Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI: Towards a harmonized segmentation protocol
An increasing number of human in vivo magnetic resonance imaging (MRI) studies have focused on examining the structure and function of the subfields of the hippocampal formation (the dentate gyrus, CA fields 1−3, and the subiculum) and subregions of the parahippocampal gyrus (entorhinal, perirhinal,...
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| Published in | NeuroImage (Orlando, Fla.) Vol. 111; pp. 526 - 541 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.05.2015
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1053-8119 1095-9572 1095-9572 |
| DOI | 10.1016/j.neuroimage.2015.01.004 |
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| Abstract | An increasing number of human in vivo magnetic resonance imaging (MRI) studies have focused on examining the structure and function of the subfields of the hippocampal formation (the dentate gyrus, CA fields 1−3, and the subiculum) and subregions of the parahippocampal gyrus (entorhinal, perirhinal, and parahippocampal cortices). The ability to interpret the results of such studies and to relate them to each other would be improved if a common standard existed for labeling hippocampal subfields and parahippocampal subregions. Currently, research groups label different subsets of structures and use different rules, landmarks, and cues to define their anatomical extents. This paper characterizes, both qualitatively and quantitatively, the variability in the existing manual segmentation protocols for labeling hippocampal and parahippocampal substructures in MRI, with the goal of guiding subsequent work on developing a harmonized substructure segmentation protocol.
MRI scans of a single healthy adult human subject were acquired both at 3T and 7T. Representatives from 21 research groups applied their respective manual segmentation protocols to the MRI modalities of their choice. The resulting set of 21 segmentations was analyzed in a common anatomical space to quantify similarity and identify areas of agreement.
The differences between the 21 protocols include the region within which segmentation is performed, the set of anatomical labels used, and the extents of specific anatomical labels. The greatest overall disagreement among the protocols is at the CA1/subiculum boundary, and disagreement across all structures is greatest in the anterior portion of the hippocampal formation relative to the body and tail.
The combined examination of the 21 protocols in the same dataset suggests possible strategies towards developing a harmonized subfield segmentation protocol and facilitates comparison between published studies.
•We compare 21 manual protocols for labeling hippocampal and parahippocampal subfields.•21 research groups applied their own manual segmentation protocol to the same anatomy.•Fuzzy similarity metrics used to quantify disagreement between protocols•Greatest disagreement is along the CA1/subiculum boundary, anterior hippocampus.•We propose a strategy for developing a harmonized segmentation protocol. |
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| AbstractList | An increasing number of human in vivo magnetic resonance imaging (MRI) studies have focused on examining the structure and function of the subfields of the hippocampal formation (the dentate gyrus, CA fields 1−3, and the subiculum) and subregions of the parahippocampal gyrus (entorhinal, perirhinal, and parahippocampal cortices). The ability to interpret the results of such studies and to relate them to each other would be improved if a common standard existed for labeling hippocampal subfields and parahippocampal subregions. Currently, research groups label different subsets of structures and use different rules, landmarks, and cues to define their anatomical extents. This paper characterizes, both qualitatively and quantitatively, the variability in the existing manual segmentation protocols for labeling hippocampal and parahippocampal substructures in MRI, with the goal of guiding subsequent work on developing a harmonized substructure segmentation protocol.
MRI scans of a single healthy adult human subject were acquired both at 3T and 7T. Representatives from 21 research groups applied their respective manual segmentation protocols to the MRI modalities of their choice. The resulting set of 21 segmentations was analyzed in a common anatomical space to quantify similarity and identify areas of agreement.
The differences between the 21 protocols include the region within which segmentation is performed, the set of anatomical labels used, and the extents of specific anatomical labels. The greatest overall disagreement among the protocols is at the CA1/subiculum boundary, and disagreement across all structures is greatest in the anterior portion of the hippocampal formation relative to the body and tail.
The combined examination of the 21 protocols in the same dataset suggests possible strategies towards developing a harmonized subfield segmentation protocol and facilitates comparison between published studies.
•We compare 21 manual protocols for labeling hippocampal and parahippocampal subfields.•21 research groups applied their own manual segmentation protocol to the same anatomy.•Fuzzy similarity metrics used to quantify disagreement between protocols•Greatest disagreement is along the CA1/subiculum boundary, anterior hippocampus.•We propose a strategy for developing a harmonized segmentation protocol. Objective An increasing number of human in vivo magnetic resonance imaging (MRI) studies have focused on examining the structure and function of the subfields of the hippocampal formation (the dentate gyrus, CA fields 1-3, and the subiculum) and subregions of the parahippocampal gyrus (entorhinal, perirhinal, and parahippocampal cortices). The ability to interpret the results of such studies and to relate them to each other would be improved if a common standard existed for labeling hippocampal subfields and parahippocampal subregions. Currently, research groups label different subsets of structures and use different rules, landmarks, and cues to define their anatomical extents. This paper characterizes, both qualitatively and quantitatively, the variability in the existing manual segmentation protocols for labeling hippocampal and parahippocampal substructures in MRI, with the goal of guiding subsequent work on developing a harmonized substructure segmentation protocol. Method MRI scans of a single healthy adult human subject were acquired both at 3T and 7T. Representatives from 21 research groups applied their respective manual segmentation protocols to the MRI modalities of their choice. The resulting set of 21 segmentations was analyzed in a common anatomical space to quantify similarity and identify areas of agreement. Results The differences between the 21 protocols include the region within which segmentation is performed, the set of anatomical labels used, and the extents of specific anatomical labels. The greatest overall disagreement among the protocols is at the CA1/subiculum boundary, and disagreement across all structures is greatest in the anterior portion of the hippocampal formation relative to the body and tail. Conclusions The combined examination of the 21 protocols in the same dataset suggests possible strategies towards developing a harmonized subfield segmentation protocol and facilitates comparison between published studies. An increasing number of human in vivo magnetic resonance imaging (MRI) studies have focused on examining the structure and function of the subfields of the hippocampal formation (the dentate gyrus, CA fields 1-3, and the subiculum) and subregions of the parahippocampal gyrus (entorhinal, perirhinal, and parahippocampal cortices). The ability to interpret the results of such studies and to relate them to each other would be improved if a common standard existed for labeling hippocampal subfields and parahippocampal subregions. Currently, research groups label different subsets of structures and use different rules, landmarks, and cues to define their anatomical extents. This paper characterizes, both qualitatively and quantitatively, the variability in the existing manual segmentation protocols for labeling hippocampal and parahippocampal substructures in MRI, with the goal of guiding subsequent work on developing a harmonized substructure segmentation protocol. MRI scans of a single healthy adult human subject were acquired both at 3 T and 7 T. Representatives from 21 research groups applied their respective manual segmentation protocols to the MRI modalities of their choice. The resulting set of 21 segmentations was analyzed in a common anatomical space to quantify similarity and identify areas of agreement. The differences between the 21 protocols include the region within which segmentation is performed, the set of anatomical labels used, and the extents of specific anatomical labels. The greatest overall disagreement among the protocols is at the CA1/subiculum boundary, and disagreement across all structures is greatest in the anterior portion of the hippocampal formation relative to the body and tail. The combined examination of the 21 protocols in the same dataset suggests possible strategies towards developing a harmonized subfield segmentation protocol and facilitates comparison between published studies. An increasing number of human in vivo magnetic resonance imaging (MRI) studies have focused on examining the structure and function of the subfields of the hippocampal formation (the dentate gyrus, CA fields 1-3, and the subiculum) and subregions of the parahippocampal gyrus (entorhinal, perirhinal, and parahippocampal cortices). The ability to interpret the results of such studies and to relate them to each other would be improved if a common standard existed for labeling hippocampal subfields and parahippocampal subregions. Currently, research groups label different subsets of structures and use different rules, landmarks, and cues to define their anatomical extents. This paper characterizes, both qualitatively and quantitatively, the variability in the existing manual segmentation protocols for labeling hippocampal and parahippocampal substructures in MRI, with the goal of guiding subsequent work on developing a harmonized substructure segmentation protocol.OBJECTIVEAn increasing number of human in vivo magnetic resonance imaging (MRI) studies have focused on examining the structure and function of the subfields of the hippocampal formation (the dentate gyrus, CA fields 1-3, and the subiculum) and subregions of the parahippocampal gyrus (entorhinal, perirhinal, and parahippocampal cortices). The ability to interpret the results of such studies and to relate them to each other would be improved if a common standard existed for labeling hippocampal subfields and parahippocampal subregions. Currently, research groups label different subsets of structures and use different rules, landmarks, and cues to define their anatomical extents. This paper characterizes, both qualitatively and quantitatively, the variability in the existing manual segmentation protocols for labeling hippocampal and parahippocampal substructures in MRI, with the goal of guiding subsequent work on developing a harmonized substructure segmentation protocol.MRI scans of a single healthy adult human subject were acquired both at 3 T and 7 T. Representatives from 21 research groups applied their respective manual segmentation protocols to the MRI modalities of their choice. The resulting set of 21 segmentations was analyzed in a common anatomical space to quantify similarity and identify areas of agreement.METHODMRI scans of a single healthy adult human subject were acquired both at 3 T and 7 T. Representatives from 21 research groups applied their respective manual segmentation protocols to the MRI modalities of their choice. The resulting set of 21 segmentations was analyzed in a common anatomical space to quantify similarity and identify areas of agreement.The differences between the 21 protocols include the region within which segmentation is performed, the set of anatomical labels used, and the extents of specific anatomical labels. The greatest overall disagreement among the protocols is at the CA1/subiculum boundary, and disagreement across all structures is greatest in the anterior portion of the hippocampal formation relative to the body and tail.RESULTSThe differences between the 21 protocols include the region within which segmentation is performed, the set of anatomical labels used, and the extents of specific anatomical labels. The greatest overall disagreement among the protocols is at the CA1/subiculum boundary, and disagreement across all structures is greatest in the anterior portion of the hippocampal formation relative to the body and tail.The combined examination of the 21 protocols in the same dataset suggests possible strategies towards developing a harmonized subfield segmentation protocol and facilitates comparison between published studies.CONCLUSIONSThe combined examination of the 21 protocols in the same dataset suggests possible strategies towards developing a harmonized subfield segmentation protocol and facilitates comparison between published studies. |
| Author | Pluta, John B. Schoemaker, Dorothee Hassan, Abdul Preston, Alison R. Augustinack, Jean C. Yassa, Michael A. Wisse, Laura E.M. Ranganath, Charan Raz, Naftali Van Leemput, Koen Bocchetta, Martina Schlichting, Margaret L. Amaral, Robert S.C. Bernstein, Jeffrey D. Zeineh, Michael M. Boccardi, Marina Ding, Song-Lin Iglesias, J. Eugenio Yushkevich, Paul A. Davachi, Lila Chételat, Gaël Geerlings, Mirjam I. Chakravarty, M. Mallar Palombo, Daniela J. LaRocque, Karen F. Mueller, Susanne G. Kerchner, Geoffrey A. Pruessner, Jens C. Parekh, Mansi B. Stark, Craig E.L. Singh, Sachi Ekstrom, Arne Carr, Valerie A. Wagner, Anthony D. La Joie, Renaud Burggren, Alison C. Tompary, Alexa Libby, Laura A. Turowski, Marta M. Huang, Yushan Olsen, Rosanna K. Wang, Lei Suthana, Nanthia Daugherty, Ana M. Bender, Andrew R. Malykhin, Nikolai Winterburn, Julie L. |
| AuthorAffiliation | z VA Boston Healthcare System u Basque Center on Cognition, Brain and Language (BCBL), Donostia-San Sebastian, Spain ae Department of Neuroscience, The University of Texas at Austin j Department of Psychology, Stanford University af McGill Centre for Studies in Aging, Faculty of Medicine, McGill University k Departments of Psychiatry and Biomedical Engineering, McGill University aa Department of Radiology, Stanford University am Department of Radiology, Northwestern University Feinberg School of Medicine t Department of Biomedical Engineering, University of Alberta, Edmonton, Alberta, Canada y Rotman Research Institute, Baycrest ak Department of Applied Mathematics and Computer Science, Technical University of Denmark n Department of Pyschology, New York University c A.A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital f Stanford Center for Memory Disorders ah Department of Psychiatry and Behavioral Sciences, Northwestern Univer |
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| Author_xml | – sequence: 1 givenname: Paul A. orcidid: 0000-0001-8543-4016 surname: Yushkevich fullname: Yushkevich, Paul A. email: pauly2@upenn.edu organization: Penn Image Computing and Science Laboratory, Department of Radiology, University of Pennsylvania, USA – sequence: 2 givenname: Robert S.C. surname: Amaral fullname: Amaral, Robert S.C. organization: Cerebral Imaging Centre, Douglas Mental Health University Institute, McGill University, Canada – sequence: 3 givenname: Jean C. surname: Augustinack fullname: Augustinack, Jean C. organization: A.A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, USA – sequence: 4 givenname: Andrew R. surname: Bender fullname: Bender, Andrew R. organization: Institute of Gerontology, Wayne State University, USA – sequence: 5 givenname: Jeffrey D. surname: Bernstein fullname: Bernstein, Jeffrey D. organization: Department of Neurology and Neurological Sciences, Stanford University School of Medicine, USA – sequence: 6 givenname: Marina surname: Boccardi fullname: Boccardi, Marina organization: LENITEM (Laboratory of Epidemiology, Neuroimaging and Telemedicine), IRCCS Centro S. Giovanni di Dio Fatebenefratelli, Italy – sequence: 7 givenname: Martina surname: Bocchetta fullname: Bocchetta, Martina organization: LENITEM (Laboratory of Epidemiology, Neuroimaging and Telemedicine), IRCCS Centro S. 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Mallar organization: Cerebral Imaging Centre, Douglas Mental Health University Institute, McGill University, Canada – sequence: 11 givenname: Gaël surname: Chételat fullname: Chételat, Gaël organization: INSERM U1077, Universitè de Caen Basse-Normandie, UMR-S1077, Ecole Pratique des Hautes Etudes, CHU de Caen, U1077, Caen, France – sequence: 12 givenname: Ana M. surname: Daugherty fullname: Daugherty, Ana M. organization: Institute of Gerontology, Wayne State University, USA – sequence: 13 givenname: Lila surname: Davachi fullname: Davachi, Lila organization: Department of Psychology, New York University, USA – sequence: 14 givenname: Song-Lin surname: Ding fullname: Ding, Song-Lin organization: Allen Institute for Brain Science, USA – sequence: 15 givenname: Arne surname: Ekstrom fullname: Ekstrom, Arne organization: Center for Neuroscience, University of California, Davis, USA – sequence: 16 givenname: Mirjam I. surname: Geerlings fullname: Geerlings, Mirjam I. organization: Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Netherlands – sequence: 17 givenname: Abdul surname: Hassan fullname: Hassan, Abdul organization: Center for Neuroscience, University of California, Davis, USA – sequence: 18 givenname: Yushan surname: Huang fullname: Huang, Yushan organization: Department of Biomedical Engineering, University of Alberta, Edmonton, Alberta, Canada – sequence: 19 givenname: J. 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Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, USA – sequence: 20 givenname: Renaud surname: La Joie fullname: La Joie, Renaud organization: INSERM U1077, Universitè de Caen Basse-Normandie, UMR-S1077, Ecole Pratique des Hautes Etudes, CHU de Caen, U1077, Caen, France – sequence: 21 givenname: Geoffrey A. surname: Kerchner fullname: Kerchner, Geoffrey A. organization: Department of Neurology and Neurological Sciences, Stanford University School of Medicine, USA – sequence: 22 givenname: Karen F. orcidid: 0000-0002-6058-2706 surname: LaRocque fullname: LaRocque, Karen F. organization: Department of Psychology, Stanford University, USA – sequence: 23 givenname: Laura A. orcidid: 0000-0003-1484-4573 surname: Libby fullname: Libby, Laura A. organization: Center for Neuroscience, University of California, Davis, USA – sequence: 24 givenname: Nikolai surname: Malykhin fullname: Malykhin, Nikolai organization: Department of Biomedical Engineering, University of Alberta, Edmonton, Alberta, Canada – sequence: 25 givenname: Susanne G. surname: Mueller fullname: Mueller, Susanne G. organization: Department of Radiology, University of California, San Francisco, USA – sequence: 26 givenname: Rosanna K. surname: Olsen fullname: Olsen, Rosanna K. organization: Rotman Research Institute, Baycrest, Canada – sequence: 27 givenname: Daniela J. surname: Palombo fullname: Palombo, Daniela J. organization: VA Boston Healthcare System, USA – sequence: 28 givenname: Mansi B. surname: Parekh fullname: Parekh, Mansi B. organization: Department of Radiology, Stanford University, USA – sequence: 29 givenname: John B. surname: Pluta fullname: Pluta, John B. organization: Penn Image Computing and Science Laboratory, Department of Radiology, University of Pennsylvania, USA – sequence: 30 givenname: Alison R. surname: Preston fullname: Preston, Alison R. organization: Department of Psychology, The University of Texas at Austin, USA – sequence: 31 givenname: Jens C. surname: Pruessner fullname: Pruessner, Jens C. organization: McGill Centre for Studies in Aging, Faculty of Medicine, McGill University, Canada – sequence: 32 givenname: Charan surname: Ranganath fullname: Ranganath, Charan organization: Center for Neuroscience, University of California, Davis, USA – sequence: 33 givenname: Naftali surname: Raz fullname: Raz, Naftali organization: Institute of Gerontology, Wayne State University, USA – sequence: 34 givenname: Margaret L. surname: Schlichting fullname: Schlichting, Margaret L. organization: Department of Psychology, The University of Texas at Austin, USA – sequence: 35 givenname: Dorothee surname: Schoemaker fullname: Schoemaker, Dorothee organization: McGill Centre for Studies in Aging, Faculty of Medicine, McGill University, Canada – sequence: 36 givenname: Sachi surname: Singh fullname: Singh, Sachi organization: Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, USA – sequence: 37 givenname: Craig E.L. surname: Stark fullname: Stark, Craig E.L. organization: Department of Neurobiology and Behavior, University of California, Irvine, USA – sequence: 38 givenname: Nanthia surname: Suthana fullname: Suthana, Nanthia organization: Department of Neurosurgery, University of California, Los Angeles, USA – sequence: 39 givenname: Alexa surname: Tompary fullname: Tompary, Alexa organization: Department of Psychology, New York University, USA – sequence: 40 givenname: Marta M. surname: Turowski fullname: Turowski, Marta M. organization: Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, USA – sequence: 41 givenname: Koen orcidid: 0000-0001-6466-5309 surname: Van Leemput fullname: Van Leemput, Koen organization: A.A. Martinos Center for Biomedical Imaging, Department of Radiology, Harvard Medical School, Massachusetts General Hospital, USA – sequence: 42 givenname: Anthony D. orcidid: 0000-0003-0624-4543 surname: Wagner fullname: Wagner, Anthony D. organization: Department of Psychology, Stanford University, USA – sequence: 43 givenname: Lei surname: Wang fullname: Wang, Lei organization: Department of Psychiatry and Behavioral Sciences, Northwestern University Feinberg School of Medicine, USA – sequence: 44 givenname: Julie L. surname: Winterburn fullname: Winterburn, Julie L. organization: Cerebral Imaging Centre, Douglas Mental Health University Institute, McGill University, Canada – sequence: 45 givenname: Laura E.M. surname: Wisse fullname: Wisse, Laura E.M. organization: Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Netherlands – sequence: 46 givenname: Michael A. surname: Yassa fullname: Yassa, Michael A. organization: Department of Neurobiology and Behavior, University of California, Irvine, USA – sequence: 47 givenname: Michael M. surname: Zeineh fullname: Zeineh, Michael M. organization: Department of Radiology, Stanford University, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25596463$$D View this record in MEDLINE/PubMed |
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| Title | Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI: Towards a harmonized segmentation protocol |
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