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Characterizing the human hippocampus in aging and Alzheimer's disease using a computational atlas derived from ex vivo MRI and histology

Adler, Daniel H ; Wisse, Laura E M LU orcid ; Ittyerah, Ranjit ; Pluta, John B ; Ding, Song-Lin ; Xie, Long ; Wang, Jiancong ; Kadivar, Salmon ; Robinson, John L and Schuck, Theresa , et al. (2018) In Proceedings of the National Academy of Sciences of the United States of America 115(16). p.4252-4257
Abstract

Although the hippocampus is one of the most studied structures in the human brain, limited quantitative data exist on its 3D organization, anatomical variability, and effects of disease on its subregions. Histological studies provide restricted reference information due to their 2D nature. In this paper, high-resolution (∼200 × 200 × 200 μm3) ex vivo MRI scans of 31 human hippocampal specimens are combined using a groupwise diffeomorphic registration approach into a 3D probabilistic atlas that captures average anatomy and anatomic variability of hippocampal subfields. Serial histological imaging in 9 of the 31 specimens was used to label hippocampal subfields in the atlas based on cytoarchitecture. Specimens were obtained from autopsies... (More)

Although the hippocampus is one of the most studied structures in the human brain, limited quantitative data exist on its 3D organization, anatomical variability, and effects of disease on its subregions. Histological studies provide restricted reference information due to their 2D nature. In this paper, high-resolution (∼200 × 200 × 200 μm3) ex vivo MRI scans of 31 human hippocampal specimens are combined using a groupwise diffeomorphic registration approach into a 3D probabilistic atlas that captures average anatomy and anatomic variability of hippocampal subfields. Serial histological imaging in 9 of the 31 specimens was used to label hippocampal subfields in the atlas based on cytoarchitecture. Specimens were obtained from autopsies in patients with a clinical diagnosis of Alzheimer's disease (AD; 9 subjects, 13 hemispheres), of other dementia (nine subjects, nine hemispheres), and in subjects without dementia (seven subjects, nine hemispheres), and morphometric analysis was performed in atlas space to measure effects of age and AD on hippocampal subfields. Disproportional involvement of the cornu ammonis (CA) 1 subfield and stratum radiatum lacunosum moleculare was found in AD, with lesser involvement of the dentate gyrus and CA2/3 subfields. An association with age was found for the dentate gyrus and, to a lesser extent, for CA1. Three-dimensional patterns of variability and disease and aging effects discovered via the ex vivo hippocampus atlas provide information highly relevant to the active field of in vivo hippocampal subfield imaging.

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publishing date
type
Contribution to journal
publication status
published
subject
keywords
Aged, Aging/pathology, Alzheimer Disease/pathology, Atlases as Topic, Atrophy, Dentate Gyrus/pathology, Hippocampus/pathology, Humans, Imaging, Three-Dimensional, Magnetic Resonance Imaging, Neuroimaging, Organ Size
in
Proceedings of the National Academy of Sciences of the United States of America
volume
115
issue
16
pages
4252 - 4257
publisher
National Academy of Sciences
external identifiers
  • scopus:85045507852
  • pmid:29592955
ISSN
1091-6490
DOI
10.1073/pnas.1801093115
language
English
LU publication?
no
id
a533424f-7e83-4a24-ad4b-1800a374325b
date added to LUP
2024-02-28 14:48:07
date last changed
2024-04-14 00:20:24
@article{a533424f-7e83-4a24-ad4b-1800a374325b,
  abstract     = {{<p>Although the hippocampus is one of the most studied structures in the human brain, limited quantitative data exist on its 3D organization, anatomical variability, and effects of disease on its subregions. Histological studies provide restricted reference information due to their 2D nature. In this paper, high-resolution (∼200 × 200 × 200 μm3) ex vivo MRI scans of 31 human hippocampal specimens are combined using a groupwise diffeomorphic registration approach into a 3D probabilistic atlas that captures average anatomy and anatomic variability of hippocampal subfields. Serial histological imaging in 9 of the 31 specimens was used to label hippocampal subfields in the atlas based on cytoarchitecture. Specimens were obtained from autopsies in patients with a clinical diagnosis of Alzheimer's disease (AD; 9 subjects, 13 hemispheres), of other dementia (nine subjects, nine hemispheres), and in subjects without dementia (seven subjects, nine hemispheres), and morphometric analysis was performed in atlas space to measure effects of age and AD on hippocampal subfields. Disproportional involvement of the cornu ammonis (CA) 1 subfield and stratum radiatum lacunosum moleculare was found in AD, with lesser involvement of the dentate gyrus and CA2/3 subfields. An association with age was found for the dentate gyrus and, to a lesser extent, for CA1. Three-dimensional patterns of variability and disease and aging effects discovered via the ex vivo hippocampus atlas provide information highly relevant to the active field of in vivo hippocampal subfield imaging.</p>}},
  author       = {{Adler, Daniel H and Wisse, Laura E M and Ittyerah, Ranjit and Pluta, John B and Ding, Song-Lin and Xie, Long and Wang, Jiancong and Kadivar, Salmon and Robinson, John L and Schuck, Theresa and Trojanowski, John Q and Grossman, Murray and Detre, John A and Elliott, Mark A and Toledo, Jon B and Liu, Weixia and Pickup, Stephen and Miller, Michael I and Das, Sandhitsu R and Wolk, David A and Yushkevich, Paul A}},
  issn         = {{1091-6490}},
  keywords     = {{Aged; Aging/pathology; Alzheimer Disease/pathology; Atlases as Topic; Atrophy; Dentate Gyrus/pathology; Hippocampus/pathology; Humans; Imaging, Three-Dimensional; Magnetic Resonance Imaging; Neuroimaging; Organ Size}},
  language     = {{eng}},
  month        = {{04}},
  number       = {{16}},
  pages        = {{4252--4257}},
  publisher    = {{National Academy of Sciences}},
  series       = {{Proceedings of the National Academy of Sciences of the United States of America}},
  title        = {{Characterizing the human hippocampus in aging and Alzheimer's disease using a computational atlas derived from ex vivo MRI and histology}},
  url          = {{http://dx.doi.org/10.1073/pnas.1801093115}},
  doi          = {{10.1073/pnas.1801093115}},
  volume       = {{115}},
  year         = {{2018}},
}