NeuroResource
An Open Resource for Non-human Primate Imaging Highlights d
Openly shared, large non-human primate neuroimaging data resource
d
Multiple imaging modalities contributed from investigators around the world
d
Quality assessments of the dataset
Authors Michael P. Milham, Lei Ai, Bonhwang Koo, ..., Yong-di Zhou, Daniel S. Margulies, Charles E. Schroeder
Correspondence
[email protected]
d
Discussed pitfalls and challenges in analyzing the non-human primate MRI data
In Brief The PRIMatE Data Exchange (PRIME-DE) consortium is an open science resource for the neuroimaging community aiming to facilitate efforts to map the non-human primate connectome. It aggregates and shares anatomical, functional, and diffusion MRI datasets from laboratories throughout the world.
Milham et al., 2018, Neuron 100, 61–74 October 10, 2018 ª 2018 The Authors. Published by Elsevier Inc. https://doi.org/10.1016/j.neuron.2018.08.039
Neuron
NeuroResource An Open Resource for Non-human Primate Imaging Michael P. Milham,1,2,51,* Lei Ai,1 Bonhwang Koo,1 Ting Xu,1 Ce´line Amiez,3 Fabien Balezeau,4 Mark G. Baxter,5 Erwin L.A. Blezer,47 Thomas Brochier,7 Aihua Chen,8 Paula L. Croxson,5 Christienne G. Damatac,9 Stanislas Dehaene,10 Stefan Everling,11 Damian A. Fair,12 Lazar Fleysher,13 Winrich Freiwald,14 Sean Froudist-Walsh,15 Timothy D. Griffiths,4 Carole Guedj,16 Fadila Hadj-Bouziane,16 Suliann Ben Hamed,6 Noam Harel,17 Bassem Hiba,6 Bechir Jarraya,10 Benjamin Jung,18 Sabine Kastner,19 P. Christiaan Klink,20,21 Sze Chai Kwok,22,23,24 Kevin N. Laland,50 David A. Leopold,25,26 Patrik Lindenfors,48,49 Rogier B. Mars,9,27 Ravi S. Menon,11 Adam Messinger,18 Martine Meunier,16 Kelvin Mok,28 John H. Morrison,29,30 Jennifer Nacef,4 Jamie Nagy,5 Michael Ortiz Rios,4 Christopher I. Petkov,4 Mark Pinsk,19 Colline Poirier,4 Emmanuel Procyk,3 Reza Rajimehr,31 Simon M. Reader,32,33 Pieter R. Roelfsema,20,21,34 (Author list continued on next page) 1Center
for the Developing Brain, Child Mind Institute, New York, NY 10022, USA for Biomedical Imaging and Neuromodulation, Nathan S. Kline Institute for Psychiatric Research, Orangeburg, NY 10962, USA 3University of Lyon, Universite ´ Claude Bernard Lyon 1, INSERM, Stem Cell and Brain Research Institute U1208, Lyon, France 4Institute of Neuroscience, Newcastle University, Newcastle upon Tyne NE1 7RU, UK 5Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA 6Institut des Sciences Cognitives – Marc Jeannerod, UMR5229, CNRS-Universite ´ de Lyon, Lyon, France 7Institut de Neurosciences de la Timone, CNRS & Aix-Marseille Universite ´ , UMR 7289, Marseille, France 8Key Laboratory of Brain Functional Genomics (Ministry of Education & Science and Technology Commission of Shanghai Municipality), School of Life Sciences, East China Normal University, Shanghai 200062, China 9Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN Nijmegen, Netherlands 10NeuroSpin, CEA, INSERM U992, Universite ´ Paris-Saclay, 91191 Gif-sur-Yvette, France 11Centre for Functional and Metabolic Mapping, The University of Western Ontario, London, ON N6A 3K7, Canada 12Department of Behavior Neuroscience, Department of Psychiatry, Advanced Imaging Research Center, Oregon Health and Science University, Portland, OR, USA 13Department of Radiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA 14Laboratory of Neural Systems, The Rockefeller University, New York, NY, USA 15Center for Neural Science, New York University, New York, NY 10023, USA 16INSERM, U1028, CNRS UMR5292, Lyon Neuroscience Research Center, Lyon, France 17Center for Magnetic Resonance Research, University of Minnesota Medical School, Minneapolis, MN 55455, USA 18Laboratory of Brain and Cognition, National Institute of Mental Health, Bethesda, MD 20892, USA 19Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08540, USA 20Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, 1105 BA Amsterdam, the Netherlands 21Department of Psychiatry, Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, the Netherlands 2Center
(Affiliations continued on next page)
SUMMARY
Non-human primate neuroimaging is a rapidly growing area of research that promises to transform and scale translational and cross-species comparative neuroscience. Unfortunately, the technological and methodological advances of the past two decades have outpaced the accrual of data, which is particularly challenging given the relatively few centers that have the necessary facilities and capabilities. The PRIMatE Data Exchange (PRIME-DE) addresses this challenge by aggregating independently acquired non-human primate magnetic resonance imaging (MRI) datasets and openly sharing them via the International Neuroimaging Data-sharing Initiative (INDI). Here, we present the rationale, design, and procedures for the PRIMEDE consortium, as well as the initial release, consisting of 25 independent data collections aggregated across 22 sites (total = 217 non-human primates). We also outline the unique pitfalls and challenges that
should be considered in the analysis of non-human primate MRI datasets, including providing automated quality assessment of the contributed datasets.
INTRODUCTION Translational, comparative neuroscience research enables a bridging of knowledge gaps across species as well as invasive and noninvasive approaches. A growing body of research has documented the utility of magnetic resonance imaging (MRI) technologies to support in vivo examination of brain organization and function in non-human primates (Vanduffel et al., 2014; Rilling, 2014; Van Essen and Glasser, 2014; Zhang et al., 2013; Shmuel and Leopold, 2008; Schwiedrzik et al., 2015). Recent work has demonstrated the ability to recapitulate findings from gold-standard invasive methodologies (Ghahremani et al., 2017; Donahue et al., 2016; Grayson et al., 2016). This work also provides novel insights into the organizational principles of the nonhuman primate (NHP) connectome (Goulas et al., 2017; Hutchison and Everling, 2014; Hutchison et al., 2011; Vincent et al., 2007)
Neuron 100, 61–74, October 10, 2018 ª 2018 The Authors. Published by Elsevier Inc. 61 This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
David A. Rudko,28 Matthew F.S. Rushworth,27,35 Brian E. Russ,25 Jerome Sallet,35 Michael Christoph Schmid,4 Caspar M. Schwiedrzik,14 Jakob Seidlitz,36,37 Julien Sein,7 Amir Shmuel,28 Elinor L. Sullivan,38,39 Leslie Ungerleider,18 Alexander Thiele,4 Orlin S. Todorov,32 Doris Tsao,40 Zheng Wang,41 Charles R.E. Wilson,3 Essa Yacoub,17 Frank Q. Ye,26 Wilbert Zarco,14 Yong-di Zhou,42 Daniel S. Margulies,43,44 and Charles E. Schroeder2,45,46 22Shanghai
Key Laboratory of Brain Functional Genomics, School of Psychology and Cognitive Science, Key Laboratory of Brain Functional Genomics (Ministry of Education), East China Normal University, Shanghai 200062, China 23Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, Shanghai 200062, China 24NYU-ECNU Institute of Brain and Cognitive Science at NYU Shanghai, Shanghai 200062, China 25Section on Cognitive Neurophysiology and Imaging, National Institute of Mental Health, Bethesda, MD 20892, USA 26Neurophysiology Imaging Facility, National Institute of Mental Health, National Institute of Neurological Disorders and Stroke, National Eye Institute, Bethesda, MD 20892, USA 27Wellcome Centre for Integrative Neuroimaging, Centre for Functional MRI of the Brain (FMRIB), Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, University of Oxford, Oxford OX3 9DU, UK 28McConnell Brain Imaging Centre, Montreal Neurological Institute, Departments of Neurology, Neurosurgery, and Biomedical Engineering, McGill University, Montreal, QC H3A 0G4, Canada 29California National Primate Research Center, Davis, CA 95616, USA 30Department of Neurology, School of Medicine, University of California, Davis, CA 95616, USA 31McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA 02139, USA 32Department of Biology and Helmholtz Institute, Utrecht University, 35 84 CH Utrecht, The Netherlands 33Department of Biology, McGill University, Montreal, QC H3A 1BA, Canada 34Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, Vrije Universiteit, 1081 HV Amsterdam, the Netherlands 35Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, Oxford OX1 3AQ, UK 36Developmental Neurogenomics Unit, National Institute of Mental Health, Bethesda, MD 20892, USA 37Brain Mapping Unit, Department of Psychiatry, University of Cambridge, Cambridge CB2 0SZ, UK 38Divisions of Neuroscience and Cardiometabolic Health, Oregon National Primate Research Center, Beaverton, OR, USA 39Department of Human Physiology, University of Oregon, Eugene, OR, USA 40Department of Computation and Neural Systems, California Institute of Technology, Pasadena, CA 91125, USA 41Institute of Neuroscience, Key Laboratory of Primate Neurobiology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China 42Krieger Mind/Brain Institute, Department of Neurosurgery, Johns Hopkins University, Baltimore, MD 21287, USA 43Max Planck Research Group for Neuroanatomy and Connectivity, Max Planck Institute for Human Cognitive and Brain Sciences, 04103 Leipzig, Germany 44Centre national de la recherche scientifique, CNRS UMR 7225, Institut du Cerveau et de la Moelle e ´ pinie`re, 75013 Paris, France 45Department of Neurological Surgery, Columbia University College of Physicians and Surgeons, New York, NY 10032, USA 46Department of Psychiatry, Columbia University College of Physicians and Surgeons, New York, NY 10032, USA 47Biomedical MR Imaging and Spectroscopy Group, Center for Image Sciences, University Medical Center Utrecht, Utrecht, The Netherlands 48Institute for Future Studies, Stockholm, Sweden 49Centre for Cultural Evolution & Department of Zoology, Stockholm University, Stockholm, Sweden 50Centre for Social Learning and Cognitive Evolution, School of Biology, University of St. Andrews, St. Andrews, UK 51Lead Contact *Correspondence:
[email protected] https://doi.org/10.1016/j.neuron.2018.08.039
and cross-species comparative connectomics (Hutchison et al., 2012, 2015; Miranda-Dominguez et al., 2014; Mars et al., 2011; Seidlitz et al., 2018a), which are possible only through in vivo studies. These advances are timely given the growing prominence of large-scale national and international initiatives focused on advancing our understanding of human brain organization and the ability to generate novel therapeutics for neurology and psychiatry (Bargmann and Newsome, 2014). Despite the clear demonstrations of feasibility and utility, the field of non-human primate neuroimaging is still developing. Numerous unique challenges related to the acquisition and processing of nonhuman primate data are still being addressed (e.g., Seidlitz et al., 2018b; Hutchison and Everling, 2012), and the potential for broad reaching cross-species studies remains unexploited. Perhaps most challenging is the limited availability of data. Here, we introduce the PRIMatE Data Exchange (PRIME-DE) to create an open science resource for the neuroimaging community
62 Neuron 100, 61–74, October 10, 2018
that will facilitate the mapping of the non-human primate connectome. To accomplish this, we aggregate a combination of anatomical, functional, and diffusion MRI datasets from laboratories throughout the world and make these data available to the scientific community. It merits emphasis that PRIME-DE supports an ongoing process that will remain open to new contributions of data from macaques and other non-human primate species. RESULTS Overview At present, PRIME-DE contains 25 collections aggregated across 22 sites; to date, data from 217 primates are included (see Table 1 for information on each institution). Contributions will continue to be accepted and shared on a rolling basis. To promote usage of a standardized data format, we organized all data using the Brain Imaging Data Structure (BIDS) format
Table 1. Experimental Design Investigators
Speciesa
Subjects
State
Contrast Agent
Structural T1
Structural T2
Resting State fMRI
Naturalistic Viewing fMRI
Task fMRI
Field map
Diffusion MRI
AMU
Belin, Brochier, Sein
MM
4
Anesthetized
No
✔
✔
–
–
–
–
✔
Caltech
Rajimehr, Tsao
MM
2
Awake
Yes
–
–
–
96 min
–
–
–
ECNU (C)
Aihua Chen
MM
10
Anesthetized
No
✔
–
–
–
–
–
–
ECNU (K)b
Kwok, Zhou
MM
4
Anesthetized
No
✔
✔
8 min
–
–
–
✔
Institute of Neuroscience (IoN)
Wang
MM, MF
8
Anesthetized
No
✔
–
20–40 min
–
–
✔
–
Institut des Sciences Cognitives Marc Jeannerod
Ben Hamed, Hiba
MM
8
Anesthetized/ Awake
Yes
✔
–
✔
–
✔
–
✔
Lyon Neuroscience Research Center
Hadj-Bouziane, Meunier, Guedj
MM
1
Anesthetized/ Awake
Yes/No
✔
✔
13 min
–
–
–
–
McGill University
Mok, Rudko, Shmuel
MM, MF
3
Anesthetized
No
✔
✔
–
–
–
–
–
Mount Sinai (P)
Croxson, Fleysher
MM, MF
9
Anesthetized
No
✔
✔
43 min
–
–
✔
✔
Mount Sinai (S)
Croxson, Fleysher, Froudist-Walsh, Damatac, Nagy
MM
5
Anesthetized
No
✔
✔
–
–
–
–
✔
NKI
Schroeder, Milham
MM
2
Anesthetized/ Awake
Yes/No
✔
76–155 min
55–345 min
–
–
–
NIMH (L)c
Leopold, Russ
MM
3
Awake
Yes
✔
✔
30–150 min
170 min
–
–
–
NIMH (M)c,d
Messinger, Jung, Seidlitz, Ungerleider
MM
3
Anesthetized/ Awake
Yes
✔
–
1015 min
–
–
–
–
Netherlands Institute for Neuroscience (NIN)
Klink, Roelfsema
MM
2
Anesthetized
No
✔
✔
9.7 min
–
–
–
–
Neuron 100, 61–74, October 10, 2018 63
NeuroSpin
Jarraya, Dehaene
MM
3
Anesthetized
Yes/No
✔
–
✔
–
–
–
–
Newcastle
Petkov, Nacef, Thiele, Poirier, Balezeau, Griffiths, Schmid, Rios
MM
14
Anesthetized/ Awake
No
✔
✔
21.6 min
–
–
–
–
OHSU
Sullivan, Fair
MM
2
Anesthetized
Yes/No
✔
✔
480 min
–
–
–
–
Princeton
Kastner, Pinsk
MM
2
Anesthetized
✔
✔
–
–
–
✔
✔
Rockefeller
Schwiedrzik, Freiwald, Zarco
MM, MF
6
Anesthetized
✔
–
80 min
–
–
✔
SBRI
Procyk, Wilson, Amiez
MM, MF
22
Anesthetized
No
✔
✔
✔
–
–
–
–
UC Davis
Baxter, Croxson, Morrison
MM
19
Anesthetized
No
✔
✔
13.5 min
–
–
✔
✔
Univ. of Minnesota (UMN)
Yacoub, Harel
M
2
Anesthetized
–
✔
–
27 min
–
–
✔
✔
Yes
(Continued on next page)
Navarrete, Blezer, Todorov, Lindenfors, Laland, Reader
Everling, Menon
NIN Primate Brain Bank/Utrecht University
Univ. of Western Ontario (UWO)
General information about PRIME-DE data collections contributed prior to the time of publication. For usage agreement, CC-BY-NC-SA: Creative Commons – Attribution-NonCommercial Share Alike, Standard INDI data sharing policy, prohibits use of the data for commercial purposes; DUA: Data Usage Agreement, users must complete a DUA prior to gaining access to the data. For species information, MM: Macaca mulatta; MF: Macaca fascicularis; M: Macaca. a Detailed species information is available on the PRIME-DE site and in Navarrete et al., 2018 b ECNU (K) provided magnetic resonance spectroscopy c The usage agreement is DUA for those sites, CC-BY-NC-SA for all other sites d NIMH (M) provided cortical thickness and brain template
– – ✔ No Anesthetized
Sallet, Mars, Rushworth Univ. of Oxfordc
MM
12
✔
60 min
–
–
–
–
–
– –
– –
– – ✔
–
– ✔ No
Yes/No
Anesthetized 20
51
MM
Multiplea
Post-mortem
53.43 min
Diffusion MRI Field map Task fMRI Naturalistic Viewing fMRI Resting State fMRI Structural T2 Structural T1 Contrast Agent State Subjects Speciesa Investigators Continued Table 1.
64 Neuron 100, 61–74, October 10, 2018
(Gorgolewski et al., 2017). All PRIME-DE datasets can be accessed through the PRIME-DE site (http://fcon_1000.projects. nitrc.org/indi/indiPRIME.html). Prior to downloading the data, users are required to establish a user account on NITRC and register with the International Neuroimaging Data-sharing Initiative (INDI; anticipated time:
