Differential atrophy along the longitudinal hippocampal axis in Alzheimer's disease for the Alzheimer's Disease Neuroimaging Initiative.

ADNI Alzheimer's disease hippocampus longitudinal axis mild cognitive impairment neuroimaging

Journal

The European journal of neuroscience
ISSN: 1460-9568
Titre abrégé: Eur J Neurosci
Pays: France
ID NLM: 8918110

Informations de publication

Date de publication:
23 Apr 2024
Historique:
received: 04 02 2023
accepted: 03 04 2024
medline: 24 4 2024
pubmed: 24 4 2024
entrez: 24 4 2024
Statut: aheadofprint

Résumé

Alzheimer's disease (AD) is a progressive neurodegenerative disorder that primarily affects the hippocampus. Since hippocampal studies have highlighted a differential subregional regulation along its longitudinal axis, a more detailed analysis addressing subregional changes along the longitudinal hippocampal axis has the potential to provide new relevant biomarkers. This study included structural brain MRI data of 583 participants from the Alzheimer's Disease Neuroimaging Initiative (ADNI). Cognitively normal (CN) subjects, mild cognitively impaired (MCI) subjects and AD patients were conveniently selected considering the age and sex match between clinical groups. Structural MRI acquisitions were pre-processed and analysed with a new longitudinal axis segmentation method, dividing the hippocampus in three subdivisions (anterior, intermediate, and posterior). When normalizing the volume of hippocampal sub-divisions to total hippocampus, the posterior hippocampus negatively correlates with age only in CN subjects (r = -.31). The longitudinal ratio of hippocampal atrophy (anterior sub-division divided by the posterior one) shows a significant increase with age only in CN (r = .25). Overall, in AD, the posterior hippocampus is predominantly atrophied early on. Consequently, the anterior/posterior hippocampal ratio is an AD differentiating metric at early disease stages with potential for diagnostic and prognostic applications.

Identifiants

pubmed: 38654447
doi: 10.1111/ejn.16361
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIH HHS
ID : U01 AG024904
Pays : United States
Organisme : NIA NIH HHS
Pays : United States
Organisme : NIBIB NIH HHS
Pays : United States

Informations de copyright

© 2024 The Authors. European Journal of Neuroscience published by Federation of European Neuroscience Societies and John Wiley & Sons Ltd.

Références

Auning, E., Selnes, P., Grambaite, R., Šaltyte Benth, J., Haram, A., Løvli Stav, A., Bjørnerud, A., Hessen, E., Hol, P. K., Muftuler Løndalen, A., Fladby, T., & Aarsland, D. (2015). Neurobiological correlates of depressive symptoms in people with subjective and mild cognitive impairment. Acta Psychiatrica Scandinavica, 131, 139–147. https://doi.org/10.1111/acps.12352
Ayhan, F., Kulkarni, A., Berto, S., Sivaprakasam, K., Douglas, C., Lega, B. C., & Konopka, G. (2021). Resolving cellular and molecular diversity along the hippocampal anterior‐to‐posterior axis in humans. Neuron, 109, 2091–2105.e6. https://doi.org/10.1016/j.neuron.2021.05.003
Cembrowski, M. S., Bachman, J. L., Wang, L., Sugino, K., Shields, B. C., & Spruston, N. (2016). Spatial gene‐expression gradients underlie prominent heterogeneity of CA1 pyramidal neurons. Neuron, 89, 351–368. https://doi.org/10.1016/j.neuron.2015.12.013
Chan, D., Fox, N. C., Scahill, R. I., Crum, W. R., Whitwell, J. L., Leschziner, G., Rossor, A. M., Stevens, J. M., Cipolotti, L., & Rossor, M. N. (2001). Patterns of temporal lobe atrophy in semantic dementia and Alzheimer's disease. Annals of Neurology, 49, 433–442. https://doi.org/10.1002/ana.92
Chapleau, M., Aldebert, J., Montembeault, M., & Brambati, S. M. (2016). Atrophy in Alzheimer's disease and semantic dementia: An ALE meta‐analysis of voxel‐based morphometry studies. Journal of Alzheimer's Disease, 54, 941–955. https://doi.org/10.3233/JAD-160382
Damoiseaux, J. S., Viviano, R. P., Yuan, P., & Raz, N. (2016). Differential effect of age on posterior and anterior hippocampal functional connectivity. NeuroImage, 133, 468–476. https://doi.org/10.1016/j.neuroimage.2016.03.047
Daugherty, A. M., Yu, Q., Flinn, R., & Ofen, N. (2015). A reliable and valid method for manual demarcation of hippocampal head, body, and tail. International Journal of Developmental Neuroscience, 41, 115–122. https://doi.org/10.1016/j.ijdevneu.2015.02.001
Dautricourt, S., de Flores, R., Landeau, B., Poisnel, G., Vanhoutte, M., Delcroix, N., Eustache, F., Vivien, D., de la Sayette, V., & Chételat, G. (2021). Longitudinal changes in hippocampal network connectivity in Alzheimer's disease. Annals of Neurology, 90, 391–406. https://doi.org/10.1002/ana.26168
de Flores, R., Wisse, L. E. M., Das, S. R., Xie, L., McMillan, C. T., Trojanowski, J. Q., Robinson, J. L., Grossman, M., Lee, E., Irwin, D. J., Yushkevich, P. A., & Wolk, D. A. (2020). Contribution of mixed pathology to medial temporal lobe atrophy in Alzheimer's disease. Alzheimer's & Dementia, 16, 1–10. https://doi.org/10.1002/alz.12079
Den Heijer, T., Tiemeier, H., Luijendijk, H. J., van der Lijn, F., Koudstaal, P. J., Hofman, A., & Breteler, M. M. B. (2011). A study of the bidirectional association between hippocampal volume on magnetic resonance imaging and depression in the elderly. Biological Psychiatry, 70, 191–197. https://doi.org/10.1016/j.biopsych.2011.04.014
Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., Buckner, R. L., Dale, A. M., Maguire, R. P., Hyman, B. T., Albert, M. S., & Killiany, R. J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage, 31, 968–980. https://doi.org/10.1016/j.neuroimage.2006.01.021
Destrieux, C., Fischl, B., Dale, A., & Halgren, E. (2010). Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. NeuroImage, 53, 1–15. https://doi.org/10.1016/j.neuroimage.2010.06.010
Donovan, N. J., Hsu, D. C., Dagley, A. S., Schultz, A. P., Amariglio, R. E., Mormino, E. C., Okereke, O. I., Rentz, D. M., Johnson, K. A., Sperling, R. A., & Marshall, G. A. (2015). Depressive symptoms and biomarkers of Alzheimer's disease in cognitively normal older adults. Journal of Alzheimer's Disease, 46, 63–73. https://doi.org/10.3233/JAD-142940
Enache, D., Cavallin, L., Lindberg, O., Farahmand, B., Kramberger, M. G., Westman, E., Jelic, V., Eriksdotter, M., Ballard, C., Winblad, B., Wahlund, L. O., & Aarsland, D. (2015). Medial temporal lobe atrophy and depressive symptoms in elderly patients with and without Alzheimer disease. Journal of Geriatric Psychiatry and Neurology, 28, 40–48. https://doi.org/10.1177/0891988714541873
Fischl, B., Salat, D. H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C., Van Der Kouwe, A., Killiany, R., Kennedy, D., Klaveness, S., Montillo, A., Makris, N., Rosen, B., & Dale, A. M. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33, 341–355. https://doi.org/10.1016/S0896-6273(02)00569-X
Genon, S., Bernhardt, B. C., La Joie, R., Amunts, K., & Eickhoff, S. B. (2021). The many dimensions of human hippocampal organization and (dys)function. Trends in Neurosciences, 44, 977–989. https://doi.org/10.1016/j.tins.2021.10.003
Gordon, B. A., Blazey, T., Benzinger, T. L. S., & Head, D. (2013). Effects of aging and Alzheimer's disease along the longitudinal axis of the hippocampus. Journal of Alzheimer's Disease, 37, 41–50. https://doi.org/10.3233/JAD-130011
Greene, S. J., & Killiany, R. J. (2012). Hippocampal subregions are differentially affected in the progression to Alzheimer's disease. Anatomical Record, 295, 132–140. https://doi.org/10.1002/ar.21493
Jack, C. R., Bennet, D. A., Blennow, K., Carrillo, M. C., Feldman, H. H., Frisoni, G. B., Hampel, H., Jagust, W. J., Johnson, K. A., Knopman, D. S., Petersen, R. C., Scheltens, P., Sperling, R. A., & Dubois, B. (2016). A/T/N: An unbiased descriptive classification scheme for Alzheimer disease biomarkers. Neurology, 87, 539–547. https://doi.org/10.1212/WNL.0000000000002923
Joko, T., Washizuka, S., Sasayama, D., Inuzuka, S., Ogihara, T., Yasaki, T., Hagiwara, T., Sugiyama, N., Takahashi, T., Kaneko, T., Hanihara, T., & Amano, N. (2016). Patterns of hippocampal atrophy differ among Alzheimer's disease, amnestic mild cognitive impairment, and late‐life depression. Psychogeriatrics, 16, 355–361. https://doi.org/10.1111/psyg.12176
Jovicich, J., Czanner, S., Han, X., Salat, D., van der Kouwe, A., Quinn, B., Pacheco, J., Albert, M., Killiany, R., Blacker, D., Maguire, P., Rosas, D., Makris, N., Gollub, R., Dale, A., Dickerson, B. C., & Fischl, B. (2009). MRI‐derived measurements of human subcortical, ventricular and intracranial brain volumes: Reliability effects of scan sessions, acquisition sequences, data analyses, scanner upgrade, scanner vendors and field strengths. NeuroImage, 46, 177–192. https://doi.org/10.1016/j.neuroimage.2009.02.010
Knopman, D. S., Amieva, H., Petersen, R. C., Chételat, G., Holtzman, D. M., Hyman, B. T., Nixon, R. A., & Jones, D. T. (2021). Alzheimer disease. Nature Reviews. Disease Primers, 7, 33. https://doi.org/10.1038/s41572-021-00269-y
Knopman, D. S., Dekosky, S. T., Cummings, J. L., Chui, H., Relkin, N., Small, G. W., Miller, B., & Stevens, J. C. (2001). Practice parameter: Diagnosis of dementia (an evidence‐based review). Neurology, 56, 1143–1153. https://doi.org/10.1212/WNL.56.9.1143
La Joie, R., Landeau, B., Perrotin, A., Bejanin, A., Egret, S., Pélerin, A., Mézenge, F., Belliard, S., de La Sayette, V., Eustache, F., Desgranges, B., & Chételat, G. (2014). Intrinsic connectivity identifies the hippocampus as a main crossroad between Alzheimer's and semantic dementia‐targeted networks. Neuron, 81, 1417–1428. https://doi.org/10.1016/j.neuron.2014.01.026
La Joie, R., Perrotin, A., de La Sayette, V., Egret, S., Doeuvre, L., Belliard, S., Eustache, F., Desgranges, B., & Chételat, G. (2013). Hippocampal subfield volumetry in mild cognitive impairment, Alzheimer's disease and semantic dementia. NeuroImage: Clinical, 3, 155–162. https://doi.org/10.1016/j.nicl.2013.08.007
Langnes, E., Sneve, M. H., Sederevicius, D., Amlien, I. K., Walhovd, K. B., & Fjell, A. M. (2020). Anterior and posterior hippocampus macro‐ and microstructure across the lifespan in relation to memory — A longitudinal study. Hippocampus, 30, 1–15. https://doi.org/10.1002/hipo.23189
Lerma‐Usabiaga, G., Iglesias, J. E., Insausti, R., Greve, D. N., & Paz‐Alonso, P. M. (2016). Automated segmentation of the human hippocampus along its longitudinal axis. Human Brain Mapping, 37, 3353–3367. https://doi.org/10.1002/hbm.23245
Lladó, A., Tort‐Merino, A., Sánchez‐Valle, R., Falgàs, N., Balasa, M., Bosch, B., Castellví, M., Olives, J., Antonell, A., & Hornberger, M. (2018). The hippocampal longitudinal axis‐relevance for underlying tau and TDP‐43 pathology. Neurobiology of Aging, 70, 1–9. https://doi.org/10.1016/j.neurobiolaging.2018.05.035
Lowe, A. J., Paquola, C., Vos de Wael, R., Girn, M., Lariviere, S., Tavakol, S., Caldairou, B., Royer, J., Schrader, D. V., Bernasconi, A., Bernasconi, N., Spreng, R. N., & Bernhardt, B. C. (2019). Targeting age‐related differences in brain and cognition with multimodal imaging and connectome topography profiling. Human Brain Mapping, 40, 5213–5230. https://doi.org/10.1002/hbm.24767
Malykhin, N. V., Huang, Y., Hrybouski, S., & Olsen, F. (2017). Differential vulnerability of hippocampal subfields and anteroposterior hippocampal subregions in healthy cognitive aging. Neurobiology of Aging, 59, 121–134. https://doi.org/10.1016/j.neurobiolaging.2017.08.001
McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E. M. (1984). Clinical diagnosis of Alzheimer's disease: Report of the NINCDS‐ADRDA work group under the auspices of Department of Health and Human Services Task Force on Alzheimer's disease. Neurology, 34, 939–944. https://doi.org/10.1212/WNL.34.7.939
Morra, J. H., Tu, Z., Apostolova, L. G., Green, A. E., Avedissian, C., Madsen, S. K., Parikshak, N., Hua, X., Toga, A. W., Jack, C. R., Schuff, N., Weiner, M. W., & Thompson, P. M. (2009). Automated 3D mapping of hippocampal atrophy and its clinical correlates in 400 subjects with Alzheimer's disease, mild cognitive impairment, and elderly controls. Human Brain Mapping, 30, 2766–2788. https://doi.org/10.1002/hbm.20708
Moser, M. B., & Moser, E. I. (1998). Distributed encoding and retrieval of spatial memory in the hippocampus. Journal of Neuroscience, 18, 7535–7542. https://doi.org/10.1523/JNEUROSCI.18‐18‐07535.1998
Nestor, P. J., Fryer, T. D., & Hodges, J. R. (2006). Declarative memory impairments in Alzheimer's disease and semantic dementia. NeuroImage, 30, 1010–1020. https://doi.org/10.1016/j.neuroimage.2005.10.008
Nestor, P. J., Scheltens, P., & Hodges, J. R. (2004). Advances in the early detection of Alzheimer's disease. Nature Medicine, 10, S34–S41. https://doi.org/10.1038/nrn1433
Pini, L., Pievani, M., Bocchetta, M., Altomare, D., Bosco, P., Cavedo, E., Galluzzi, S., Marizzoni, M., & Frisoni, G. B. (2016). Brain atrophy in Alzheimer's disease and aging. Ageing Research Reviews, 30, 25–48. https://doi.org/10.1016/j.arr.2016.01.002
Plachti, A., Eickhoff, S. B., Hoffstaedter, F., Patil, K. R., Laird, A. R., Fox, P. T., Amunts, K., & Genon, S. (2019). Multimodal parcellations and extensive behavioral profiling tackling the hippocampus gradient. Cerebral Cortex, 29, 4595–4612. https://doi.org/10.1093/cercor/bhy336
Plachti, A., Kharabian, S., Eickhoff, S. B., Balajoo, S. M., Hoffstaedter, F., Varikuti, D. P., Jockwitz, C., Caspers, S., Amunts, K., & Genon, S. (2020). Hippocampus co‐atrophy pattern in dementia deviates from covariance patterns across the lifespan. Brain, 143, 2788–2802. https://doi.org/10.1093/brain/awaa222
Poppenk, J., Evensmoen, H. R., Moscovitch, M., & Nadel, L. (2013). Long‐axis specialization of the human hippocampus. Trends in Cognitive Sciences, 17, 230–240. https://doi.org/10.1016/j.tics.2013.03.005
Small, S. A., Nava, A. S., Perera, G. M., DeLaPaz, R., Mayeux, R., & Stern, Y. (2001). Circuit mechanisms underlying memory encoding and retrieval in the long axis of the hippocampal formation. Nature Neuroscience, 4, 442–449. https://doi.org/10.1038/86115
Strange, B. A., Witter, M. P., Lein, E. S., & Moser, E. I. (2014). Functional organization of the hippocampal longitudinal axis. Nature Reviews. Neuroscience, 15, 655–669. https://doi.org/10.1038/nrn3785
Touron, E., Moulinet, I., Kuhn, E., Sherif, S., Ourry, V., Landeau, B., Mézenge, F., Vivien, D., Klimecki, O. M., Poisnel, G., Marchant, N. L., Chételat, G., Arenaza‐Urquijo, E. M., Allais, F., André, C., Asselineau, J., Baez Lugo, S., Batchelor, M., Beaugonin, A., … Wirth, M. (2022). Depressive symptoms in cognitively unimpaired older adults are associated with lower structural and functional integrity in a frontolimbic network. Molecular Psychiatry, 27, 5086–5095. https://doi.org/10.1038/s41380-022-01772-8
Van Leemput, K. (2009). Encoding probabilistic brain atlases using Bayesian inference. IEEE Transactions on Medical Imaging, 28, 822–837. https://doi.org/10.1109/TMI.2008.2010434
Wolf, D., Fischer, F. U., de Flores, R., Chételat, G., & Fellgiebel, A. (2015). Differential associations of age with volume and microstructure of hippocampal subfields in healthy older adults. Human Brain Mapping, 36, 3819–3831. https://doi.org/10.1002/hbm.22880

Auteurs

Rafaela Morais-Ribeiro (R)

Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, Campus Gualtar, Braga, Portugal.
ICVS/3B's - PT Government Associate Laboratory, Braga/Guimarães, Portugal.

Francisco C Almeida (FC)

Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, Campus Gualtar, Braga, Portugal.
ICVS/3B's - PT Government Associate Laboratory, Braga/Guimarães, Portugal.
Department of Neuroradiology, Centro Hospitalar Universitário do Porto, Porto, Portugal.

Ana Coelho (A)

Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, Campus Gualtar, Braga, Portugal.
ICVS/3B's - PT Government Associate Laboratory, Braga/Guimarães, Portugal.

Tiago Gil Oliveira (TG)

Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, Campus Gualtar, Braga, Portugal.
ICVS/3B's - PT Government Associate Laboratory, Braga/Guimarães, Portugal.
Division of Neuroradiology, Hospital de Braga, Braga, Portugal.

Classifications MeSH