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Brain scans from 21297 individuals reveal the genetic architecture of hippocampal subfield volumes

Dennis van der Meer, Jaroslav Rokicki, Tobias Kaufmann, Aldo Córdova-Palomera, Torgeir Moberget, Dag Alnæs, Francesco Bettella, Oleksandr Frei, Nhat Trung Doan, Ingrid Agartz, Alessandro Bertolino, Janita Bralten, Christine L. Brandt, Jan K. Buitelaar, Srdjan Djurovic, Marjolein van Donkelaar, Erlend S. Dørum, Thomas Espeseth, Stephen V. Faraone, Guillén Fernández, Simon E. Fisher D.Phil., Barbara Franke, Beathe Haatveit, Catharina A. Hartman, Pieter J. Hoekstra, Asta K. Håberg, Erik G. Jönsson, Knut K. Kolskår, Cand. Psychol., Stephanie Le Hellard, Martina J. Lund, Astri J. Lundervold, Arvid Lundervold, Ingrid Melle, Jennifer Monereo Sánchez, Linn C. Norbom, Jan E. Nordvik, Lars Nyberg, Jaap Oosterlaan, Marco Papalino, Andreas Papassotiropoulos, Giulio Pergola, Dominique J.F. de Quervain, Geneviève Richard, Anne-Marthe Sanders, Pierluigi Selvaggi, Elena Shumskaya, Vidar M. Steen, Siren Tønnesen, Kristine M. Ulrichsen Cand.Psychol., Marcel P. Zwiers, Ole A. Andreassen Lars, Lars T. Westlye
doi: https://doi.org/10.1101/299578
Dennis van der Meer
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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  • For correspondence: d.v.d.meer@medisin.uio.no
Jaroslav Rokicki
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
2Department of Psychology, University of Oslo, Norway
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Tobias Kaufmann
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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Aldo Córdova-Palomera
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
3Department of Pediatrics, Stanford University School of Medicine, Stanford University, Stanford, USA
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Torgeir Moberget
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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Dag Alnæs
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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Francesco Bettella
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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Oleksandr Frei
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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Nhat Trung Doan
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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Ingrid Agartz
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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Alessandro Bertolino
4Department of Basic Medical Sciences, Neuroscience and Sense Organs, University of Bari Aldo Moro, Bari, Italy
5Azienda Ospedaliero-Universitaria Consorziale Policlinico, Bari, Italy
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Janita Bralten
6Department of Human Genetics, Radboud University Medical Center, Nijmegen, The Netherlands
7Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
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Christine L. Brandt
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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Jan K. Buitelaar
7Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
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Srdjan Djurovic
8Department of Medical Genetics, Oslo University Hospital, Oslo, Norway
9NORMENT, KG Jebsen Centre for Psychosis Research, Department of Clinical Science, University of Bergen, Bergen, Norway
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Marjolein van Donkelaar
6Department of Human Genetics, Radboud University Medical Center, Nijmegen, The Netherlands
7Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
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Erlend S. Dørum
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
2Department of Psychology, University of Oslo, Norway
10Sunnaas Rehabilitation Hospital HT, Nesodden, Norway
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Thomas Espeseth
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
2Department of Psychology, University of Oslo, Norway
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Stephen V. Faraone
11Departments of Psychiatry and of Neuroscience and Physiology, SUNY Upstate Medical University, Syracuse, NY, USA
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Guillén Fernández
7Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
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Simon E. Fisher D.Phil.
7Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
12Language and Genetics Department, Max Planck Institute for Psycholinguistics, Nijmegen, the Netherlands.
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Barbara Franke
6Department of Human Genetics, Radboud University Medical Center, Nijmegen, The Netherlands
7Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
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Beathe Haatveit
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
2Department of Psychology, University of Oslo, Norway
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Catharina A. Hartman
13University of Groningen, University Medical Center Groningen, Interdisciplinary Center Psychopathology and Emotion regulation, Groningen, The Netherlands
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Pieter J. Hoekstra
14University of Groningen, University Medical Center Groningen, Department of Child and Adolescent Psychiatry, Groningen, Netherlands
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Asta K. Håberg
15Department of Neuromedicine and Movement Science, NTNU – Norwegian University of Science and Technology, Trondheim, Norway
16Department of Radiology and Nuclear Medicine, St. Olavs Hospital, Trondheim, Norway
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Erik G. Jönsson
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
17Centre for Psychiatric Research, Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden
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Knut K. Kolskår
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
2Department of Psychology, University of Oslo, Norway
10Sunnaas Rehabilitation Hospital HT, Nesodden, Norway
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Stephanie Le Hellard
9NORMENT, KG Jebsen Centre for Psychosis Research, Department of Clinical Science, University of Bergen, Bergen, Norway
18Dr. Einar Martens Research Group for Biological Psychiatry, Center for Medical Genetics and Molecular Medicine, Haukeland University Hospital, Bergen, Norway
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Martina J. Lund
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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Astri J. Lundervold
19Department of Biological and Medical Psychology, University of Bergen, Norway
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Arvid Lundervold
20Department of Biomedicine, University of Bergen, Bergen, Norway
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Ingrid Melle
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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Jennifer Monereo Sánchez
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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Linn C. Norbom
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
2Department of Psychology, University of Oslo, Norway
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Jan E. Nordvik
10Sunnaas Rehabilitation Hospital HT, Nesodden, Norway
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Lars Nyberg
21Departments of Radiation Sciences and Integrative Medical Biology, Umeå Center for Functional Brain Imaging (UFB), Umeå University, Sweden
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Jaap Oosterlaan
22Emma Children’s Hospital Amsterdam Medical Center, Amsterdam, The Netherlands
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Marco Papalino
4Department of Basic Medical Sciences, Neuroscience and Sense Organs, University of Bari Aldo Moro, Bari, Italy
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Andreas Papassotiropoulos
23Division of Molecular Neuroscience, Department of Psychology, University of Basel, Basel, Switzerland
24Transfaculty Research Platform Molecular and Cognitive Neurosciences, University of Basel, Basel, Switzerland
25Department Biozentrum, Life Sciences Training Facility, University of Basel, Basel, Switzerland
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Giulio Pergola
4Department of Basic Medical Sciences, Neuroscience and Sense Organs, University of Bari Aldo Moro, Bari, Italy
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Dominique J.F. de Quervain
26Division of Cognitive Neuroscience, Department of Psychology, University of Basel, Basel, Switzerland
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Geneviève Richard
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
2Department of Psychology, University of Oslo, Norway
10Sunnaas Rehabilitation Hospital HT, Nesodden, Norway
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Anne-Marthe Sanders
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
2Department of Psychology, University of Oslo, Norway
10Sunnaas Rehabilitation Hospital HT, Nesodden, Norway
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Pierluigi Selvaggi
4Department of Basic Medical Sciences, Neuroscience and Sense Organs, University of Bari Aldo Moro, Bari, Italy
27Department of Neuroimaging, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, UK
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Elena Shumskaya
6Department of Human Genetics, Radboud University Medical Center, Nijmegen, The Netherlands
7Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
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Vidar M. Steen
9NORMENT, KG Jebsen Centre for Psychosis Research, Department of Clinical Science, University of Bergen, Bergen, Norway
18Dr. Einar Martens Research Group for Biological Psychiatry, Center for Medical Genetics and Molecular Medicine, Haukeland University Hospital, Bergen, Norway
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Siren Tønnesen
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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Kristine M. Ulrichsen Cand.Psychol.
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
2Department of Psychology, University of Oslo, Norway
10Sunnaas Rehabilitation Hospital HT, Nesodden, Norway
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Marcel P. Zwiers
7Donders Institute for Brain, Cognition and Behaviour, Radboud University, Nijmegen, The Netherlands
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Ole A. Andreassen Lars
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
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Lars T. Westlye
1NORMENT, KG Jebsen Centre for Psychosis Research, Division of Mental Health and Addiction, Oslo University Hospital & Institute of Clinical Medicine, University of Oslo, Oslo, Norway
2Department of Psychology, University of Oslo, Norway
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ABSTRACT

The hippocampus is a heterogeneous structure, comprising histologically distinguishable subfields. These subfields are differentially involved in memory consolidation, spatial navigation and pattern separation, complex functions often impaired in individuals with brain disorders characterized by reduced hippocampal volume, including Alzheimer’s disease (AD) and schizophrenia. Given the structural and functional heterogeneity of the hippocampal formation, we sought to characterize the subfields’ genetic architecture. T1-weighted brain scans (n=21297, 16 cohorts) were processed with the hippocampal subfields algorithm in FreeSurfer v6.0. We ran a genome-wide association analysis on each subfield, covarying for total hippocampal volume. We further calculated the single nucleotide polymorphism (SNP)-based heritability of twelve subfields, as well as their genetic correlation with each other, with other structural brain features, and with AD and schizophrenia. All outcome measures were corrected for age, sex, and intracranial volume. We found 15 unique genome-wide significant loci across six subfields, of which eight had not been previously linked to the hippocampus. Top SNPs were mapped to genes associated with neuronal differentiation, locomotor behaviour, schizophrenia and AD. The volumes of all the subfields were estimated to be heritable (h2 from .14 to .27, all p< 1×10-16) and clustered together based on their genetic correlations compared to other structural brain features. There was also evidence of genetic overlap of subicular subfield volumes with schizophrenia. We conclude that hippocampal subfields have partly distinct genetic determinants associated with specific biological processes and traits. Taking into account this specificity may increase our understanding of hippocampal neurobiology and associated pathologies.

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Brain scans from 21297 individuals reveal the genetic architecture of hippocampal subfield volumes
Dennis van der Meer, Jaroslav Rokicki, Tobias Kaufmann, Aldo Córdova-Palomera, Torgeir Moberget, Dag Alnæs, Francesco Bettella, Oleksandr Frei, Nhat Trung Doan, Ingrid Agartz, Alessandro Bertolino, Janita Bralten, Christine L. Brandt, Jan K. Buitelaar, Srdjan Djurovic, Marjolein van Donkelaar, Erlend S. Dørum, Thomas Espeseth, Stephen V. Faraone, Guillén Fernández, Simon E. Fisher D.Phil., Barbara Franke, Beathe Haatveit, Catharina A. Hartman, Pieter J. Hoekstra, Asta K. Håberg, Erik G. Jönsson, Knut K. Kolskår, Cand. Psychol., Stephanie Le Hellard, Martina J. Lund, Astri J. Lundervold, Arvid Lundervold, Ingrid Melle, Jennifer Monereo Sánchez, Linn C. Norbom, Jan E. Nordvik, Lars Nyberg, Jaap Oosterlaan, Marco Papalino, Andreas Papassotiropoulos, Giulio Pergola, Dominique J.F. de Quervain, Geneviève Richard, Anne-Marthe Sanders, Pierluigi Selvaggi, Elena Shumskaya, Vidar M. Steen, Siren Tønnesen, Kristine M. Ulrichsen Cand.Psychol., Marcel P. Zwiers, Ole A. Andreassen Lars, Lars T. Westlye
bioRxiv 299578; doi: https://doi.org/10.1101/299578
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Brain scans from 21297 individuals reveal the genetic architecture of hippocampal subfield volumes
Dennis van der Meer, Jaroslav Rokicki, Tobias Kaufmann, Aldo Córdova-Palomera, Torgeir Moberget, Dag Alnæs, Francesco Bettella, Oleksandr Frei, Nhat Trung Doan, Ingrid Agartz, Alessandro Bertolino, Janita Bralten, Christine L. Brandt, Jan K. Buitelaar, Srdjan Djurovic, Marjolein van Donkelaar, Erlend S. Dørum, Thomas Espeseth, Stephen V. Faraone, Guillén Fernández, Simon E. Fisher D.Phil., Barbara Franke, Beathe Haatveit, Catharina A. Hartman, Pieter J. Hoekstra, Asta K. Håberg, Erik G. Jönsson, Knut K. Kolskår, Cand. Psychol., Stephanie Le Hellard, Martina J. Lund, Astri J. Lundervold, Arvid Lundervold, Ingrid Melle, Jennifer Monereo Sánchez, Linn C. Norbom, Jan E. Nordvik, Lars Nyberg, Jaap Oosterlaan, Marco Papalino, Andreas Papassotiropoulos, Giulio Pergola, Dominique J.F. de Quervain, Geneviève Richard, Anne-Marthe Sanders, Pierluigi Selvaggi, Elena Shumskaya, Vidar M. Steen, Siren Tønnesen, Kristine M. Ulrichsen Cand.Psychol., Marcel P. Zwiers, Ole A. Andreassen Lars, Lars T. Westlye
bioRxiv 299578; doi: https://doi.org/10.1101/299578

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