An Open Resource for Non-human Primate Imaging

Michael P Milham¹, Lei Ai², Bonhwang Koo², Ting Xu², Céline Amiez³, Fabien Balezeau⁴, Mark G Baxter⁵, Erwin L A Blezer⁶, Thomas Brochier⁷, Aihua Chen⁸, Paula L Croxson⁵, Christienne G Damatac⁹, Stanislas Dehaene¹⁰, Stefan Everling¹¹, Damian A Fair¹², Lazar Fleysher¹³, Winrich Freiwald¹⁴, Sean Froudist-Walsh¹⁵, Timothy D Griffiths⁴, Carole Guedj¹⁶, Fadila Hadj-Bouziane¹⁶, Suliann Ben Hamed¹⁷, Noam Harel¹⁸, Bassem Hiba¹⁷, Bechir Jarraya¹⁰, Benjamin Jung¹⁹, Sabine Kastner²⁰, P Christiaan Klink²¹, Sze Chai Kwok²², Kevin N Laland²³, David A Leopold²⁴, Patrik Lindenfors²⁵, Rogier B Mars²⁶, Ravi S Menon¹¹, Adam Messinger¹⁹, Martine Meunier¹⁶, Kelvin Mok²⁷, John H Morrison²⁸, Jennifer Nacef⁴, Jamie Nagy⁵, Michael Ortiz Rios⁴, Christopher I Petkov⁴, Mark Pinsk²⁰, Colline Poirier⁴, Emmanuel Procyk³, Reza Rajimehr²⁹, Simon M Reader³⁰, Pieter R Roelfsema³¹, David A Rudko²⁷, Matthew F S Rushworth³², Brian E Russ³³, Jerome Sallet³⁴, Michael Christoph Schmid⁴, Caspar M Schwiedrzik¹⁴, Jakob Seidlitz³⁵, Julien Sein⁷, Amir Shmuel²⁷, Elinor L Sullivan³⁶, Leslie Ungerleider¹⁹, Alexander Thiele⁴, Orlin S Todorov³⁷, Doris Tsao³⁸, Zheng Wang³⁹, Charles R E Wilson³, Essa Yacoub¹⁸, Frank Q Ye⁴⁰, Wilbert Zarco¹⁴, Yong-di Zhou⁴¹, Daniel S Margulies⁴², Charles E Schroeder⁴³

Affiliations

¹ Center for the Developing Brain, Child Mind Institute, New York, NY 10022, USA; Center for Biomedical Imaging and Neuromodulation, Nathan S. Kline Institute for Psychiatric Research, Orangeburg, NY 10962, USA. Electronic address: michael.milham@childmind.org.
² Center for the Developing Brain, Child Mind Institute, New York, NY 10022, USA.
³ University of Lyon, Université Claude Bernard Lyon 1, INSERM, Stem Cell and Brain Research Institute U1208, Lyon, France.
⁴ Institute of Neuroscience, Newcastle University, Newcastle upon Tyne NE1 7RU, UK.
⁵ Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
⁶ Biomedical MR Imaging and Spectroscopy Group, Center for Image Sciences, University Medical Center Utrecht, Utrecht, The Netherlands.
⁷ Institut de Neurosciences de la Timone, CNRS & Aix-Marseille Université, UMR 7289, Marseille, France.
⁸ Key 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.
⁹ Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN Nijmegen, Netherlands.
¹⁰ NeuroSpin, CEA, INSERM U992, Université Paris-Saclay, 91191 Gif-sur-Yvette, France.
¹¹ Centre for Functional and Metabolic Mapping, The University of Western Ontario, London, ON N6A 3K7, Canada.
¹² Department of Behavior Neuroscience, Department of Psychiatry, Advanced Imaging Research Center, Oregon Health and Science University, Portland, OR, USA.
¹³ Department of Radiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
¹⁴ Laboratory of Neural Systems, The Rockefeller University, New York, NY, USA.
¹⁵ Center for Neural Science, New York University, New York, NY 10023, USA.
¹⁶ INSERM, U1028, CNRS UMR5292, Lyon Neuroscience Research Center, Lyon, France.
¹⁷ Institut des Sciences Cognitives - Marc Jeannerod, UMR5229, CNRS-Université de Lyon, Lyon, France.
¹⁸ Center for Magnetic Resonance Research, University of Minnesota Medical School, Minneapolis, MN 55455, USA.
¹⁹ Laboratory of Brain and Cognition, National Institute of Mental Health, Bethesda, MD 20892, USA.
²⁰ Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08540, USA.
²¹ Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, 1105 BA Amsterdam, the Netherlands; Department of Psychiatry, Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, the Netherlands.
²² Shanghai 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; Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, Shanghai 200062, China; NYU-ECNU Institute of Brain and Cognitive Science at NYU Shanghai, Shanghai 200062, China.
²³ Centre for Social Learning and Cognitive Evolution, School of Biology, University of St. Andrews, St. Andrews, UK.
²⁴ Section on Cognitive Neurophysiology and Imaging, National Institute of Mental Health, Bethesda, MD 20892, USA; Neurophysiology Imaging Facility, National Institute of Mental Health, National Institute of Neurological Disorders and Stroke, National Eye Institute, Bethesda, MD 20892, USA.
²⁵ Institute for Future Studies, Stockholm, Sweden; Centre for Cultural Evolution & Department of Zoology, Stockholm University, Stockholm, Sweden.
²⁶ Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN Nijmegen, Netherlands; Wellcome 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.
²⁷ McConnell Brain Imaging Centre, Montreal Neurological Institute, Departments of Neurology, Neurosurgery, and Biomedical Engineering, McGill University, Montreal, QC H3A 0G4, Canada.
²⁸ California National Primate Research Center, Davis, CA 95616, USA; Department of Neurology, School of Medicine, University of California, Davis, CA 95616, USA.
²⁹ McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
³⁰ Department of Biology and Helmholtz Institute, Utrecht University, 35 84 CH Utrecht, The Netherlands; Department of Biology, McGill University, Montreal, QC H3A 1BA, Canada.
³¹ Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, 1105 BA Amsterdam, the Netherlands; Department of Psychiatry, Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, the Netherlands; Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, Vrije Universiteit, 1081 HV Amsterdam, the Netherlands.
³² Wellcome 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; Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, Oxford OX1 3AQ, UK.
³³ Section on Cognitive Neurophysiology and Imaging, National Institute of Mental Health, Bethesda, MD 20892, USA.
³⁴ Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, Oxford OX1 3AQ, UK.
³⁵ Developmental Neurogenomics Unit, National Institute of Mental Health, Bethesda, MD 20892, USA; Brain Mapping Unit, Department of Psychiatry, University of Cambridge, Cambridge CB2 0SZ, UK.
³⁶ Divisions of Neuroscience and Cardiometabolic Health, Oregon National Primate Research Center, Beaverton, OR, USA; Department of Human Physiology, University of Oregon, Eugene, OR, USA.
³⁷ Department of Biology and Helmholtz Institute, Utrecht University, 35 84 CH Utrecht, The Netherlands.
³⁸ Department of Computation and Neural Systems, California Institute of Technology, Pasadena, CA 91125, USA.
³⁹ Institute of Neuroscience, Key Laboratory of Primate Neurobiology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China.
⁴⁰ Neurophysiology Imaging Facility, National Institute of Mental Health, National Institute of Neurological Disorders and Stroke, National Eye Institute, Bethesda, MD 20892, USA.
⁴¹ Krieger Mind/Brain Institute, Department of Neurosurgery, Johns Hopkins University, Baltimore, MD 21287, USA.
⁴² Max Planck Research Group for Neuroanatomy and Connectivity, Max Planck Institute for Human Cognitive and Brain Sciences, 04103 Leipzig, Germany; Centre national de la recherche scientifique, CNRS UMR 7225, Institut du Cerveau et de la Moelle épinière, 75013 Paris, France.
⁴³ Center for Biomedical Imaging and Neuromodulation, Nathan S. Kline Institute for Psychiatric Research, Orangeburg, NY 10962, USA; Department of Neurological Surgery, Columbia University College of Physicians and Surgeons, New York, NY 10032, USA; Department of Psychiatry, Columbia University College of Physicians and Surgeons, New York, NY 10032, USA.

PMID: 30269990
PMCID: PMC6231397
DOI: 10.1016/j.neuron.2018.08.039

An Open Resource for Non-human Primate Imaging

Michael P Milham et al. Neuron. 2018.

. 2018 Oct 10;100(1):61-74.e2.

doi: 10.1016/j.neuron.2018.08.039. Epub 2018 Sep 27.

Authors

Affiliations

¹ Center for the Developing Brain, Child Mind Institute, New York, NY 10022, USA; Center for Biomedical Imaging and Neuromodulation, Nathan S. Kline Institute for Psychiatric Research, Orangeburg, NY 10962, USA. Electronic address: michael.milham@childmind.org.
² Center for the Developing Brain, Child Mind Institute, New York, NY 10022, USA.
³ University of Lyon, Université Claude Bernard Lyon 1, INSERM, Stem Cell and Brain Research Institute U1208, Lyon, France.
⁴ Institute of Neuroscience, Newcastle University, Newcastle upon Tyne NE1 7RU, UK.
⁵ Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
⁶ Biomedical MR Imaging and Spectroscopy Group, Center for Image Sciences, University Medical Center Utrecht, Utrecht, The Netherlands.
⁷ Institut de Neurosciences de la Timone, CNRS & Aix-Marseille Université, UMR 7289, Marseille, France.
⁸ Key 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.
⁹ Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN Nijmegen, Netherlands.
¹⁰ NeuroSpin, CEA, INSERM U992, Université Paris-Saclay, 91191 Gif-sur-Yvette, France.
¹¹ Centre for Functional and Metabolic Mapping, The University of Western Ontario, London, ON N6A 3K7, Canada.
¹² Department of Behavior Neuroscience, Department of Psychiatry, Advanced Imaging Research Center, Oregon Health and Science University, Portland, OR, USA.
¹³ Department of Radiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
¹⁴ Laboratory of Neural Systems, The Rockefeller University, New York, NY, USA.
¹⁵ Center for Neural Science, New York University, New York, NY 10023, USA.
¹⁶ INSERM, U1028, CNRS UMR5292, Lyon Neuroscience Research Center, Lyon, France.
¹⁷ Institut des Sciences Cognitives - Marc Jeannerod, UMR5229, CNRS-Université de Lyon, Lyon, France.
¹⁸ Center for Magnetic Resonance Research, University of Minnesota Medical School, Minneapolis, MN 55455, USA.
¹⁹ Laboratory of Brain and Cognition, National Institute of Mental Health, Bethesda, MD 20892, USA.
²⁰ Princeton Neuroscience Institute, Princeton University, Princeton, NJ 08540, USA.
²¹ Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, 1105 BA Amsterdam, the Netherlands; Department of Psychiatry, Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, the Netherlands.
²² Shanghai 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; Shanghai Key Laboratory of Magnetic Resonance, East China Normal University, Shanghai 200062, China; NYU-ECNU Institute of Brain and Cognitive Science at NYU Shanghai, Shanghai 200062, China.
²³ Centre for Social Learning and Cognitive Evolution, School of Biology, University of St. Andrews, St. Andrews, UK.
²⁴ Section on Cognitive Neurophysiology and Imaging, National Institute of Mental Health, Bethesda, MD 20892, USA; Neurophysiology Imaging Facility, National Institute of Mental Health, National Institute of Neurological Disorders and Stroke, National Eye Institute, Bethesda, MD 20892, USA.
²⁵ Institute for Future Studies, Stockholm, Sweden; Centre for Cultural Evolution & Department of Zoology, Stockholm University, Stockholm, Sweden.
²⁶ Donders Institute for Brain, Cognition and Behavior, Radboud University Nijmegen, 6525 EN Nijmegen, Netherlands; Wellcome 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.
²⁷ McConnell Brain Imaging Centre, Montreal Neurological Institute, Departments of Neurology, Neurosurgery, and Biomedical Engineering, McGill University, Montreal, QC H3A 0G4, Canada.
²⁸ California National Primate Research Center, Davis, CA 95616, USA; Department of Neurology, School of Medicine, University of California, Davis, CA 95616, USA.
²⁹ McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA 02139, USA.
³⁰ Department of Biology and Helmholtz Institute, Utrecht University, 35 84 CH Utrecht, The Netherlands; Department of Biology, McGill University, Montreal, QC H3A 1BA, Canada.
³¹ Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, 1105 BA Amsterdam, the Netherlands; Department of Psychiatry, Amsterdam UMC, University of Amsterdam, 1105 AZ Amsterdam, the Netherlands; Department of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research, Vrije Universiteit, 1081 HV Amsterdam, the Netherlands.
³² Wellcome 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; Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, Oxford OX1 3AQ, UK.
³³ Section on Cognitive Neurophysiology and Imaging, National Institute of Mental Health, Bethesda, MD 20892, USA.
³⁴ Wellcome Centre for Integrative Neuroimaging, Department of Experimental Psychology, University of Oxford, Oxford OX1 3AQ, UK.
³⁵ Developmental Neurogenomics Unit, National Institute of Mental Health, Bethesda, MD 20892, USA; Brain Mapping Unit, Department of Psychiatry, University of Cambridge, Cambridge CB2 0SZ, UK.
³⁶ Divisions of Neuroscience and Cardiometabolic Health, Oregon National Primate Research Center, Beaverton, OR, USA; Department of Human Physiology, University of Oregon, Eugene, OR, USA.
³⁷ Department of Biology and Helmholtz Institute, Utrecht University, 35 84 CH Utrecht, The Netherlands.
³⁸ Department of Computation and Neural Systems, California Institute of Technology, Pasadena, CA 91125, USA.
³⁹ Institute of Neuroscience, Key Laboratory of Primate Neurobiology, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai, China.
⁴⁰ Neurophysiology Imaging Facility, National Institute of Mental Health, National Institute of Neurological Disorders and Stroke, National Eye Institute, Bethesda, MD 20892, USA.
⁴¹ Krieger Mind/Brain Institute, Department of Neurosurgery, Johns Hopkins University, Baltimore, MD 21287, USA.
⁴² Max Planck Research Group for Neuroanatomy and Connectivity, Max Planck Institute for Human Cognitive and Brain Sciences, 04103 Leipzig, Germany; Centre national de la recherche scientifique, CNRS UMR 7225, Institut du Cerveau et de la Moelle épinière, 75013 Paris, France.
⁴³ Center for Biomedical Imaging and Neuromodulation, Nathan S. Kline Institute for Psychiatric Research, Orangeburg, NY 10962, USA; Department of Neurological Surgery, Columbia University College of Physicians and Surgeons, New York, NY 10032, USA; Department of Psychiatry, Columbia University College of Physicians and Surgeons, New York, NY 10032, USA.

PMID: 30269990
PMCID: PMC6231397
DOI: 10.1016/j.neuron.2018.08.039

Abstract

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 PRIME-DE 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.

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Figures

**Figure 1**
Spatial Quality Metrics for Morphometry MRI Datasets Spatial quality metrics include: contrast-to-noise ratio (CNR), smoothness of voxels indexed as full width at half maximum (FWHM), signal-to-noise ratio (SNR), and artifactual voxel detection (Qi1). See Table 3 for details on this and the other quality metrics released. The colored scatterplots illustrate the quality metrics distribution for each data collection. The violin plots on the left of each panel represent a kernel density estimation of the distribution across all data collections for each quality metric. Starting from the bottom: each horizontal line marks the 1^st, 5^th, 25^th, 50^th, 75^th, 95^th, and 99^th percentiles.

**Figure 2**
Spatial and Temporal Quality Metrics for Functional MRI Datasets Spatial quality metrics include: ghost-to-single ratio (GSR), smoothness of voxels indexed as full width at half maximum (FWHM), and signal-to-noise ratio (SNR). Temporal metrics are mean frame-wise displacement (Mean FD), standardized DVARS, global correlation (GCORR), and temporal signal-to-noise ratio (tSNR). See Table 3 for details on this and the other quality metrics released. The colored scatterplots illustrate the quality metrics distribution for each data collection. The violin plots on the left of each panel represent a kernel density estimation of the distribution across all data collections for each quality metric. Starting from the bottom: each horizontal line marks the 1^st, 5^th, 25^th, 50^th, 75^th, 95^th, and 99^th percentiles.

**Figure 3**
Example Structural Images Example structural images aligned to the common space defined by the NMT template.

**Figure 4**
Example Functional Images Example functional images aligned to the common space defined by the NMT template.

See this image and copyright information in PMC

Comment in

The Blind Men and the Elephant: The Quest for Open Data Repositories.
Vanduffel W. Vanduffel W. Neuron. 2018 Oct 10;100(1):1-3. doi: 10.1016/j.neuron.2018.09.039. Neuron. 2018. PMID: 30308163
A nonhuman primate imaging resource.
Strack R. Strack R. Nat Methods. 2018 Dec;15(12):1002. doi: 10.1038/s41592-018-0251-4. Nat Methods. 2018. PMID: 30504876 No abstract available.

References

1. Alexander L.M., Escalera J., Ai L., Andreotti C., Febre K., Mangone A., Vega-Potler N., Langer N., Alexander A., Kovacs M. An open resource for transdiagnostic research in pediatric mental health and learning disorders. Sci. Data. 2017;4:170181. - PMC - PubMed
1. Avants B.B., Tustison N.J., Song G., Cook P.A., Klein A., Gee J.C. A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage. 2011;54:2033–2044. - PMC - PubMed
1. Balbastre Y., Rivière D., Souedet N., Fischer C., Hérard A.-S., Williams S., Vandenberghe M.E., Flament J., Aron-Badin R., Hantraye P. Primatologist: a modular segmentation pipeline for macaque brain morphometry. Neuroimage. 2017;162:306–321. - PubMed
1. Bargmann C.I., Newsome W.T. The Brain Research through Advancing Innovative Neurotechnologies (BRAIN) initiative and neurology. JAMA Neurol. 2014;71:675–676. - PubMed
1. Barttfeld P., Uhrig L., Sitt J.D., Sigman M., Jarraya B., Dehaene S. Signature of consciousness in the dynamics of resting-state brain activity. Proc. Natl. Acad. Sci. USA. 2015;112:887–892. - PMC - PubMed

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An Open Resource for Non-human Primate Imaging

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An Open Resource for Non-human Primate Imaging

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