Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI

Towards a harmonized segmentation protocol

Paul A. Yushkevich, Robert S C Amaral, Jean C. Augustinack, Andrew R. Bender, Jeffrey D. Bernstein, Marina Boccardi, Martina Bocchetta, Alison C. Burggren, Valerie A. Carr, M. Mallar Chakravarty, Gaël Chételat, Ana M. Daugherty, Lila Davachi, Song Lin Ding, Arne Ekstrom, Mirjam I. Geerlings, Abdul Hassan, Yushan Huang, J. Eugenio Iglesias, Renaud La Joie & 27 others Geoffrey A. Kerchner, Karen F. LaRocque, Laura A. Libby, Nikolai Malykhin, Susanne G. Mueller, Rosanna K. Olsen, Daniela J. Palombo, Mansi B. Parekh, John B. Pluta, Alison R. Preston, Jens C. Pruessner, Charan Ranganath, Naftali Raz, Margaret L. Schlichting, Dorothee Schoemaker, Sachi Singh, Craig E L Stark, Nanthia Suthana, Alexa Tompary, Marta M. Turowski, Koen Van Leemput, Anthony D. Wagner, Lei Wang, Julie L. Winterburn, Laura E M Wisse, Michael A. Yassa, Michael M. Zeineh

Research output: Contribution to journalArticle

107 Citations (Scopus)

Abstract

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 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. 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.

Original languageEnglish
Pages (from-to)526-541
Number of pages16
JournalNeuroImage
Volume111
DOIs
Publication statusPublished - May 1 2015

Fingerprint

Hippocampus
Magnetic Resonance Imaging
Parahippocampal Gyrus
Aptitude
Dentate Gyrus
Research
Cues
Tail

Keywords

  • CA1
  • CA2
  • CA3
  • Dentate gyrus
  • Entorhinal cortex
  • Hippocampal subfields
  • Hippocampus
  • Magnetic resonance imaging
  • Medial temporal lobe
  • Parahippocampal gyrus
  • Perirhinal cortex
  • Segmentation
  • Subiculum
  • Unified protocol

ASJC Scopus subject areas

  • Cognitive Neuroscience
  • Neurology

Cite this

Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI : Towards a harmonized segmentation protocol. / Yushkevich, Paul A.; Amaral, Robert S C; Augustinack, Jean C.; Bender, Andrew R.; Bernstein, Jeffrey D.; Boccardi, Marina; Bocchetta, Martina; Burggren, Alison C.; Carr, Valerie A.; Chakravarty, M. Mallar; Chételat, Gaël; Daugherty, Ana M.; Davachi, Lila; Ding, Song Lin; Ekstrom, Arne; Geerlings, Mirjam I.; Hassan, Abdul; Huang, Yushan; Iglesias, J. Eugenio; La Joie, Renaud; Kerchner, Geoffrey A.; LaRocque, Karen F.; Libby, Laura A.; Malykhin, Nikolai; Mueller, Susanne G.; Olsen, Rosanna K.; Palombo, Daniela J.; Parekh, Mansi B.; Pluta, John B.; Preston, Alison R.; Pruessner, Jens C.; Ranganath, Charan; Raz, Naftali; Schlichting, Margaret L.; Schoemaker, Dorothee; Singh, Sachi; Stark, Craig E L; Suthana, Nanthia; Tompary, Alexa; Turowski, Marta M.; Van Leemput, Koen; Wagner, Anthony D.; Wang, Lei; Winterburn, Julie L.; Wisse, Laura E M; Yassa, Michael A.; Zeineh, Michael M.

In: NeuroImage, Vol. 111, 01.05.2015, p. 526-541.

Research output: Contribution to journalArticle

Yushkevich, PA, Amaral, RSC, Augustinack, JC, Bender, AR, Bernstein, JD, Boccardi, M, Bocchetta, M, Burggren, AC, Carr, VA, Chakravarty, MM, Chételat, G, Daugherty, AM, Davachi, L, Ding, SL, Ekstrom, A, Geerlings, MI, Hassan, A, Huang, Y, Iglesias, JE, La Joie, R, Kerchner, GA, LaRocque, KF, Libby, LA, Malykhin, N, Mueller, SG, Olsen, RK, Palombo, DJ, Parekh, MB, Pluta, JB, Preston, AR, Pruessner, JC, Ranganath, C, Raz, N, Schlichting, ML, Schoemaker, D, Singh, S, Stark, CEL, Suthana, N, Tompary, A, Turowski, MM, Van Leemput, K, Wagner, AD, Wang, L, Winterburn, JL, Wisse, LEM, Yassa, MA & Zeineh, MM 2015, 'Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI: Towards a harmonized segmentation protocol', NeuroImage, vol. 111, pp. 526-541. https://doi.org/10.1016/j.neuroimage.2015.01.004
Yushkevich, Paul A. ; Amaral, Robert S C ; Augustinack, Jean C. ; Bender, Andrew R. ; Bernstein, Jeffrey D. ; Boccardi, Marina ; Bocchetta, Martina ; Burggren, Alison C. ; Carr, Valerie A. ; Chakravarty, M. Mallar ; Chételat, Gaël ; Daugherty, Ana M. ; Davachi, Lila ; Ding, Song Lin ; Ekstrom, Arne ; Geerlings, Mirjam I. ; Hassan, Abdul ; Huang, Yushan ; Iglesias, J. Eugenio ; La Joie, Renaud ; Kerchner, Geoffrey A. ; LaRocque, Karen F. ; Libby, Laura A. ; Malykhin, Nikolai ; Mueller, Susanne G. ; Olsen, Rosanna K. ; Palombo, Daniela J. ; Parekh, Mansi B. ; Pluta, John B. ; Preston, Alison R. ; Pruessner, Jens C. ; Ranganath, Charan ; Raz, Naftali ; Schlichting, Margaret L. ; Schoemaker, Dorothee ; Singh, Sachi ; Stark, Craig E L ; Suthana, Nanthia ; Tompary, Alexa ; Turowski, Marta M. ; Van Leemput, Koen ; Wagner, Anthony D. ; Wang, Lei ; Winterburn, Julie L. ; Wisse, Laura E M ; Yassa, Michael A. ; Zeineh, Michael M. / Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI : Towards a harmonized segmentation protocol. In: NeuroImage. 2015 ; Vol. 111. pp. 526-541.
@article{84b2f4f4420e4b2dacd94d65d2b66ffb,
title = "Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI: Towards a harmonized segmentation protocol",
abstract = "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 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. 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.",
keywords = "CA1, CA2, CA3, Dentate gyrus, Entorhinal cortex, Hippocampal subfields, Hippocampus, Magnetic resonance imaging, Medial temporal lobe, Parahippocampal gyrus, Perirhinal cortex, Segmentation, Subiculum, Unified protocol",
author = "Yushkevich, {Paul A.} and Amaral, {Robert S C} and Augustinack, {Jean C.} and Bender, {Andrew R.} and Bernstein, {Jeffrey D.} and Marina Boccardi and Martina Bocchetta and Burggren, {Alison C.} and Carr, {Valerie A.} and Chakravarty, {M. Mallar} and Ga{\"e}l Ch{\'e}telat and Daugherty, {Ana M.} and Lila Davachi and Ding, {Song Lin} and Arne Ekstrom and Geerlings, {Mirjam I.} and Abdul Hassan and Yushan Huang and Iglesias, {J. Eugenio} and {La Joie}, Renaud and Kerchner, {Geoffrey A.} and LaRocque, {Karen F.} and Libby, {Laura A.} and Nikolai Malykhin and Mueller, {Susanne G.} and Olsen, {Rosanna K.} and Palombo, {Daniela J.} and Parekh, {Mansi B.} and Pluta, {John B.} and Preston, {Alison R.} and Pruessner, {Jens C.} and Charan Ranganath and Naftali Raz and Schlichting, {Margaret L.} and Dorothee Schoemaker and Sachi Singh and Stark, {Craig E L} and Nanthia Suthana and Alexa Tompary and Turowski, {Marta M.} and {Van Leemput}, Koen and Wagner, {Anthony D.} and Lei Wang and Winterburn, {Julie L.} and Wisse, {Laura E M} and Yassa, {Michael A.} and Zeineh, {Michael M.}",
year = "2015",
month = "5",
day = "1",
doi = "10.1016/j.neuroimage.2015.01.004",
language = "English",
volume = "111",
pages = "526--541",
journal = "NeuroImage",
issn = "1053-8119",
publisher = "Academic Press Inc.",

}

TY - JOUR

T1 - Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI

T2 - Towards a harmonized segmentation protocol

AU - Yushkevich, Paul A.

AU - Amaral, Robert S C

AU - Augustinack, Jean C.

AU - Bender, Andrew R.

AU - Bernstein, Jeffrey D.

AU - Boccardi, Marina

AU - Bocchetta, Martina

AU - Burggren, Alison C.

AU - Carr, Valerie A.

AU - Chakravarty, M. Mallar

AU - Chételat, Gaël

AU - Daugherty, Ana M.

AU - Davachi, Lila

AU - Ding, Song Lin

AU - Ekstrom, Arne

AU - Geerlings, Mirjam I.

AU - Hassan, Abdul

AU - Huang, Yushan

AU - Iglesias, J. Eugenio

AU - La Joie, Renaud

AU - Kerchner, Geoffrey A.

AU - LaRocque, Karen F.

AU - Libby, Laura A.

AU - Malykhin, Nikolai

AU - Mueller, Susanne G.

AU - Olsen, Rosanna K.

AU - Palombo, Daniela J.

AU - Parekh, Mansi B.

AU - Pluta, John B.

AU - Preston, Alison R.

AU - Pruessner, Jens C.

AU - Ranganath, Charan

AU - Raz, Naftali

AU - Schlichting, Margaret L.

AU - Schoemaker, Dorothee

AU - Singh, Sachi

AU - Stark, Craig E L

AU - Suthana, Nanthia

AU - Tompary, Alexa

AU - Turowski, Marta M.

AU - Van Leemput, Koen

AU - Wagner, Anthony D.

AU - Wang, Lei

AU - Winterburn, Julie L.

AU - Wisse, Laura E M

AU - Yassa, Michael A.

AU - Zeineh, Michael M.

PY - 2015/5/1

Y1 - 2015/5/1

N2 - 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 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. 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.

AB - 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 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. 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.

KW - CA1

KW - CA2

KW - CA3

KW - Dentate gyrus

KW - Entorhinal cortex

KW - Hippocampal subfields

KW - Hippocampus

KW - Magnetic resonance imaging

KW - Medial temporal lobe

KW - Parahippocampal gyrus

KW - Perirhinal cortex

KW - Segmentation

KW - Subiculum

KW - Unified protocol

UR - http://www.scopus.com/inward/record.url?scp=84939468449&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84939468449&partnerID=8YFLogxK

U2 - 10.1016/j.neuroimage.2015.01.004

DO - 10.1016/j.neuroimage.2015.01.004

M3 - Article

VL - 111

SP - 526

EP - 541

JO - NeuroImage

JF - NeuroImage

SN - 1053-8119

ER -