An Open Resource for Non-human Primate Imaging

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.

References 66

1. 1.
   An open resource for transdiagnostic research in pediatric mental health and learning disorders · 2017

   No notice
2. 2.

   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.

   Not in our library10.1016/j.neuroimage.2010.09.025

3. 3.

   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.

   Not in our library10.1016/j.neuroimage.2017.09.007

4. 4.

   Bargmann C.I., Newsome W.T. The Brain Research through Advancing Innovative Neurotechnologies (BRAIN) initiative and neurology. JAMA Neurol. 2014;71:675-676.

   Not in our library10.1001/jamaneurol.2014.411

5. 5.

   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.

   Not in our library10.1073/pnas.1418031112

6. 6.

   Calabrese E., Badea A., Coe C.L., Lubach G.R., Shi Y., Styner M.A., Johnson G.A. A diffusion tensor MRI atlas of the postmortem rhesus macaque brain. Neuroimage. 2015;117:408-416.

   Not in our library10.1016/j.neuroimage.2015.05.072

7. 7.

   Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996;29:162-173.

   Not in our library10.1006/cbmr.1996.0014

8. 8.
   Enhancing studies of the connectome in autism using the autism brain imaging data exchange II · 2017

   No notice
9. 9.

   Donahue C.J., Sotiropoulos S.N., Jbabdi S., Hernandez-Fernandez M., Behrens T.E., Dyrby T.B., Coalson T., Kennedy H., Knoblauch K., Van Essen D.C., Glasser M.F. Using diffusion tractography to predict cortical connection strength and distance: a quantitative comparison with tracers in the monkey. J. Neurosci. 2016;36:6758-6770.

   Not in our library10.1523/jneurosci.0493-16.2016

10. 10.

    Fischl B. FreeSurfer. Neuroimage. 2012;62:774-781.

    Not in our library10.1016/j.neuroimage.2012.01.021

11. 11.

    Fox A.S., Oler J.A., Shackman A.J., Shelton S.E., Raveendran M., McKay D.R., Converse A.K., Alexander A., Davidson R.J., Blangero J. Intergenerational neural mediators of early-life anxious temperament. Proc. Natl. Acad. Sci. USA. 2015;112:9118-9122.

    Not in our library10.1073/pnas.1508593112

12. 12.

    Frey S., Pandya D.N., Chakravarty M.M., Bailey L., Petrides M., Collins D.L. An MRI based average macaque monkey stereotaxic atlas and space (MNI monkey space). Neuroimage. 2011;55:1435-1442.

    Not in our library10.1016/j.neuroimage.2011.01.040

13. 13.

    Friedman L., Glover G.H., Krenz D., Magnotta V., FIRST BIRN. Reducing inter-scanner variability of activation in a multicenter fMRI study: role of smoothness equalization. Neuroimage. 2006;32:1656-1668.

    Not in our library10.1016/j.neuroimage.2006.03.062

14. 14.

    Ghahremani M., Hutchison R.M., Menon R.S., Everling S. Frontoparietal functional connectivity in the common marmoset. Cereb. Cortex. 2017;27:3890-3905.

    Not in our library10.1093/cercor/bhw198

15. 15.

    Giannelli M., Diciotti S., Tessa C., Mascalchi M. Characterization of Nyquist ghost in EPI-fMRI acquisition sequences implemented on two clinical 1.5 T MR scanner systems: effect of readout bandwidth and echo spacing. J. Appl. Clin. Med. Phys. 2010;11:3237.

    Not in our library10.1120/jacmp.v11i4.3237

16. 16.
    NeuroVault.org: a web-based repository for collecting and sharing unthresholded statistical maps of the human brain · 2015

    No notice
17. 17.
    BIDS apps: Improving ease of use, accessibility, and reproducibility of neuroimaging data analysis methods · 2017

    No notice
18. 18.

    Goulas A., Stiers P., Hutchison R.M., Everling S., Petrides M., Margulies D.S. Intrinsic functional architecture of the macaque dorsal and ventral lateral frontal cortex. J. Neurophysiol. 2017;117:1084-1099.

    Not in our library10.1152/jn.00486.2016

19. 19.

    Grayson D.S., Bliss-Moreau E., Machado C.J., Bennett J., Shen K., Grant K.A., Fair D.A., Amaral D.G. The rhesus monkey connectome predicts disrupted functional networks resulting from pharmacogenetic inactivation of the amygdala. Neuron. 2016;91:453-466.

    Not in our library10.1016/j.neuron.2016.06.005

20. 20.
    Monkey in the middle: why non-human primates are needed to bridge the gap in resting-state investigations · 2012

    No notice
21. 21.

    Hutchison R.M., Everling S. Broad intrinsic functional connectivity boundaries of the macaque prefrontal cortex. Neuroimage. 2014;88:202-211.

    Not in our library10.1016/j.neuroimage.2013.11.024

22. 22.

    Hutchison R.M., Leung L.S., Mirsattari S.M., Gati J.S., Menon R.S., Everling S. Resting-state networks in the macaque at 7 T. Neuroimage. 2011;56:1546-1555.

    Not in our library10.1016/j.neuroimage.2011.02.063

23. 23.

    Hutchison R.M., Gallivan J.P., Culham J.C., Gati J.S., Menon R.S., Everling S. Functional connectivity of the frontal eye fields in humans and macaque monkeys investigated with resting-state fMRI. J. Neurophysiol. 2012;107:2463-2474.

    Not in our library10.1152/jn.00891.2011

24. 24.

    Hutchison R.M., Culham J.C., Flanagan J.R., Everling S., Gallivan J.P. Functional subdivisions of medial parieto-occipital cortex in humans and nonhuman primates using resting-state fMRI. Neuroimage. 2015;116:10-29.

    Not in our library10.1016/j.neuroimage.2015.04.068

25. 25.

    Iglesias J.E., Liu C.-Y., Thompson P.M., Tu Z. Robust brain extraction across datasets and comparison with publicly available methods. IEEE Trans. Med. Imaging. 2011;30:1617-1634.

    Not in our library10.1109/tmi.2011.2138152

26. 26.

    Jenkinson M., Bannister P., Brady M., Smith S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage. 2002;17:825-841.

    Not in our library10.1016/s1053-8119(02)91132-8

27. 27.

    Keliris G.A., Shmuel A., Ku S.-P., Pfeuffer J., Oeltermann A., Steudel T., Logothetis N.K. Robust controlled functional MRI in alert monkeys at high magnetic field: effects of jaw and body movements. Neuroimage. 2007;36:550-570.

    Not in our library10.1016/j.neuroimage.2007.02.057

28. 28.

    Love S.A., Marie D., Roth M., Lacoste R., Nazarian B., Bertello A., Coulon O., Anton J.-L., Meguerditchian A. The average baboon brain: MRI templates and tissue probability maps from 89 individuals. Neuroimage. 2016;132:526-533.

    Not in our library10.1016/j.neuroimage.2016.03.018

29. 29.

    Magnotta V.A., Friedman L., FIRST BIRN. Measurement of signal-to-noise and contrast-to-noise in the fBIRN multicenter imaging study. J. Digit. Imaging. 2006;19:140-147.

    Not in our library10.1007/s10278-006-0264-x

30. 30.

    Markov N.T., Ercsey-Ravasz M.M., Ribeiro Gomes A.R., Lamy C., Magrou L., Vezoli J., Misery P., Falchier A., Quilodran R., Gariel M.A. A weighted and directed interareal connectivity matrix for macaque cerebral cortex. Cereb. Cortex. 2014;24:17-36.

    Not in our library10.1093/cercor/bhs270

31. 31.

    Mars R.B., Jbabdi S., Sallet J., O’Reilly J.X., Croxson P.L., Olivier E., Noonan M.P., Bergmann C., Mitchell A.S., Baxter M.G. Diffusion-weighted imaging tractography-based parcellation of the human parietal cortex and comparison with human and macaque resting-state functional connectivity. J. Neurosci. 2011;31:4087-4100.

    Not in our library10.1523/jneurosci.5102-10.2011

32. 32.

    McLaren D.G., Kosmatka K.J., Oakes T.R., Kroenke C.D., Kohama S.G., Matochik J.A., Ingram D.K., Johnson S.C. A population-average MRI-based atlas collection of the rhesus macaque. Neuroimage. 2009;45:52-59.

    Not in our library10.1016/j.neuroimage.2008.10.058

33. 33.

    Mennes M., Biswal B.B., Castellanos F.X., Milham M.P. Making data sharing work: the FCP/INDI experience. Neuroimage. 2013;82:683-691.

    Not in our library10.1016/j.neuroimage.2012.10.064

34. 34.

    Miranda-Dominguez O., Mills B.D., Grayson D., Woodall A., Grant K.A., Kroenke C.D., Fair D.A. Bridging the gap between the human and macaque connectome: a quantitative comparison of global interspecies structure-function relationships and network topology. J. Neurosci. 2014;34:5552-5563.

    Not in our library10.1523/jneurosci.4229-13.2014

35. 35.

    Mortamet B., Bernstein M.A., Jack C.R., Gunter J.L., Ward C., Britson P.J., Meuli R., Thiran J.-P., Krueger G., Alzheimer’s Disease Neuroimaging Initiative. Automatic quality assessment in structural brain magnetic resonance imaging. Magn. Reson. Med. 2009;62:365-372.

    Not in our library10.1002/mrm.21992

36. 36.

    Navarrete A.F., Blezer E.L.A., Pagnotta M., de Viet E.S.M., Todorov O.S., Lindenfors P., Laland K.N., Reader S.M. Primate brain anatomy: New volumetric MRI measurements for neuroanatomical studies. Brain, Behavior and Evolution. 2018;91:1-9.

    Not in our library10.1159/000488136

37. 37.

    Nichols T.E. Standardizing DVARS, 28/10/12. 2012.

    Not in our library

38. 38.
    The NKI-Rockland Sample: A Model for Accelerating the Pace of Discovery Science in Psychiatry · 2012

    No notice
39. 39.

    Paxinos G. The Rhesus Monkey Brain in Stereotaxic Coordinates. 2009.

    Not in our library

40. 40.

    Paxinos G., Huang X.-F., Toga A.W. The Rhesus Monkey Brain in Stereotaxic Coordinates. 1999.

    Not in our library

41. 41.

    Pfeuffer J., Shmuel A., Keliris G.A., Steudel T., Merkle H., Logothetis N.K. Functional MR imaging in the awake monkey: effects of motion on dynamic off-resonance and processing strategies. Magn. Reson. Imaging. 2007;25:869-882.

    Not in our library10.1016/j.mri.2007.03.002

42. 42.

    Power J.D. A simple but useful way to assess fMRI scan qualities. Neuroimage. 2017;154:150-158.

    Not in our library10.1016/j.neuroimage.2016.08.009

43. 43.

    Reveley C., Gruslys A., Ye F.Q., Glen D., Samaha J., E Russ B., Saad Z., K Seth A., Leopold D.A., Saleem K.S. Three-dimensional digital template atlas of the macaque brain. Cereb. Cortex. 2017;27:4463-4477.

    Not in our library10.1093/cercor/bhw248

44. 44.

    Rilling J.K. Comparative primate neuroimaging: insights into human brain evolution. Trends Cogn. Sci. 2014;18:46-55.

    Not in our library10.1016/j.tics.2013.09.013

45. 45.
    The INIA19 Template and NeuroMaps Atlas for Primate Brain Image Parcellation and Spatial Normalization · 2012

    No notice
46. 46.

    Saleem K.S., Logothetis N.K. A Combined MRI and Histology Atlas of the Rhesus Monkey Brain in Stereotaxic Coordinates. 2012.

    Not in our library

47. 47.

    Schwiedrzik C.M., Zarco W., Everling S., Freiwald W.A. Face patch resting state networks link face processing to social cognition. PLoS Biol. 2015;13:e1002245.

    Not in our library10.1371/journal.pbio.1002245

48. 48.

    Ségonne F., Dale A.M., Busa E., Glessner M., Salat D., Hahn H.K., Fischl B. A hybrid approach to the skull stripping problem in MRI. Neuroimage. 2004;22:1060-1075.

    Not in our library10.1016/j.neuroimage.2004.03.032

49. 49.

    Seidlitz J., Váša F., Shinn M., Romero-Garcia R., Whitaker K.J., Vértes P.E., Wagstyl K., Kirkpatrick Reardon P., Clasen L., Liu S., NSPN Consortium. Morphometric similarity networks detect microscale cortical organization and predict inter-individual cognitive variation. Neuron. 2018;97:231-247.e7.

    Not in our library10.1016/j.neuron.2017.11.039

50. 50.

    Seidlitz J., Sponheim C., Glen D., Ye F.Q., Saleem K.S., Leopold D.A., Ungerleider L., Messinger A. A population MRI brain template and analysis tools for the macaque. Neuroimage. 2018;170:121-131.

    Not in our library10.1016/j.neuroimage.2017.04.063

51. 51.

    Shattuck D.W., Leahy R.M. BrainSuite: an automated cortical surface identification tool. Med. Image Anal. 2002;6:129-142.

    Not in our library10.1016/s1361-8415(02)00054-3

52. 52.

    Shehzad Z., Giavasis S., Li Q., Benhajali Y., Yan C., Yang Z., Milham M., Bellec P., Craddock C. The Preprocessed Connectomes Project Quality Assessment Protocol - a resource for measuring the quality of MRI data. Front. Neurosci. 2015.

    Not in our library

53. 53.

    Shmuel A., Leopold D.A. Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: Implications for functional connectivity at rest. Hum. Brain Mapp. 2008;29:751-761.

    Not in our library10.1002/hbm.20580

54. 54.

    Smith S.M. Fast robust automated brain extraction. Hum. Brain Mapp. 2002;17:143-155.

    Not in our library10.1002/hbm.10062

55. 55.

    Smith S.M., Jenkinson M., Woolrich M.W., Beckmann C.F., Behrens T.E.J., Johansen-Berg H., Bannister P.R., De Luca M., Drobnjak I., Flitney D.E. Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage. 2004;23:S208-S219.

    Not in our library10.1016/j.neuroimage.2004.07.051

56. 56.

    Van Essen D.C. Windows on the brain: the emerging role of atlases and databases in neuroscience. Curr. Opin. Neurobiol. 2002;12:574-579.

    Not in our library10.1016/s0959-4388(02)00361-6

57. 57.

    Van Essen D.C. Cortical cartography and Caret software. Neuroimage. 2012;62:757-764.

    Not in our library10.1016/j.neuroimage.2011.10.077

58. 58.

    Van Essen D.C., Glasser M.F. In vivo architectonics: a cortico-centric perspective. Neuroimage. 2014;93:157-164.

    Not in our library10.1016/j.neuroimage.2013.04.095

59. 59.

    Van Essen D.C., Glasser M.F., Dierker D.L., Harwell J. Cortical parcellations of the macaque monkey analyzed on surface-based atlases. Cereb. Cortex. 2012;22:2227-2240.

    Not in our library10.1093/cercor/bhr290

60. 60.

    Van Essen D.C., Smith S.M., Barch D.M., Behrens T.E.J., Yacoub E., Ugurbil K., WU-Minn HCP Consortium. The WU-Minn Human Connectome Project: an overview. Neuroimage. 2013;80:62-79.

    Not in our library10.1016/j.neuroimage.2013.05.041

61. 61.

    Vanderwal T., Kelly C., Eilbott J., Mayes L.C., Castellanos F.X. Inscapes: a movie paradigm to improve compliance in functional magnetic resonance imaging. Neuroimage. 2015;122:222-232.

    Not in our library10.1016/j.neuroimage.2015.07.069

62. 62.

    Vanduffel W., Zhu Q., Orban G.A. Monkey cortex through fMRI glasses. Neuron. 2014;83:533-550.

    Not in our library10.1016/j.neuron.2014.07.015

63. 63.

    Vincent J.L., Patel G.H., Fox M.D., Snyder A.Z., Baker J.T., Van Essen D.C., Zempel J.M., Snyder L.H., Corbetta M., Raichle M.E. Intrinsic functional architecture in the anaesthetized monkey brain. Nature. 2007;447:83-86.

    Not in our library10.1038/nature05758

64. 64.

    Xu T., Falchier A., Sullivan E.L., Linn G., Ramirez J.S.B., Ross D., Feczko E., Opitz A., Bagley J., Sturgeon D. Delineating the macroscale areal organization of the macaque cortex in vivo. Cell Rep. 2018;23:429-441.

    Not in our library10.1016/j.celrep.2018.03.049

65. 65.

    Young J.T., Shi Y., Niethammer M., Grauer M., Coe C.L., Lubach G.R., Davis B., Budin F., Knickmeyer R.C., Alexander A.L., Styner M.A. The UNC-Wisconsin Rhesus Macaque Neurodevelopment Database: a structural MRI and DTI database of early postnatal development. Front. Neurosci. 2017;11:29.

    Not in our library10.3389/fnins.2017.00029

66. 66.

    Zhang D., Guo L., Zhu D., Li K., Li L., Chen H., Zhao Q., Hu X., Liu T. Diffusion tensor imaging reveals evolution of primate brain architectures. Brain Struct. Funct. 2013;218:1429-1450.

    Not in our library10.1007/s00429-012-0468-4

Cited by papers we hold 12

• A somato-cognitive action network alternates with effector regions in motor cortex · 2023
  No notice
• Robust estimation of cortical similarity networks from brain MRI · 2023
  No notice
• Genetic and phylogenetic uncoupling of structure and function in human transmodal cortex · 2022
  No notice
• Minimal specifications for non-human primate MRI: Challenges in standardizing and harmonizing data collection · 2021
  Not checked
• Distinct higher-order representations of natural sounds in human and ferret auditory cortex · 2021
  Not checked
• Animal Functional Magnetic Resonance Imaging: Trends and Path Toward Standardization · 2020
  Not checked
• Nature abhors a paywall: How open science can realize the potential of naturalistic stimuli · 2020
  Not checked
• XTRACT - Standardised protocols for automated tractography in the human and macaque brain · 2020
  No notice
• ENIGMA and global neuroscience: A decade of large-scale studies of the brain in health and disease across more than 40 countries · 2020
  No notice
• Shaping brain structure: Genetic and phylogenetic axes of macroscale organization of cortical thickness · 2020
  No notice
• Sulcal organization in the medial frontal cortex provides insights into primate brain evolution · 2019
  Not checked
• Open science challenges, benefits and tips in early career and beyond · 2019
  Corrected

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.