A Diffeomorphic Vector Field Approach to Analyze the Thickness of the Hippocampus from 7 T MRI

Alexis Guyot; Ana B.Graciano Fouquier; Emilie Gerardin; Marie Chupin; Joan A. Glaunes; Linda Marrakchi-Kacem; Johanne Germain; Claire Boutet; Claire Cury; Lucie Hertz-Pannier; Alexandre Vignaud; Stanley Durrleman; Thomas R. Henry; Pierre Francois Van De Moortele; Alain Trouve; Olivier Colliot

doi:10.1109/TBME.2020.2999941

A Diffeomorphic Vector Field Approach to Analyze the Thickness of the Hippocampus from 7 T MRI

Alexis Guyot, Ana B.Graciano Fouquier, Emilie Gerardin, Marie Chupin, Joan A. Glaunes, Linda Marrakchi-Kacem, Johanne Germain, Claire Boutet, Claire Cury, Lucie Hertz-Pannier, Alexandre Vignaud, Stanley Durrleman, Thomas R. Henry, Pierre Francois Van De Moortele, Alain Trouve, Olivier Colliot

Research output: Contribution to journal › Article › peer-review

Abstract

Objective: 7-Tesla MRI of the hippocampus enhances the visualization of its internal substructures. Among these substructures, the cornu Ammonis and subiculum form a contiguous folded ribbon of gray matter. Here, we propose a method to analyze local thickness measurements of this ribbon. Methods: We introduce an original approach based upon the estimation of a diffeomorphic vector field that traverses the ribbon. The method is designed to handle specificities of the hippocampus and corresponding 7-Tesla acquisitions: highly convoluted surface, non-closed ribbon, incompletely defined inner/outer boundaries, anisotropic acquisitions. We furthermore propose to conduct group comparisons using a population template built from the central surfaces of individual subjects. Results: We first assessed the robustness of our approach to anisotropy, as well as to inter-rater variability, on a post-mortem scan and on in vivo acquisitions respectively. We then conducted a group study on a dataset of in vivo MRI from temporal lobe epilepsy (TLE) patients and healthy controls. The method detected local thinning patterns in patients, predominantly ipsilaterally to the seizure focus, which is consistent with medical knowledge. Conclusion: This new technique allows measuring the thickness of the hippocampus from 7-Tesla MRI. It shows good robustness with respect to anisotropy and inter-rater variability and has the potential to detect local atrophy in patients. Significance: As 7-Tesla MRI is increasingly available, this new method may become a useful tool to study local alterations of the hippocampus in brain disorders. It is made freely available to the community (code: https://github.com/aramis-lab/hiplay7-thickness, postmortem segmentation: https://doi.org/10.5281/zenodo.3533264).

Original language	English (US)
Article number	9108539
Pages (from-to)	393-403
Number of pages	11
Journal	IEEE Transactions on Biomedical Engineering
Volume	68
Issue number	2
DOIs	https://doi.org/10.1109/TBME.2020.2999941
State	Published - Feb 2021

Bibliographical note

Funding Information:
May 27, 2020. Date of publication June 4, 2020; date of current version January 20, 2021. This work was supported in part by ANR (HM-HE hippocampus is a structure of the medial temporal lobe

Funding Information:
bytheCATI project, by Investissementsd’avenir ANR-19-P3IA-0001TC,ANR-09-EMER-006),inpartbyFranceAlzheimer(IRMA7),inpart Tofthebrainwhichplaysacrucialroleinvariousneuro- (PRAIRIE3IAInstitute)andANR-10-IAIHU-06,inpartbythePhilippe logical and psychiatric diseases including epilepsy, Alzheimer’s foundation, and in part by the NSF/NIH/ANR program “Collaborative disease, schizophrenia and depression [1]. The hippocampus is a Research in Computational Neuroscience” (HIPLAY7, NSF-CRCSN- highly complex arrangement of histologically and functionally Fouquier,andÉmilieGerardincontributedequallytothiswork.)(Corre-1607835andANR-16-NEUC-0001-01).(AlexisGuyot,AnaB.Graciano distinct regions [2]. In particular, the gray matter part of the spondingauthor:OlivierColliot.) hippocampus is mainly composed of a larger ribbon, called Alexis Guyot, Ana B. Graciano Fouquier, Émilie Gerardin, Linda Ammon’s horn or cornu Ammonis (CA), folded around a small Marrakchi-Kacem, Johanne Germain, Claire Boutet, Claire Cury, and gyrus, called the dentate gyrus (DG). The cornu Ammonis is CNRS,UMR7225,SorbonneUniversité,andalsowithInria.StanleyDurrlemanarewiththeParisBrainInstitute,Inserm,U1127, further composed of four sectors: CA1-4. CA1 is the largest sec- Marie Chupin is with the Paris Brain Institute, Inserm, U 1127, CNRS, tor and is continuous with the subiculum. Moreover, subregions UMR7225,SorbonneUniversité,andalsowiththeCATI. are composed of different layers that vary in terms of cellular LucieHertz-PannieriswithNeurospin,I2BM,DSV,CEA,andalsowithJoanA.GlaunèsiswiththeMAP5,UniversitéParisDescartes. composition. The stratum pyramidale (SP) is richer in neuronal the INSERM; CEA; Université Paris Descartes. bodies whereas the strata radiatum, lacunosum and moleculare AlexandreVignaudiswithNeurospin,I2BM,DSV,CEA. (SRLM) are poorer in neuronal bodies. Histological studies Minnesota.ThomasR.HenryiswiththeDepartmentofNeurology,Universityof have shown that hippocampal subregions present differential Pierre-François van de Moortele is with the Center for Magnetic Res-vulnerability to distinct diseases, such as temporal lobe epilepsy onanceResearch,UniversityofMinnesota. (TLE) [3] and Alzheimer’s disease [4].

Publisher Copyright:
© 1964-2012 IEEE.

Keywords

7-Tesla
Diffeomorphism
Hippocampus
Magnetic Resonance Imaging
Morphometry
Thickness
Ultra-high-field

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10.1109/TBME.2020.2999941

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Guyot, A., Fouquier, A. B. G., Gerardin, E., Chupin, M., Glaunes, J. A., Marrakchi-Kacem, L., Germain, J., Boutet, C., Cury, C., Hertz-Pannier, L., Vignaud, A., Durrleman, S., Henry, T. R., Van De Moortele, P. F., Trouve, A., & Colliot, O. (2021). A Diffeomorphic Vector Field Approach to Analyze the Thickness of the Hippocampus from 7 T MRI. IEEE Transactions on Biomedical Engineering, 68(2), 393-403. [9108539]. https://doi.org/10.1109/TBME.2020.2999941

Guyot, A, Fouquier, ABG, Gerardin, E, Chupin, M, Glaunes, JA, Marrakchi-Kacem, L, Germain, J, Boutet, C, Cury, C, Hertz-Pannier, L, Vignaud, A, Durrleman, S, Henry, TR, Van De Moortele, PF, Trouve, A & Colliot, O 2021, 'A Diffeomorphic Vector Field Approach to Analyze the Thickness of the Hippocampus from 7 T MRI', IEEE Transactions on Biomedical Engineering, vol. 68, no. 2, 9108539, pp. 393-403. https://doi.org/10.1109/TBME.2020.2999941

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title = "A Diffeomorphic Vector Field Approach to Analyze the Thickness of the Hippocampus from 7 T MRI",

abstract = "Objective: 7-Tesla MRI of the hippocampus enhances the visualization of its internal substructures. Among these substructures, the cornu Ammonis and subiculum form a contiguous folded ribbon of gray matter. Here, we propose a method to analyze local thickness measurements of this ribbon. Methods: We introduce an original approach based upon the estimation of a diffeomorphic vector field that traverses the ribbon. The method is designed to handle specificities of the hippocampus and corresponding 7-Tesla acquisitions: highly convoluted surface, non-closed ribbon, incompletely defined inner/outer boundaries, anisotropic acquisitions. We furthermore propose to conduct group comparisons using a population template built from the central surfaces of individual subjects. Results: We first assessed the robustness of our approach to anisotropy, as well as to inter-rater variability, on a post-mortem scan and on in vivo acquisitions respectively. We then conducted a group study on a dataset of in vivo MRI from temporal lobe epilepsy (TLE) patients and healthy controls. The method detected local thinning patterns in patients, predominantly ipsilaterally to the seizure focus, which is consistent with medical knowledge. Conclusion: This new technique allows measuring the thickness of the hippocampus from 7-Tesla MRI. It shows good robustness with respect to anisotropy and inter-rater variability and has the potential to detect local atrophy in patients. Significance: As 7-Tesla MRI is increasingly available, this new method may become a useful tool to study local alterations of the hippocampus in brain disorders. It is made freely available to the community (code: https://github.com/aramis-lab/hiplay7-thickness, postmortem segmentation: https://doi.org/10.5281/zenodo.3533264).",

keywords = "7-Tesla, Diffeomorphism, Hippocampus, Magnetic Resonance Imaging, Morphometry, Thickness, Ultra-high-field",

author = "Alexis Guyot and Fouquier, {Ana B.Graciano} and Emilie Gerardin and Marie Chupin and Glaunes, {Joan A.} and Linda Marrakchi-Kacem and Johanne Germain and Claire Boutet and Claire Cury and Lucie Hertz-Pannier and Alexandre Vignaud and Stanley Durrleman and Henry, {Thomas R.} and {Van De Moortele}, {Pierre Francois} and Alain Trouve and Olivier Colliot",

note = "Funding Information: May 27, 2020. Date of publication June 4, 2020; date of current version January 20, 2021. This work was supported in part by ANR (HM-HE hippocampus is a structure of the medial temporal lobe Funding Information: bytheCATI project, by Investissementsd{\textquoteright}avenir ANR-19-P3IA-0001TC,ANR-09-EMER-006),inpartbyFranceAlzheimer(IRMA7),inpart Tofthebrainwhichplaysacrucialroleinvariousneuro- (PRAIRIE3IAInstitute)andANR-10-IAIHU-06,inpartbythePhilippe logical and psychiatric diseases including epilepsy, Alzheimer{\textquoteright}s foundation, and in part by the NSF/NIH/ANR program “Collaborative disease, schizophrenia and depression [1]. The hippocampus is a Research in Computational Neuroscience” (HIPLAY7, NSF-CRCSN- highly complex arrangement of histologically and functionally Fouquier,and{\'E}milieGerardincontributedequallytothiswork.)(Corre-1607835andANR-16-NEUC-0001-01).(AlexisGuyot,AnaB.Graciano distinct regions [2]. In particular, the gray matter part of the spondingauthor:OlivierColliot.) hippocampus is mainly composed of a larger ribbon, called Alexis Guyot, Ana B. Graciano Fouquier, {\'E}milie Gerardin, Linda Ammon{\textquoteright}s horn or cornu Ammonis (CA), folded around a small Marrakchi-Kacem, Johanne Germain, Claire Boutet, Claire Cury, and gyrus, called the dentate gyrus (DG). The cornu Ammonis is CNRS,UMR7225,SorbonneUniversit{\'e},andalsowithInria.StanleyDurrlemanarewiththeParisBrainInstitute,Inserm,U1127, further composed of four sectors: CA1-4. CA1 is the largest sec- Marie Chupin is with the Paris Brain Institute, Inserm, U 1127, CNRS, tor and is continuous with the subiculum. Moreover, subregions UMR7225,SorbonneUniversit{\'e},andalsowiththeCATI. are composed of different layers that vary in terms of cellular LucieHertz-PannieriswithNeurospin,I2BM,DSV,CEA,andalsowithJoanA.Glaun{\`e}siswiththeMAP5,Universit{\'e}ParisDescartes. composition. The stratum pyramidale (SP) is richer in neuronal the INSERM; CEA; Universit{\'e} Paris Descartes. bodies whereas the strata radiatum, lacunosum and moleculare AlexandreVignaudiswithNeurospin,I2BM,DSV,CEA. (SRLM) are poorer in neuronal bodies. Histological studies Minnesota.ThomasR.HenryiswiththeDepartmentofNeurology,Universityof have shown that hippocampal subregions present differential Pierre-Fran{\c c}ois van de Moortele is with the Center for Magnetic Res-vulnerability to distinct diseases, such as temporal lobe epilepsy onanceResearch,UniversityofMinnesota. (TLE) [3] and Alzheimer{\textquoteright}s disease [4]. Publisher Copyright: {\textcopyright} 1964-2012 IEEE.",

year = "2021",

month = feb,

doi = "10.1109/TBME.2020.2999941",

language = "English (US)",

volume = "68",

pages = "393--403",

journal = "IRE transactions on medical electronics",

issn = "0018-9294",

publisher = "IEEE Computer Society",

number = "2",

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TY - JOUR

T1 - A Diffeomorphic Vector Field Approach to Analyze the Thickness of the Hippocampus from 7 T MRI

AU - Guyot, Alexis

AU - Fouquier, Ana B.Graciano

AU - Gerardin, Emilie

AU - Chupin, Marie

AU - Glaunes, Joan A.

AU - Marrakchi-Kacem, Linda

AU - Germain, Johanne

AU - Boutet, Claire

AU - Cury, Claire

AU - Hertz-Pannier, Lucie

AU - Vignaud, Alexandre

AU - Durrleman, Stanley

AU - Henry, Thomas R.

AU - Van De Moortele, Pierre Francois

AU - Trouve, Alain

AU - Colliot, Olivier

N1 - Funding Information: May 27, 2020. Date of publication June 4, 2020; date of current version January 20, 2021. This work was supported in part by ANR (HM-HE hippocampus is a structure of the medial temporal lobe Funding Information: bytheCATI project, by Investissementsd’avenir ANR-19-P3IA-0001TC,ANR-09-EMER-006),inpartbyFranceAlzheimer(IRMA7),inpart Tofthebrainwhichplaysacrucialroleinvariousneuro- (PRAIRIE3IAInstitute)andANR-10-IAIHU-06,inpartbythePhilippe logical and psychiatric diseases including epilepsy, Alzheimer’s foundation, and in part by the NSF/NIH/ANR program “Collaborative disease, schizophrenia and depression [1]. The hippocampus is a Research in Computational Neuroscience” (HIPLAY7, NSF-CRCSN- highly complex arrangement of histologically and functionally Fouquier,andÉmilieGerardincontributedequallytothiswork.)(Corre-1607835andANR-16-NEUC-0001-01).(AlexisGuyot,AnaB.Graciano distinct regions [2]. In particular, the gray matter part of the spondingauthor:OlivierColliot.) hippocampus is mainly composed of a larger ribbon, called Alexis Guyot, Ana B. Graciano Fouquier, Émilie Gerardin, Linda Ammon’s horn or cornu Ammonis (CA), folded around a small Marrakchi-Kacem, Johanne Germain, Claire Boutet, Claire Cury, and gyrus, called the dentate gyrus (DG). The cornu Ammonis is CNRS,UMR7225,SorbonneUniversité,andalsowithInria.StanleyDurrlemanarewiththeParisBrainInstitute,Inserm,U1127, further composed of four sectors: CA1-4. CA1 is the largest sec- Marie Chupin is with the Paris Brain Institute, Inserm, U 1127, CNRS, tor and is continuous with the subiculum. Moreover, subregions UMR7225,SorbonneUniversité,andalsowiththeCATI. are composed of different layers that vary in terms of cellular LucieHertz-PannieriswithNeurospin,I2BM,DSV,CEA,andalsowithJoanA.GlaunèsiswiththeMAP5,UniversitéParisDescartes. composition. The stratum pyramidale (SP) is richer in neuronal the INSERM; CEA; Université Paris Descartes. bodies whereas the strata radiatum, lacunosum and moleculare AlexandreVignaudiswithNeurospin,I2BM,DSV,CEA. (SRLM) are poorer in neuronal bodies. Histological studies Minnesota.ThomasR.HenryiswiththeDepartmentofNeurology,Universityof have shown that hippocampal subregions present differential Pierre-François van de Moortele is with the Center for Magnetic Res-vulnerability to distinct diseases, such as temporal lobe epilepsy onanceResearch,UniversityofMinnesota. (TLE) [3] and Alzheimer’s disease [4]. Publisher Copyright: © 1964-2012 IEEE.

PY - 2021/2

Y1 - 2021/2

N2 - Objective: 7-Tesla MRI of the hippocampus enhances the visualization of its internal substructures. Among these substructures, the cornu Ammonis and subiculum form a contiguous folded ribbon of gray matter. Here, we propose a method to analyze local thickness measurements of this ribbon. Methods: We introduce an original approach based upon the estimation of a diffeomorphic vector field that traverses the ribbon. The method is designed to handle specificities of the hippocampus and corresponding 7-Tesla acquisitions: highly convoluted surface, non-closed ribbon, incompletely defined inner/outer boundaries, anisotropic acquisitions. We furthermore propose to conduct group comparisons using a population template built from the central surfaces of individual subjects. Results: We first assessed the robustness of our approach to anisotropy, as well as to inter-rater variability, on a post-mortem scan and on in vivo acquisitions respectively. We then conducted a group study on a dataset of in vivo MRI from temporal lobe epilepsy (TLE) patients and healthy controls. The method detected local thinning patterns in patients, predominantly ipsilaterally to the seizure focus, which is consistent with medical knowledge. Conclusion: This new technique allows measuring the thickness of the hippocampus from 7-Tesla MRI. It shows good robustness with respect to anisotropy and inter-rater variability and has the potential to detect local atrophy in patients. Significance: As 7-Tesla MRI is increasingly available, this new method may become a useful tool to study local alterations of the hippocampus in brain disorders. It is made freely available to the community (code: https://github.com/aramis-lab/hiplay7-thickness, postmortem segmentation: https://doi.org/10.5281/zenodo.3533264).

AB - Objective: 7-Tesla MRI of the hippocampus enhances the visualization of its internal substructures. Among these substructures, the cornu Ammonis and subiculum form a contiguous folded ribbon of gray matter. Here, we propose a method to analyze local thickness measurements of this ribbon. Methods: We introduce an original approach based upon the estimation of a diffeomorphic vector field that traverses the ribbon. The method is designed to handle specificities of the hippocampus and corresponding 7-Tesla acquisitions: highly convoluted surface, non-closed ribbon, incompletely defined inner/outer boundaries, anisotropic acquisitions. We furthermore propose to conduct group comparisons using a population template built from the central surfaces of individual subjects. Results: We first assessed the robustness of our approach to anisotropy, as well as to inter-rater variability, on a post-mortem scan and on in vivo acquisitions respectively. We then conducted a group study on a dataset of in vivo MRI from temporal lobe epilepsy (TLE) patients and healthy controls. The method detected local thinning patterns in patients, predominantly ipsilaterally to the seizure focus, which is consistent with medical knowledge. Conclusion: This new technique allows measuring the thickness of the hippocampus from 7-Tesla MRI. It shows good robustness with respect to anisotropy and inter-rater variability and has the potential to detect local atrophy in patients. Significance: As 7-Tesla MRI is increasingly available, this new method may become a useful tool to study local alterations of the hippocampus in brain disorders. It is made freely available to the community (code: https://github.com/aramis-lab/hiplay7-thickness, postmortem segmentation: https://doi.org/10.5281/zenodo.3533264).

KW - 7-Tesla

KW - Diffeomorphism

KW - Hippocampus

KW - Magnetic Resonance Imaging

KW - Morphometry

KW - Thickness

KW - Ultra-high-field

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A Diffeomorphic Vector Field Approach to Analyze the Thickness of the Hippocampus from 7 T MRI

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