Progress update from the hippocampal subfields group

Rosanna K Olsen^{1

2}, Valerie A Carr³, Ana M Daugherty^{4

5

6}, Renaud La Joie⁷, Robert S C Amaral⁸, Katrin Amunts^{9

10

11}, Jean C Augustinack^{12

13}, Arnold Bakker¹⁴, Andrew R Bender^{15

16

17}, David Berron^{18

19}, Marina Boccardi^{20

21}, Martina Bocchetta²², Alison C Burggren²³, M Mallar Chakravarty^{8

24

25}, Gaël Chételat^{26

27

28}, Robin de Flores^{26

27}, Jordan DeKraker²⁹, Song-Lin Ding³⁰, Mirjam I Geerlings^{31

32}, Yushan Huang³³, Ricardo Insausti³⁴, Elliott G Johnson³⁵, Prabesh Kanel³⁶, Olga Kedo¹⁰, Kristen M Kennedy³⁷, Attila Keresztes^{38

39}, Joshua K Lee^{40

35}, Ulman Lindenberger^{39

41}, Susanne G Mueller⁴², Elizabeth M Mulligan⁴³, Noa Ofen^{4

6

44}, Daniela J Palombo⁴⁵, Lorenzo Pasquini⁷, John Pluta⁴⁶, Naftali Raz^{4

6

38}, Karen M Rodrigue³⁷, Margaret L Schlichting², Yee Lee Shing^{38

47}, Craig E L Stark⁴⁸, Trevor A Steve⁴⁹, Nanthia A Suthana⁵⁰, Lei Wang⁵¹, Markus Werkle-Bergner³⁸, Paul A Yushkevich⁵², Qijing Yu^{4

6}, Laura E M Wisse^{52

53}; Hippocampal Subfields Group

Affiliations

¹ Rotman Research Institute, Baycrest Health Sciences, Toronto, Ontario, Canada.
² Department of Psychology, University of Toronto, Toronto, Ontario, Canada.
³ Department of Psychology, San Jose State University, San Jose, CA, USA.
⁴ Department of Psychology, Wayne State University, Detroit, MI, USA.
⁵ Department of Psychiatry and Behavioral Neurosciences, Wayne State University, Detroit, MI, USA.
⁶ Institute of Gerontology, Wayne State University, Detroit, MI, USA.
⁷ Department of Neurology, Memory and Aging Center, University of California, San Francisco, CA, USA.
⁸ Cerebral Imaging Centre, Douglas Hospital Mental Health University Institute, Verdun, Quebec, Canada.
⁹ C. and O. Vogt Institute for Brain Research, Medical Faculty, University Hospital Düsseldorf, Düsseldorf, Germany.
¹⁰ Heinrich Heine University Düsseldorf, Düsseldorf, Germany.
¹¹ Institute of Neuroscience and Medicine (INM-1), Research Centre Jülich, Jülich, Germany.
¹² Department of Radiology, Harvard Medical School, Charlestown, MA, USA.
¹³ Massachusetts General Hospital, Charlestown, MA, USA.
¹⁴ Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
¹⁵ Department of Epidemiology and Biostatistics, Michigan State University, East Lansing, MI, USA.
¹⁶ Department of Neurology and Ophthalmology, Michigan State University, East Lansing, MI, USA.
¹⁷ College of Human Medicine, Michigan State University, East Lansing, MI, USA.
¹⁸ Clinical Memory Research Unit, Department of Clinical Sciences Malmö, Lund University, Lund, Sweden.
¹⁹ German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany.
²⁰ Department of Psychiatry, University of Geneva, Geneva, Switzerland.
²¹ IRCCS Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy.
²² Dementia Research Centre, Department of Neurodegenerative Disease, University College London, London, United Kingdom.
²³ Robert and Beverly Lewis Center for Neuroimaging, University of Oregon, Eugene, OR, USA.
²⁴ Department of Psychiatry, McGill University, Montreal, Quebec, Canada.
²⁵ Department of Biological and Biomedical Engineering, McGill University, Montreal, Quebec, Canada.
²⁶ Université Normandie, Université de Caen-Normandie, Caen, France.
²⁷ Institut National de la Santé et de la Recherché Médicale (INSERM), UMR-S U1237, Caen, France.
²⁸ GIP Cyceron, Caen, France.
²⁹ Robarts Research Institute, Brain and Mind Institute, University of Western Ontario, London, Ontario, Canada.
³⁰ Allen Institute for Brain Science, Seattle, WA, USA.
³¹ Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The Netherlands.
³² Utrecht University, Utrecht, The Netherlands.
³³ Department of Biomedical Engineering, University of Alberta, Edmonton, Alberta, Canada.
³⁴ Human Neuroanatomy Laboratory, University of Castilla-La Mancha, Albacete, Spain.
³⁵ Center for Mind and Brain, University of California, Davis, CA, USA.
³⁶ Department of Radiology at the University of Michigan, Ann Arbor, MI, USA.
³⁷ Center for Vital Longevity, Behavioral and Brain Science, The University of Texas at Dallas, Dallas, TX, USA.
³⁸ Center for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, Germany.
³⁹ Research Centre for Natural Sciences, Hungarian Academy of Sciences, Budapest, Hungary.
⁴⁰ Department of Psychiatry and Behavioral Sciences, University of California Davis School of Medicine, Davis, CA, USA.
⁴¹ Max Planck - University College London Centre for Computational Psychiatry and Ageing Research, Berlin, Germany and London, United Kingdom.
⁴² Department of Radiology, University of California, San Francisco, CA, USA.
⁴³ Department of Psychology, Florida State University, Tallahassee, FL, USA.
⁴⁴ Neurobiology Department, Weizmann Institute of Science, Rehovot, Israel.
⁴⁵ Department of Psychology, University of British Columbia, Vancouver, British Colombia, Canada.
⁴⁶ Division of Translational Medicine and Genomics, University of Pennsylvania, Philadelphia, PA, USA.
⁴⁷ Institute of Psychology, Goethe University Frankfurt, Frankfurt, Germany.
⁴⁸ Department of Neurobiology and Behavior, Center for Learning and Memory, University of California, Irvine, CA, USA.
⁴⁹ Division of Neurology, Department of Medicine, University of Alberta, Edmonton, Alberta, Canada.
⁵⁰ Department of Psychiatry and Biobehavioral Sciences, Department of Neurosurgery, University of California, Los Angeles, CA, USA.
⁵¹ Department of Psychiatry and Behavioral Sciences and Department Radiology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.
⁵² Department of Radiology, University of Pennsylvania, Philadelphia, PA, USA.
⁵³ Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA.

PMID: 31245529
PMCID: PMC6581847
DOI: 10.1016/j.dadm.2019.04.001

Progress update from the hippocampal subfields group

Rosanna K Olsen et al. Alzheimers Dement (Amst). 2019.

. 2019 Jun 13:11:439-449.

doi: 10.1016/j.dadm.2019.04.001. eCollection 2019 Dec.

Authors

Affiliations

¹ Rotman Research Institute, Baycrest Health Sciences, Toronto, Ontario, Canada.
² Department of Psychology, University of Toronto, Toronto, Ontario, Canada.
³ Department of Psychology, San Jose State University, San Jose, CA, USA.
⁴ Department of Psychology, Wayne State University, Detroit, MI, USA.
⁵ Department of Psychiatry and Behavioral Neurosciences, Wayne State University, Detroit, MI, USA.
⁶ Institute of Gerontology, Wayne State University, Detroit, MI, USA.
⁷ Department of Neurology, Memory and Aging Center, University of California, San Francisco, CA, USA.
⁸ Cerebral Imaging Centre, Douglas Hospital Mental Health University Institute, Verdun, Quebec, Canada.
⁹ C. and O. Vogt Institute for Brain Research, Medical Faculty, University Hospital Düsseldorf, Düsseldorf, Germany.
¹⁰ Heinrich Heine University Düsseldorf, Düsseldorf, Germany.
¹¹ Institute of Neuroscience and Medicine (INM-1), Research Centre Jülich, Jülich, Germany.
¹² Department of Radiology, Harvard Medical School, Charlestown, MA, USA.
¹³ Massachusetts General Hospital, Charlestown, MA, USA.
¹⁴ Department of Psychiatry and Behavioral Sciences, Johns Hopkins University School of Medicine, Baltimore, MD, USA.
¹⁵ Department of Epidemiology and Biostatistics, Michigan State University, East Lansing, MI, USA.
¹⁶ Department of Neurology and Ophthalmology, Michigan State University, East Lansing, MI, USA.
¹⁷ College of Human Medicine, Michigan State University, East Lansing, MI, USA.
¹⁸ Clinical Memory Research Unit, Department of Clinical Sciences Malmö, Lund University, Lund, Sweden.
¹⁹ German Center for Neurodegenerative Diseases (DZNE), Magdeburg, Germany.
²⁰ Department of Psychiatry, University of Geneva, Geneva, Switzerland.
²¹ IRCCS Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy.
²² Dementia Research Centre, Department of Neurodegenerative Disease, University College London, London, United Kingdom.
²³ Robert and Beverly Lewis Center for Neuroimaging, University of Oregon, Eugene, OR, USA.
²⁴ Department of Psychiatry, McGill University, Montreal, Quebec, Canada.
²⁵ Department of Biological and Biomedical Engineering, McGill University, Montreal, Quebec, Canada.
²⁶ Université Normandie, Université de Caen-Normandie, Caen, France.
²⁷ Institut National de la Santé et de la Recherché Médicale (INSERM), UMR-S U1237, Caen, France.
²⁸ GIP Cyceron, Caen, France.
²⁹ Robarts Research Institute, Brain and Mind Institute, University of Western Ontario, London, Ontario, Canada.
³⁰ Allen Institute for Brain Science, Seattle, WA, USA.
³¹ Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The Netherlands.
³² Utrecht University, Utrecht, The Netherlands.
³³ Department of Biomedical Engineering, University of Alberta, Edmonton, Alberta, Canada.
³⁴ Human Neuroanatomy Laboratory, University of Castilla-La Mancha, Albacete, Spain.
³⁵ Center for Mind and Brain, University of California, Davis, CA, USA.
³⁶ Department of Radiology at the University of Michigan, Ann Arbor, MI, USA.
³⁷ Center for Vital Longevity, Behavioral and Brain Science, The University of Texas at Dallas, Dallas, TX, USA.
³⁸ Center for Lifespan Psychology, Max Planck Institute for Human Development, Berlin, Germany.
³⁹ Research Centre for Natural Sciences, Hungarian Academy of Sciences, Budapest, Hungary.
⁴⁰ Department of Psychiatry and Behavioral Sciences, University of California Davis School of Medicine, Davis, CA, USA.
⁴¹ Max Planck - University College London Centre for Computational Psychiatry and Ageing Research, Berlin, Germany and London, United Kingdom.
⁴² Department of Radiology, University of California, San Francisco, CA, USA.
⁴³ Department of Psychology, Florida State University, Tallahassee, FL, USA.
⁴⁴ Neurobiology Department, Weizmann Institute of Science, Rehovot, Israel.
⁴⁵ Department of Psychology, University of British Columbia, Vancouver, British Colombia, Canada.
⁴⁶ Division of Translational Medicine and Genomics, University of Pennsylvania, Philadelphia, PA, USA.
⁴⁷ Institute of Psychology, Goethe University Frankfurt, Frankfurt, Germany.
⁴⁸ Department of Neurobiology and Behavior, Center for Learning and Memory, University of California, Irvine, CA, USA.
⁴⁹ Division of Neurology, Department of Medicine, University of Alberta, Edmonton, Alberta, Canada.
⁵⁰ Department of Psychiatry and Biobehavioral Sciences, Department of Neurosurgery, University of California, Los Angeles, CA, USA.
⁵¹ Department of Psychiatry and Behavioral Sciences and Department Radiology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.
⁵² Department of Radiology, University of Pennsylvania, Philadelphia, PA, USA.
⁵³ Department of Neurology, University of Pennsylvania, Philadelphia, PA, USA.

PMID: 31245529
PMCID: PMC6581847
DOI: 10.1016/j.dadm.2019.04.001

Abstract

Introduction: Heterogeneity of segmentation protocols for medial temporal lobe regions and hippocampal subfields on in vivo magnetic resonance imaging hinders the ability to integrate findings across studies. We aim to develop a harmonized protocol based on expert consensus and histological evidence.

Methods: Our international working group, funded by the EU Joint Programme-Neurodegenerative Disease Research (JPND), is working toward the production of a reliable, validated, harmonized protocol for segmentation of medial temporal lobe regions. The working group uses a novel postmortem data set and online consensus procedures to ensure validity and facilitate adoption.

Results: This progress report describes the initial results and milestones that we have achieved to date, including the development of a draft protocol and results from the initial reliability tests and consensus procedures.

Discussion: A harmonized protocol will enable the standardization of segmentation methods across laboratories interested in medial temporal lobe research worldwide.

Keywords: Cytoarchitecture; Hippocampus; Histology; Human; Neuroanatomy; Neuroimaging; Structural imaging; Volumetry; ex vivo.

PubMed Disclaimer

Figures

**Fig. 1**
(A) Map highlighting the global membership of the HSG. Over 200 members from 18 countries are currently in the HSG. (B) Workflow procedure for the HSG. Abbreviations: HSG, Hippocampal Subfield Group.

**Fig. 2**
(A) Examples of the variability in the position of the CA1, subiculum/prosubiculum boundary (white line) across three different segmentation protocols overlaid on the same brain (adapted from Yushkevich et al., 2015, Fig. 3). This variability is likely due to differences in reference atlases. (B) Histological and MRI slices of the human hippocampal formation depicting the body (upper) and head (lower) regions. Note that the subfield anatomy in the body and head differ in composition and organization relative to macroscopic features. Abbreviations: FD, fascia dentata (dentate gyrus); Ent, entorhinal cortex; JC, La Joie, Chetalat protocol; OAP, Olsen, Amaral, Palombo protocol; PreS, presubiculum; ProS, prosubiculum; Sub, subiculum; WG, Wisse, Geerlings protocol.

**Fig. 3**
The same single histological slice of the hippocampal body stained with Kluver-Barrera stain, segmented by three different neuroanatomists. Abbreviations: DG/FD, dentate gyrus/fascia dentata; ProS, prosubiculum; PreS, presubiculum; PaS/ParaS, parasubiculum; S/Sub, subiculum.

**Fig. 4**
Hippocampal head displaying the uncus in both hemispheres. (A2) Slice showing the disappearance of the uncus in the left hemisphere, and as such, the anterior-most slice of the hippocampal body in the left hemisphere. (B1) Final posterior slice of the hippocampal body displaying the colliculi, the crus fornix, and the “tear drop” shape of the hippocampal body. (B2) Colliculi are no longer visualized, and as such this slice is considered the first slice of the hippocampal tail. (C) Sagittal view, illustrating the anterior and posterior limits of the inclusive hippocampal body range. All images are T2-weighted, resolution 0.39 × 0.39 × 2 mm. (D) Screenshot from the online questionnaire used to reach consensus on the outer boundaries of the hippocampal body.

See this image and copyright information in PMC

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Progress update from the hippocampal subfields group

Affiliations

Progress update from the hippocampal subfields group

Authors

Affiliations

Abstract

Figures

References

Grants and funding

LinkOut - more resources

Full Text Sources