alzheimer’s disease. Neuroscience, 309, 51–67. https://doi.org/10.1016/j.neuroscience.2015.03.006
doi: 10.1016/j.neuroscience.2015.03.006
pubmed: 25772787
Murray, M. E., Lowe, V. J., Graff-Radford, N. R., Liesinger, A. M., Cannon, A., Przybelski, S. A., Rawal, B., Parisi, J. E., Petersen, R. C., Kantarci, K., Ross, O. A., Duara, R., Knopman, D. S., Jack, C. R., Jr., & Dickson, D. W. (2015). Clinicopathologic and 11C-Pittsburgh compound B implications of Thal amyloid phase across the Alzheimer’s disease spectrum. Brain: A Journal of Neurology,138(Pt 5), 1370–1381. https://doi.org/10.1093/brain/awv050
doi: 10.1093/brain/awv050
pubmed: 25805643
Nadel, L., & Moscovitch, M. (1997). Memory consolidation, retrograde amnesia and the hippocampal complex. Current Opinion in Neurobiology,7(2), 217–227. https://doi.org/10.1016/s0959-4388(97)80010-4
doi: 10.1016/s0959-4388(97)80010-4
pubmed: 9142752
Olsen, R. K., Carr, V. A., Daugherty, A. M., La Joie, R., Amaral, R. S. C., Amunts, K., Augustinack, J. C., Bakker, A., Bender, A. R., Berron, D., Boccardi, M., Bocchetta, M., Burggren, A. C., Chakravarty, M. M., Chételat, G., de Flores, R., DeKraker, J., Ding, S. L., Geerlings, M. I., Huang, Y., ..., & Hippocampal Subfields Group. (2019). Progress update from the hippocampal subfields group. Alzheimer's & dementia (Amsterdam, Netherlands), 11, 439–449. https://doi.org/10.1016/j.dadm.2019.04.001
Page, M. J., McKenzie, J. E., Bossuyt, P. M., Boutron, I., Hoffmann, T. C., Mulrow, C. D., Shamseer, L., Tetzlaff, J. M., Akl, E. A., Brennan, S. E., Chou, R., Glanville, J., Grimshaw, J. M., Hróbjartsson, A., Lalu, M. M., Li, T., Loder, E. W., Mayo-Wilson, E., McDonald, S., McGuinness, L. A., …, & Moher, D. (2021). The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ (Clinical research ed.), 372, n71. https://doi.org/10.1136/bmj.n71
Parker, T. D., Cash, D. M., Lane, C. A. S., Lu, K., Malone, I. B., Nicholas, J. M., James, S. N., Keshavan, A., Murray-Smith, H., Wong, A., Buchanan, S. M., Keuss, S. E., Sudre, C. H., Modat, M., Thomas, D. L., Crutch, S. J., Richards, M., Fox, N. C., & Schott, J. M. (2019). Hippocampal subfield volumes and pre-clinical Alzheimer’s disease in 408 cognitively normal adults born in 1946. PloS one,14(10), e0224030. https://doi.org/10.1371/journal.pone.0224030
doi: 10.1371/journal.pone.0224030
pubmed: 31622410
pmcid: 6797197
Pelkmans, W., Ossenkoppele, R., Dicks, E., Strandberg, O., Barkhof, F., Tijms, B. M., Pereira, J. B., & Hansson, O. (2021). Tau-related grey matter network breakdown across the Alzheimer’s disease continuum. Alzheimer’s Research & Therapy,13(1), 138. https://doi.org/10.1186/s13195-021-00876-7
doi: 10.1186/s13195-021-00876-7
Pluta, J., Yushkevich, P., Das, S., & Wolk, D. (2012). In vivo analysis of hippocampal subfield atrophy in mild cognitive impairment via semi-automatic segmentation of T2-weighted MRI. Journal of Alzheimer’s Disease: JAD,31(1), 85–99. https://doi.org/10.3233/JAD-2012-111931
doi: 10.3233/JAD-2012-111931
pubmed: 22504319
Poppenk, J., Evensmoen, H. R., Moscovitch, M., & Nadel, L. (2013). Long-axis specialization of the human hippocampus. Trends in Cognitive Sciences,17(5), 230–240. https://doi.org/10.1016/j.tics.2013.03.005
doi: 10.1016/j.tics.2013.03.005
pubmed: 23597720
Rahayel, S., Bocti, C., Sévigny Dupont, P., Joannette, M., Lavallée, M. M., Nikelski, J., Chertkow, H., & Joubert, S. (2019). Subcortical amyloid load is associated with shape and volume in cognitively normal individuals. Human Brain Mapping,40(13), 3951–3965. https://doi.org/10.1002/hbm.24680
doi: 10.1002/hbm.24680
pubmed: 31148327
pmcid: 6865639
Rao, Y. L., Ganaraja, B., Murlimanju, B. V., Joy, T., Krishnamurthy, A., & Agrawal, A. (2022). Hippocampus and its involvement in Alzheimer’s disease: a review. 3 Biotech,12(2), 55. https://doi.org/10.1007/s13205-022-03123-4
doi: 10.1007/s13205-022-03123-4
pubmed: 35116217
pmcid: 8807768
Reitz, C., Brayne, C., & Mayeux, R. (2011). Epidemiology of Alzheimer disease. Nature Reviews Neurology,7(3), 137–152. https://doi.org/10.1038/nrneurol.2011.2
doi: 10.1038/nrneurol.2011.2
pubmed: 21304480
pmcid: 3339565
Rolls, E. T. (2013). The mechanisms for pattern completion and pattern separation in the hippocampus. Frontiers in systems neuroscience, 7, 74. https://doi.org/10.3389/fnsys.2013.00074
doi: 10.3389/fnsys.2013.00074
pubmed: 24198767
pmcid: 3812781
Sahay, A., Scobie, K. N., Hill, A. S., O'Carroll, C. M., Kheirbek, M. A., Burghardt, N. S., Fenton, A. A., Dranovsky, A., & Hen, R. (2011). Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature, 472(7344), 466–470. https://doi.org/10.1038/nature09817
doi: 10.1038/nature09817
pubmed: 21460835
pmcid: 3084370
Serrano-Pozo, A., Frosch, M. P., Masliah, E., & Hyman, B. T. (2011). Neuropathological alterations in Alzheimer disease. Cold Spring Harbor perspectives in medicine, 1(1), a006189. https://doi.org/10.1101/cshperspect.a006189
doi: 10.1101/cshperspect.a006189
pubmed: 22229116
pmcid: 3234452
Sone, D., Imabayashi, E., Maikusa, N., Okamura, N., Furumoto, S., Kudo, Y., Ogawa, M., Takano, H., Yokoi, Y., Sakata, M., Tsukamoto, T., Kato, K., & Matsuda, H. (2017). Regional tau deposition and subregion atrophy of medial temporal structures in early Alzheimer’s disease: A combined positron emission tomography/magnetic resonance imaging study. Alzheimer’s & Dementia (Amsterdam Netherlands),9, 35–40. https://doi.org/10.1016/j.dadm.2017.07.001
doi: 10.1016/j.dadm.2017.07.001
Stern, Y., Albert, M., Barnes, C. A., Cabeza, R., Pascual-Leone, A., & Rapp, P. R. (2023). A framework for concepts of reserve and resilience in aging. Neurobiology of Aging,124, 100–103. https://doi.org/10.1016/j.neurobiolaging.2022.10.015
doi: 10.1016/j.neurobiolaging.2022.10.015
pubmed: 36653245
Strange, B. A., Witter, M. P., Lein, E. S., & Moser, E. I. (2014). Functional organization of the hippocampal longitudinal axis. Nature Reviews Neuroscience,15(10), 655–669. https://doi.org/10.1038/nrn3785
doi: 10.1038/nrn3785
pubmed: 25234264
Suthana, N. A., Donix, M., Wozny, D. R., Bazih, A., Jones, M., Heidemann, R. M., Trampel, R., Ekstrom, A. D., Scharf, M., Knowlton, B., Turner, R., & Bookheimer, S. Y. (2015). High-resolution 7T fMRI of Human Hippocampal Subfields during Associative Learning. Journal of Cognitive Neuroscience,27(6), 1194–1206. https://doi.org/10.1162/jocn_a_00772
doi: 10.1162/jocn_a_00772
pubmed: 25514656
Thal, D. R., Rüb, U., Orantes, M., & Braak, H. (2002). Phases of A beta-deposition in the human brain and its relevance for the development of AD. Neurology,58(12), 1791–1800. https://doi.org/10.1212/wnl.58.12.1791
doi: 10.1212/wnl.58.12.1791
pubmed: 12084879
Voevodskaya, O., Simmons, A., Nordenskjöld, R., Kullberg, J., Ahlström, H., Lind, L., Wahlund, L. O., Larsson, E. M., Westman, E., Alzheimer’s Disease Neuroimaging Initiative. (2014). The effects of intracranial volume adjustment approaches on multiple regional MRI volumes in healthy aging and Alzheimer’s disease. Frontiers in Aging Neuroscience,6, 264. https://doi.org/10.3389/fnagi.2014.00264
doi: 10.3389/fnagi.2014.00264
pubmed: 25339897
pmcid: 4188138
Wisniewski, H. M., Sadowski, M., Jakubowska-Sadowska, K., Tarnawski, M., & Wegiel, J. (1998). Diffuse, lake-like amyloid-beta deposits in the parvopyramidal layer of the presubiculum in Alzheimer disease. Journal of Neuropathology and Experimental Neurology,57(7), 674–683. https://doi.org/10.1097/00005072-199807000-00004
doi: 10.1097/00005072-199807000-00004
pubmed: 9690671
Wisse, L. E. M., Daugherty, A. M., Olsen, R. K., Berron, D., Carr, V. A., Stark, C. E. L., Amaral, R. S. C., Amunts, K., Augustinack, J. C., Bender, A. R., Bernstein, J. D., Boccardi, M., Bocchetta, M., Burggren, A., Chakravarty, M. M., Chupin, M., Ekstrom, A., de Flores, R., Insausti, R., Kanel, P. (2017). A harmonized segmentation protocol for hippocampal and parahippocampal subregions: Why do we need one and what are the key goals? Hippocampus, 27(1), 3–11. https://doi.org/10.1002/hipo.22671
Wisse, L. E. M., Chételat, G., Daugherty, A. M., de Flores, R., la Joie, R., Mueller, S. G., Stark, C. E. L., Wang, L., Yushkevich, P. A., Berron, D., Raz, N., Bakker, A., Olsen, R. K., & Carr, V. A. (2021). Hippocampal subfield volumetry from structural isotropic 1 mm3 MRI scans: A note of caution. Human Brain Mapping,42(2), 539–550. https://doi.org/10.1002/hbm.25234
doi: 10.1002/hbm.25234
pubmed: 33058385
Wolk, D. A., Das, S. R., Mueller, S. G., Weiner, M. W., Yushkevich, P. A., Alzheimer’s Disease Neuroimaging Initiative. (2017). Medial temporal lobe subregional morphometry using high resolution MRI in Alzheimer’s disease. Neurobiology of aging,49, 204–213. https://doi.org/10.1016/j.neurobiolaging.2016.09.011
doi: 10.1016/j.neurobiolaging.2016.09.011
pubmed: 27836336
Yildirim, Z., Delen, F., Berron, D., Baumeister, H., Ziegler, G., Schütze, H., Glanz, W., Dobisch, L., Peters, O., Freiesleben, S. D., Schneider, L. S., Priller, J., Spruth, E. J., Schneider, A., Fliessbach, K., Wiltfang, J., Schott, B. H., Meiberth, D., Buerger, K., Janowitz, D., …, & Duzel, E. (2023). Brain reserve contributes to distinguishing preclinical Alzheimer's stages 1 and 2. Alzheimer's Research & Therapy, 15(1), 43. https://doi.org/10.1186/s13195-023-01187-9
Yushkevich, P. A., Amaral, R. S., Augustinack, J. C., Bender, A. R., Bernstein, J. D., Boccardi, M., Bocchetta, M., Burggren, A. C., Carr, V. A., Chakravarty, M. M., Chételat, G., Daugherty, A. M., Davachi, L., Ding, S. L., Ekstrom, A., Geerlings, M. I., Hassan, A., Huang, Y., Iglesias, J. E., La Joie, R., …, & Hippocampal Subfields Group (HSG) (2015). Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI: towards a harmonized segmentation protocol. NeuroImage, 111, 526–541. https://doi.org/10.1016/j.neuroimage.2015.01.004
Zammit, A. R., Ezzati, A., Zimmerman, M. E., Lipton, R. B., Lipton, M. L., & Katz, M. J. (2017). Roles of hippocampal subfields in verbal and visual episodic memory. Behavioural Brain Research,317, 157–162. https://doi.org/10.1016/j.bbr.2016.09.038
doi: 10.1016/j.bbr.2016.09.038
pubmed: 27646772
Zeidman, P., & Maguire, E. A. (2016). Anterior hippocampus: The anatomy of perception, imagination and episodic memory. Nature Reviews Neuroscience,17(3), 173–182. https://doi.org/10.1038/nrn.2015.24
doi: 10.1038/nrn.2015.24
pubmed: 26865022
pmcid: 5358751
Zhang, J., Xie, L., Cheng, C., Liu, Y., Zhang, X., Wang, H., Hu, J., Yu, H., & Xu, J. (2023). Hippocampal subfield volumes in mild cognitive impairment and alzheimer’s disease: a systematic review and meta-analysis. Brain Imaging and Behavior. https://doi.org/10.1007/s11682-023-00804-3
doi: 10.1007/s11682-023-00804-3
pubmed: 38155336
pmcid: 11156756
Zhao, W., Wang, X., Yin, C., He, M., Li, S., & Han, Y. (2019). Trajectories of the Hippocampal subfields Atrophy in the Alzheimer’s Disease: A structural imaging study. Frontiers in Neuroinformatics, 13, 13. https://doi.org/10.3389/fninf.2019.00013
doi: 10.3389/fninf.2019.00013
pubmed: 30983985
pmcid: 6450438