Skip to main content
Top
Published in: Neuroinformatics 3/2022

14-09-2021 | Original Article

Population-Average Brain Templates and Application to Automated Voxel-Wise Analysis Pipelines for Cynomolgus Macaque

Authors: Fubing Ouyang, Xinran Chen, Jiahui Liang, Jianle Li, Zimu Jiang, Yicong Chen, Zhicong Yan, Jinsheng Zeng, Shihui Xing

Published in: Neuroinformatics | Issue 3/2022

Log in

Activate our intelligent search to find suitable subject content or patents.

search-config
loading …

Abstract

The growing number of neuroimaging studies of cynomolgus macaques require extending existing templates to facilitate species-specific application of voxel-wise neuroimaging methodologies. This study aimed to create population-averaged structural magnetic resonance imaging (MRI) and diffusion tensor imaging (DTI) templates for the cynomolgus macaques and apply the templates in fully automated voxel-wise analyses. We presented the development of symmetric and asymmetric MRI and DTI templates from a sample of 63 young male cynomolgus monkeys with the use of optimized template creation approaches. We also generated the associated average tissue probability maps and Diffeomorphic Anatomical Registration using Exponentiated Lie Algebra templates for use with the Statistical Parametric Mapping (SPM), as well as the average fractional anisotropy/skeleton targets for incorporation into tract-based spatial statistics (TBSS) framework. Both asymmetric and symmetric templates in a standardized coordinate space demonstrated low bias and high contrast. Fully automated processing using SPM was accomplished for all native MRI datasets and demonstrated outstanding performance regarding skull-stripping, segmentation, and normalization when using the MRI templates. Automated normalization to the DTI template was excellently achieved for all native DTI images using the TBSS pipeline. The cynomolgus MRI and DTI templates are anticipated to provide a common platform for precise single-subject data analysis and facilitate comparison of neuroimaging findings in cynomolgus monkeys across studies and sites. It is also hoped that the procedures of template creation and fully-automated voxel-wise frameworks will provide a straightforward avenue for investigating brain function, development, and neuro-psychopathological disorders in non-human primate models.

Dont have a licence yet? Then find out more about our products and how to get one now:

Springer Professional "Wirtschaft+Technik"

Online-Abonnement

Mit Springer Professional "Wirtschaft+Technik" erhalten Sie Zugriff auf:

  • über 102.000 Bücher
  • über 537 Zeitschriften

aus folgenden Fachgebieten:

  • Automobil + Motoren
  • Bauwesen + Immobilien
  • Business IT + Informatik
  • Elektrotechnik + Elektronik
  • Energie + Nachhaltigkeit
  • Finance + Banking
  • Management + Führung
  • Marketing + Vertrieb
  • Maschinenbau + Werkstoffe
  • Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

Springer Professional "Technik"

Online-Abonnement

Mit Springer Professional "Technik" erhalten Sie Zugriff auf:

  • über 67.000 Bücher
  • über 390 Zeitschriften

aus folgenden Fachgebieten:

  • Automobil + Motoren
  • Bauwesen + Immobilien
  • Business IT + Informatik
  • Elektrotechnik + Elektronik
  • Energie + Nachhaltigkeit
  • Maschinenbau + Werkstoffe




 

Jetzt Wissensvorsprung sichern!

Springer Professional "Wirtschaft"

Online-Abonnement

Mit Springer Professional "Wirtschaft" erhalten Sie Zugriff auf:

  • über 67.000 Bücher
  • über 340 Zeitschriften

aus folgenden Fachgebieten:

  • Bauwesen + Immobilien
  • Business IT + Informatik
  • Finance + Banking
  • Management + Führung
  • Marketing + Vertrieb
  • Versicherung + Risiko




Jetzt Wissensvorsprung sichern!

Appendix
Available only for authorised users
Literature
go back to reference Adluru, N., Zhang, H., Fox, A. S., Shelton, S. E., Ennis, C. M., Bartosic, A. M., et al. (2012). A diffusion tensor brain template for rhesus macaques. NeuroImage, 59(1), 306–318.PubMedCrossRef Adluru, N., Zhang, H., Fox, A. S., Shelton, S. E., Ennis, C. M., Bartosic, A. M., et al. (2012). A diffusion tensor brain template for rhesus macaques. NeuroImage, 59(1), 306–318.PubMedCrossRef
go back to reference Alexander, G. E., Chen, K., Aschenbrenner, M., Merkley, T. L., Santerre-Lemmon, L. E., Shamy, J. L., et al. (2008). Age-related regional network of magnetic resonance imaging gray matter in the rhesus macaque. Journal of Neuroscience, 28(11), 2710–2718.PubMedCrossRef Alexander, G. E., Chen, K., Aschenbrenner, M., Merkley, T. L., Santerre-Lemmon, L. E., Shamy, J. L., et al. (2008). Age-related regional network of magnetic resonance imaging gray matter in the rhesus macaque. Journal of Neuroscience, 28(11), 2710–2718.PubMedCrossRef
go back to reference Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. NeuroImage, 38(1), 95–113.PubMedCrossRef Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. NeuroImage, 38(1), 95–113.PubMedCrossRef
go back to reference Avants, B. B., Tustison, N. J., Song, G., Cook, P. A., Klein, A., & Gee, J. C. (2011a). A reproducible evaluation of ANTs similarity metric performance in brain image registration. NeuroImage, 54(3), 2033–2044.PubMedCrossRef Avants, B. B., Tustison, N. J., Song, G., Cook, P. A., Klein, A., & Gee, J. C. (2011a). A reproducible evaluation of ANTs similarity metric performance in brain image registration. NeuroImage, 54(3), 2033–2044.PubMedCrossRef
go back to reference Avants, B. B., Tustison, N. J., Wu, J., Cook, P. A., & Gee, J. C. (2011b). An open source multivariate framework for n-tissue segmentation with evaluation on public data. Neuroinformatics, 9(4), 381–400.PubMedPubMedCentralCrossRef Avants, B. B., Tustison, N. J., Wu, J., Cook, P. A., & Gee, J. C. (2011b). An open source multivariate framework for n-tissue segmentation with evaluation on public data. Neuroinformatics, 9(4), 381–400.PubMedPubMedCentralCrossRef
go back to reference Avants, B. B., Yushkevich, P., Pluta, J., Minkoff, D., Korczykowski, M., Detre, J., et al. (2010). The optimal template effect in hippocampus studies of diseased populations. NeuroImage, 49(3), 2457–2466.PubMedCrossRef Avants, B. B., Yushkevich, P., Pluta, J., Minkoff, D., Korczykowski, M., Detre, J., et al. (2010). The optimal template effect in hippocampus studies of diseased populations. NeuroImage, 49(3), 2457–2466.PubMedCrossRef
go back to reference Ballanger, B., Tremblay, L., Sgambato-Faure, V., Beaudoin-Gobert, M., Lavenne, F., Le Bars, D., et al. (2013). A multi-atlas based method for automated anatomical Macaca fascicularis brain MRI segmentation and PET kinetic extraction. NeuroImage, 77, 26–43.PubMedCrossRef Ballanger, B., Tremblay, L., Sgambato-Faure, V., Beaudoin-Gobert, M., Lavenne, F., Le Bars, D., et al. (2013). A multi-atlas based method for automated anatomical Macaca fascicularis brain MRI segmentation and PET kinetic extraction. NeuroImage, 77, 26–43.PubMedCrossRef
go back to reference Behrens, T. E., Berg, H. J., Jbabdi, S., Rushworth, M. F., & Woolrich, M. W. (2007). Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? NeuroImage, 34(1), 144–155.PubMedCrossRef Behrens, T. E., Berg, H. J., Jbabdi, S., Rushworth, M. F., & Woolrich, M. W. (2007). Probabilistic diffusion tractography with multiple fibre orientations: What can we gain? NeuroImage, 34(1), 144–155.PubMedCrossRef
go back to reference Black, K. J., Koller, J. M., Snyder, A. Z., & Perlmutter, J. S. (2001a). Template images for nonhuman primate neuroimaging: 2 Macaque. Neuroimage, 14(3), 744–748.PubMedCrossRef Black, K. J., Koller, J. M., Snyder, A. Z., & Perlmutter, J. S. (2001a). Template images for nonhuman primate neuroimaging: 2 Macaque. Neuroimage, 14(3), 744–748.PubMedCrossRef
go back to reference Black, K. J., Koller, J. M., Snyder, A. Z., & Perlmutter, J. S. (2004). Atlas template images for nonhuman primate neuroimaging: Baboon and macaque. Methods in Enzymology, 385, 91–102.PubMedCrossRef Black, K. J., Koller, J. M., Snyder, A. Z., & Perlmutter, J. S. (2004). Atlas template images for nonhuman primate neuroimaging: Baboon and macaque. Methods in Enzymology, 385, 91–102.PubMedCrossRef
go back to reference Black, K. J., Snyder, A. Z., Koller, J. M., Gado, M. H., & Perlmutter, J. S. (2001b). Template images for nonhuman primate neuroimaging: 1 Baboon. Neuroimage, 14(3), 736–743.PubMedCrossRef Black, K. J., Snyder, A. Z., Koller, J. M., Gado, M. H., & Perlmutter, J. S. (2001b). Template images for nonhuman primate neuroimaging: 1 Baboon. Neuroimage, 14(3), 736–743.PubMedCrossRef
go back to reference Carmichael, S. T., & Price, J. L. (1994). Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. The Journal of Comparative Neurology, 346(3), 366–402.PubMedCrossRef Carmichael, S. T., & Price, J. L. (1994). Architectonic subdivision of the orbital and medial prefrontal cortex in the macaque monkey. The Journal of Comparative Neurology, 346(3), 366–402.PubMedCrossRef
go back to reference Chen, X., Dang, G., Dang, C., Liu, G., Xing, S., Chen, Y., et al. (2015). An ischemic stroke model of nonhuman primates for remote lesion studies: A behavioral and neuroimaging investigation. Restorative Neurology and Neuroscience, 33(2), 131–142.PubMedCrossRef Chen, X., Dang, G., Dang, C., Liu, G., Xing, S., Chen, Y., et al. (2015). An ischemic stroke model of nonhuman primates for remote lesion studies: A behavioral and neuroimaging investigation. Restorative Neurology and Neuroscience, 33(2), 131–142.PubMedCrossRef
go back to reference Chen, X., Errangi, B., Li, L., Glasser, M. F., Westlye, L. T., Fjell, A. M., et al. (2013). Brain aging in humans, chimpanzees (Pan troglodytes), and rhesus macaques (Macaca mulatta): Magnetic resonance imaging studies of macro- and microstructural changes. Neurobiology of Aging, 34(10), 2248–2260.PubMedPubMedCentralCrossRef Chen, X., Errangi, B., Li, L., Glasser, M. F., Westlye, L. T., Fjell, A. M., et al. (2013). Brain aging in humans, chimpanzees (Pan troglodytes), and rhesus macaques (Macaca mulatta): Magnetic resonance imaging studies of macro- and microstructural changes. Neurobiology of Aging, 34(10), 2248–2260.PubMedPubMedCentralCrossRef
go back to reference Collantes, M., Prieto, E., Penuelas, I., Blesa, J., Juri, C., Marti-Climent, J. M., et al. (2009). New MRI, 18F-DOPA and 11C-(+)-alpha-dihydrotetrabenazine templates for Macaca fascicularis neuroimaging: Advantages to improve PET quantification. NeuroImage, 47(2), 533–539.PubMedCrossRef Collantes, M., Prieto, E., Penuelas, I., Blesa, J., Juri, C., Marti-Climent, J. M., et al. (2009). New MRI, 18F-DOPA and 11C-(+)-alpha-dihydrotetrabenazine templates for Macaca fascicularis neuroimaging: Advantages to improve PET quantification. NeuroImage, 47(2), 533–539.PubMedCrossRef
go back to reference Dice, L. (1945). Measures of the amount of ecologic association between species. Ecology, 26, 297–302.CrossRef Dice, L. (1945). Measures of the amount of ecologic association between species. Ecology, 26, 297–302.CrossRef
go back to reference Enard, D., Depaulis, F., & Roest Crollius, H. (2010). Human and non-human primate genomes share hotspots of positive selection. PLoS Genetics, 6(2), e1000840.PubMedPubMedCentralCrossRef Enard, D., Depaulis, F., & Roest Crollius, H. (2010). Human and non-human primate genomes share hotspots of positive selection. PLoS Genetics, 6(2), e1000840.PubMedPubMedCentralCrossRef
go back to reference Evans, A. C., & Collins, D. L., et al. (1993). 3D statistical neuroanatomical models from 305 MRI volumes. Nuclear Science Symposium and Medical Imaging Conference IEEE Conference Record. Evans, A. C., & Collins, D. L., et al. (1993). 3D statistical neuroanatomical models from 305 MRI volumes. Nuclear Science Symposium and Medical Imaging Conference IEEE Conference Record.
go back to reference Fonov, V., Evans, A. C., Botteron, K., Almli, C. R., McKinstry, R. C., Collins, D. L., et al. (2011). Unbiased average age-appropriate atlases for pediatric studies. NeuroImage, 54(1), 313–327.PubMedCrossRef Fonov, V., Evans, A. C., Botteron, K., Almli, C. R., McKinstry, R. C., Collins, D. L., et al. (2011). Unbiased average age-appropriate atlases for pediatric studies. NeuroImage, 54(1), 313–327.PubMedCrossRef
go back to reference Frey, S., Pandya, D. N., Chakravarty, M. M., Bailey, L., Petrides, M., & Collins, D. L. (2011). An MRI based average macaque monkey stereotaxic atlas and space (MNI monkey space). NeuroImage, 55(4), 1435–1442.PubMedCrossRef Frey, S., Pandya, D. N., Chakravarty, M. M., Bailey, L., Petrides, M., & Collins, D. L. (2011). An MRI based average macaque monkey stereotaxic atlas and space (MNI monkey space). NeuroImage, 55(4), 1435–1442.PubMedCrossRef
go back to reference Good, C. D., Johnsrude, I., Ashburner, J., Henson, R. N., Friston, K. J., & Frackowiak, R. S. (2001). Cerebral asymmetry and the effects of sex and handedness on brain structure: A voxel-based morphometric analysis of 465 normal adult human brains. NeuroImage, 14(3), 685–700.PubMedCrossRef Good, C. D., Johnsrude, I., Ashburner, J., Henson, R. N., Friston, K. J., & Frackowiak, R. S. (2001). Cerebral asymmetry and the effects of sex and handedness on brain structure: A voxel-based morphometric analysis of 465 normal adult human brains. NeuroImage, 14(3), 685–700.PubMedCrossRef
go back to reference Greer, P. J., Villemagne, V. L., Ruszkiewicz, J., Graves, A. K., Meltzer, C. C., Mathis, C. A., et al. (2002). MR atlas of the baboon brain for functional neuroimaging. Brain Research Bulletin, 58(4), 429–438.PubMedCrossRef Greer, P. J., Villemagne, V. L., Ruszkiewicz, J., Graves, A. K., Meltzer, C. C., Mathis, C. A., et al. (2002). MR atlas of the baboon brain for functional neuroimaging. Brain Research Bulletin, 58(4), 429–438.PubMedCrossRef
go back to reference Hagmann, P., Cammoun, L., Gigandet, X., Gerhard, S., Grant, P. E., Wedeen, V., et al. (2010). MR connectomics: Principles and challenges. Journal of Neuroscience Methods, 194(1), 34–45.PubMedCrossRef Hagmann, P., Cammoun, L., Gigandet, X., Gerhard, S., Grant, P. E., Wedeen, V., et al. (2010). MR connectomics: Principles and challenges. Journal of Neuroscience Methods, 194(1), 34–45.PubMedCrossRef
go back to reference Heilbroner, P. L., & Holloway, R. L. (1988). Anatomical brain asymmetries in New World and Old World monkeys: Stages of temporal lobe development in primate evolution. American Journal of Physical Anthropology, 76(1), 39–48.PubMedCrossRef Heilbroner, P. L., & Holloway, R. L. (1988). Anatomical brain asymmetries in New World and Old World monkeys: Stages of temporal lobe development in primate evolution. American Journal of Physical Anthropology, 76(1), 39–48.PubMedCrossRef
go back to reference Hikishima, K., Quallo, M. M., Komaki, Y., Yamada, M., Kawai, K., Momoshima, S., et al. (2011). Population-averaged standard template brain atlas for the common marmoset (Callithrix jacchus). NeuroImage, 54(4), 2741–2749.PubMedCrossRef Hikishima, K., Quallo, M. M., Komaki, Y., Yamada, M., Kawai, K., Momoshima, S., et al. (2011). Population-averaged standard template brain atlas for the common marmoset (Callithrix jacchus). NeuroImage, 54(4), 2741–2749.PubMedCrossRef
go back to reference Hirouchi, Y., Suzuki, E., Mitsuoka, C., Jin, H., Kitajima, S., Kohjimoto, Y., et al. (2007). Neuroimaging and histopathological evaluation of delayed neurological damage produced by artificial occlusion of the middle cerebral artery in Cynomolgus monkeys: Establishment of a monkey model for delayed cerebral ischemia. Experimental and Toxicologic Pathology, 59(1), 9–16.PubMedCrossRef Hirouchi, Y., Suzuki, E., Mitsuoka, C., Jin, H., Kitajima, S., Kohjimoto, Y., et al. (2007). Neuroimaging and histopathological evaluation of delayed neurological damage produced by artificial occlusion of the middle cerebral artery in Cynomolgus monkeys: Establishment of a monkey model for delayed cerebral ischemia. Experimental and Toxicologic Pathology, 59(1), 9–16.PubMedCrossRef
go back to reference Hopkins, W. D., Taglialatela, J. P., Meguerditchian, A., Nir, T., Schenker, N. M., & Sherwood, C. C. (2008). Gray matter asymmetries in chimpanzees as revealed by voxel-based morphometry. NeuroImage, 42(2), 491–497.PubMedCrossRef Hopkins, W. D., Taglialatela, J. P., Meguerditchian, A., Nir, T., Schenker, N. M., & Sherwood, C. C. (2008). Gray matter asymmetries in chimpanzees as revealed by voxel-based morphometry. NeuroImage, 42(2), 491–497.PubMedCrossRef
go back to reference Hutchison, R. M., & Everling, S. (2012). Monkey in the middle: Why non-human primates are needed to bridge the gap in resting-state investigations. Frontiers in Neuroanatomy, 6, 29.PubMedPubMedCentralCrossRef Hutchison, R. M., & Everling, S. (2012). Monkey in the middle: Why non-human primates are needed to bridge the gap in resting-state investigations. Frontiers in Neuroanatomy, 6, 29.PubMedPubMedCentralCrossRef
go back to reference Imai, N., Sawada, K., Fukunishi, K., Sakata-Haga, H., & Fukui, Y. (2011). Sexual dimorphism of sulcal length asymmetry in the cerebrum of adult cynomolgus monkeys (Macaca fascicularis). Congenit Anom (kyoto), 51(4), 161–166.CrossRef Imai, N., Sawada, K., Fukunishi, K., Sakata-Haga, H., & Fukui, Y. (2011). Sexual dimorphism of sulcal length asymmetry in the cerebrum of adult cynomolgus monkeys (Macaca fascicularis). Congenit Anom (kyoto), 51(4), 161–166.CrossRef
go back to reference Kirk, E. C. (2006). Visual influences on primate encephalization. Journal of Human Evolution, 51(1), 76–90.PubMedCrossRef Kirk, E. C. (2006). Visual influences on primate encephalization. Journal of Human Evolution, 51(1), 76–90.PubMedCrossRef
go back to reference Koikkalainen, J., Lotjonen, J., Thurfjell, L., Rueckert, D., Waldemar, G., Soininen, H., et al. (2011). Multi-template tensor-based morphometry: Application to analysis of Alzheimer’s disease. NeuroImage, 56(3), 1134–1144.PubMedCrossRef Koikkalainen, J., Lotjonen, J., Thurfjell, L., Rueckert, D., Waldemar, G., Soininen, H., et al. (2011). Multi-template tensor-based morphometry: Application to analysis of Alzheimer’s disease. NeuroImage, 56(3), 1134–1144.PubMedCrossRef
go back to reference Kong, X. Z., Mathias, S. R., Guadalupe, T., Group, E. L. W., Glahn, D. C., Franke, B., et al. (2018). Mapping cortical brain asymmetry in 17,141 healthy individuals worldwide via the ENIGMA Consortium. Proceedings of the National Academy of Sciences of the United States of America, 115(22), 5154–5163. Kong, X. Z., Mathias, S. R., Guadalupe, T., Group, E. L. W., Glahn, D. C., Franke, B., et al. (2018). Mapping cortical brain asymmetry in 17,141 healthy individuals worldwide via the ENIGMA Consortium. Proceedings of the National Academy of Sciences of the United States of America, 115(22), 5154–5163.
go back to reference Kovacevic, N., Henderson, J. T., Chan, E., Lifshitz, N., Bishop, J., Evans, A. C., et al. (2005). A three-dimensional MRI atlas of the mouse brain with estimates of the average and variability. Cerebral Cortex, 15(5), 639–645.PubMedCrossRef Kovacevic, N., Henderson, J. T., Chan, E., Lifshitz, N., Bishop, J., Evans, A. C., et al. (2005). A three-dimensional MRI atlas of the mouse brain with estimates of the average and variability. Cerebral Cortex, 15(5), 639–645.PubMedCrossRef
go back to reference Kurth, F., Gaser, C., & Luders, E. (2015). A 12-step user guide for analyzing voxel-wise gray matter asymmetries in statistical parametric mapping (SPM). Nature Protocols, 10(2), 293–304.PubMedCrossRef Kurth, F., Gaser, C., & Luders, E. (2015). A 12-step user guide for analyzing voxel-wise gray matter asymmetries in statistical parametric mapping (SPM). Nature Protocols, 10(2), 293–304.PubMedCrossRef
go back to reference Latzman, R. D., Taglialatela, J. P., & Hopkins, W. D. (2015). Delay of gratification is associated with white matter connectivity in the dorsal prefrontal cortex: A diffusion tensor imaging study in chimpanzees (Pan troglodytes). Proceedings of the Biological Sciences, 282(1809), 20150764. Latzman, R. D., Taglialatela, J. P., & Hopkins, W. D. (2015). Delay of gratification is associated with white matter connectivity in the dorsal prefrontal cortex: A diffusion tensor imaging study in chimpanzees (Pan troglodytes). Proceedings of the Biological Sciences, 282(1809), 20150764.
go back to reference Li, H. W., Zhang, L., & Qin, C. (2019). Current state of research on non-human primate models of Alzheimer’s disease. Animal Models and Experimental Medicine, 2(4), 227–238.PubMedPubMedCentralCrossRef Li, H. W., Zhang, L., & Qin, C. (2019). Current state of research on non-human primate models of Alzheimer’s disease. Animal Models and Experimental Medicine, 2(4), 227–238.PubMedPubMedCentralCrossRef
go back to reference Liu, C., Tian, X., Liu, H., Mo, Y., Bai, F., Zhao, X., et al. (2015). Rhesus monkey brain development during late infancy and the effect of phencyclidine: A longitudinal MRI and DTI study. NeuroImage, 107, 65–75.PubMedCrossRef Liu, C., Tian, X., Liu, H., Mo, Y., Bai, F., Zhao, X., et al. (2015). Rhesus monkey brain development during late infancy and the effect of phencyclidine: A longitudinal MRI and DTI study. NeuroImage, 107, 65–75.PubMedCrossRef
go back to reference Liu, Z., Li, X., Zhang, J. T., Cai, Y. J., Cheng, T. L., Cheng, C., et al. (2016). Autism-like behaviours and germline transmission in transgenic monkeys overexpressing MeCP2. Nature, 530(7588), 98–102.PubMedCrossRef Liu, Z., Li, X., Zhang, J. T., Cai, Y. J., Cheng, T. L., Cheng, C., et al. (2016). Autism-like behaviours and germline transmission in transgenic monkeys overexpressing MeCP2. Nature, 530(7588), 98–102.PubMedCrossRef
go back to reference Love, S. A., Marie, D., Roth, M., Lacoste, R., Nazarian, B., Bertello, A., et al. (2016). The average baboon brain: MRI templates and tissue probability maps from 89 individuals. NeuroImage, 132, 526–533.PubMedCrossRef Love, S. A., Marie, D., Roth, M., Lacoste, R., Nazarian, B., Bertello, A., et al. (2016). The average baboon brain: MRI templates and tissue probability maps from 89 individuals. NeuroImage, 132, 526–533.PubMedCrossRef
go back to reference Lv, Q., Yan, M., Shen, X., Wu, J., Yu, W., Yan, S., et al. (2021). Normative analysis of individual brain differences based on a population MRI-based atlas of cynomolgus macaques. Cerebral Cortex, 31(1), 341–355.PubMedCrossRef Lv, Q., Yan, M., Shen, X., Wu, J., Yu, W., Yan, S., et al. (2021). Normative analysis of individual brain differences based on a population MRI-based atlas of cynomolgus macaques. Cerebral Cortex, 31(1), 341–355.PubMedCrossRef
go back to reference Maldjian, J. A., Daunais, J. B., Friedman, D. P., & Whitlow, C. T. (2014). Vervet MRI atlas and label map for fully automated morphometric analyses. Neuroinformatics, 12(4), 543–550.PubMedPubMedCentralCrossRef Maldjian, J. A., Daunais, J. B., Friedman, D. P., & Whitlow, C. T. (2014). Vervet MRI atlas and label map for fully automated morphometric analyses. Neuroinformatics, 12(4), 543–550.PubMedPubMedCentralCrossRef
go back to reference Maldjian, J. A., Shively, C. A., Nader, M. A., Friedman, D. P., & Whitlow, C. T. (2016). Multi-atlas library for eliminating normalization failures in non-human primates. Neuroinformatics, 14(2), 183–190.PubMedPubMedCentralCrossRef Maldjian, J. A., Shively, C. A., Nader, M. A., Friedman, D. P., & Whitlow, C. T. (2016). Multi-atlas library for eliminating normalization failures in non-human primates. Neuroinformatics, 14(2), 183–190.PubMedPubMedCentralCrossRef
go back to reference Mazziotta, J., Toga, A., Evans, A., Fox, P., Lancaster, J., Zilles, K., et al. (2001). A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philosophical Transactions of the Royal Society of London. Series b, Biological Sciences, 356(1412), 1293–1322.PubMedPubMedCentralCrossRef Mazziotta, J., Toga, A., Evans, A., Fox, P., Lancaster, J., Zilles, K., et al. (2001). A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philosophical Transactions of the Royal Society of London. Series b, Biological Sciences, 356(1412), 1293–1322.PubMedPubMedCentralCrossRef
go back to reference McLaren, D. G., Kosmatka, K. J., Kastman, E. K., Bendlin, B. B., & Johnson, S. C. (2010). Rhesus macaque brain morphometry: A methodological comparison of voxel-wise approaches. Methods, 50(3), 157–165.PubMedCrossRef McLaren, D. G., Kosmatka, K. J., Kastman, E. K., Bendlin, B. B., & Johnson, S. C. (2010). Rhesus macaque brain morphometry: A methodological comparison of voxel-wise approaches. Methods, 50(3), 157–165.PubMedCrossRef
go back to reference McLaren, D. G., Kosmatka, K. J., Oakes, T. R., Kroenke, C. D., Kohama, S. G., Matochik, J. A., et al. (2009). A population-average MRI-based atlas collection of the rhesus macaque. NeuroImage, 45(1), 52–59.PubMedCrossRef McLaren, D. G., Kosmatka, K. J., Oakes, T. R., Kroenke, C. D., Kohama, S. G., Matochik, J. A., et al. (2009). A population-average MRI-based atlas collection of the rhesus macaque. NeuroImage, 45(1), 52–59.PubMedCrossRef
go back to reference McNab, J. A., Jbabdi, S., Deoni, S. C., Douaud, G., Behrens, T. E., & Miller, K. L. (2009). High resolution diffusion-weighted imaging in fixed human brain using diffusion-weighted steady state free precession. NeuroImage, 46(3), 775–785.PubMedCrossRef McNab, J. A., Jbabdi, S., Deoni, S. C., Douaud, G., Behrens, T. E., & Miller, K. L. (2009). High resolution diffusion-weighted imaging in fixed human brain using diffusion-weighted steady state free precession. NeuroImage, 46(3), 775–785.PubMedCrossRef
go back to reference Mori, S., Oishi, K., Jiang, H., Jiang, L., Li, X., Akhter, K., et al. (2008). Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. NeuroImage, 40(2), 570–582.PubMedCrossRef Mori, S., Oishi, K., Jiang, H., Jiang, L., Li, X., Akhter, K., et al. (2008). Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. NeuroImage, 40(2), 570–582.PubMedCrossRef
go back to reference Nelson, E. E., & Winslow, J. T. (2009). Non-human primates: Model animals for developmental psychopathology. Neuropsychopharmacology, 34(1), 90–105.PubMedCrossRef Nelson, E. E., & Winslow, J. T. (2009). Non-human primates: Model animals for developmental psychopathology. Neuropsychopharmacology, 34(1), 90–105.PubMedCrossRef
go back to reference Neumane, S., Mounayar, S., Jan, C., Epinat, J., Ballanger, B., Costes, N., et al. (2012). Effects of dopamine and serotonin antagonist injections into the striatopallidal complex of asymptomatic MPTP-treated monkeys. Neurobiology of Diseases, 48(1), 27–39.CrossRef Neumane, S., Mounayar, S., Jan, C., Epinat, J., Ballanger, B., Costes, N., et al. (2012). Effects of dopamine and serotonin antagonist injections into the striatopallidal complex of asymptomatic MPTP-treated monkeys. Neurobiology of Diseases, 48(1), 27–39.CrossRef
go back to reference Nie, B., Wang, L., Hu, Y., Liang, S., Tan, Z., Chai, P., et al. (2019). A population stereotaxic positron emission tomography brain template for the macaque and its application to ischemic model. Neuroimage, 203, 116163.PubMedCrossRef Nie, B., Wang, L., Hu, Y., Liang, S., Tan, Z., Chai, P., et al. (2019). A population stereotaxic positron emission tomography brain template for the macaque and its application to ischemic model. Neuroimage, 203, 116163.PubMedCrossRef
go back to reference Ramnani, N., Behrens, T. E., Johansen-Berg, H., Richter, M. C., Pinsk, M. A., Andersson, J. L., et al. (2006). The evolution of prefrontal inputs to the cortico-pontine system: Diffusion imaging evidence from Macaque monkeys and humans. Cerebral Cortex, 16(6), 811–818.PubMedCrossRef Ramnani, N., Behrens, T. E., Johansen-Berg, H., Richter, M. C., Pinsk, M. A., Andersson, J. L., et al. (2006). The evolution of prefrontal inputs to the cortico-pontine system: Diffusion imaging evidence from Macaque monkeys and humans. Cerebral Cortex, 16(6), 811–818.PubMedCrossRef
go back to reference Reveley, C., Gruslys, A., Ye, F. Q., Glen, D., Samaha, J., et al. (2017). Three-dimensional digital template atlas of the macaque brain. Cerebral Cortex, 27(9), 4463–4477.PubMed Reveley, C., Gruslys, A., Ye, F. Q., Glen, D., Samaha, J., et al. (2017). Three-dimensional digital template atlas of the macaque brain. Cerebral Cortex, 27(9), 4463–4477.PubMed
go back to reference Rilling, J. K., Barks, S. K., Parr, L. A., Preuss, T. M., Faber, T. L., Pagnoni, G., et al. (2007). A comparison of resting-state brain activity in humans and chimpanzees. Proceedings of the National Academy of Sciences of the United States of America, 104(43), 17146–17151.PubMedPubMedCentralCrossRef Rilling, J. K., Barks, S. K., Parr, L. A., Preuss, T. M., Faber, T. L., Pagnoni, G., et al. (2007). A comparison of resting-state brain activity in humans and chimpanzees. Proceedings of the National Academy of Sciences of the United States of America, 104(43), 17146–17151.PubMedPubMedCentralCrossRef
go back to reference Seidlitz, J., Sponheim, C., Glen, D., Ye, F. Q., Saleem, K. S., Leopold, D. A., et al. (2018). A population MRI brain template and analysis tools for the macaque. NeuroImage, 170, 121–131.PubMedCrossRef Seidlitz, J., Sponheim, C., Glen, D., Ye, F. Q., Saleem, K. S., Leopold, D. A., et al. (2018). A population MRI brain template and analysis tools for the macaque. NeuroImage, 170, 121–131.PubMedCrossRef
go back to reference Shu, N., Liu, Y., Duan, Y., Li, K. (2015). Hemispheric Asymmetry of Human Brain Anatomical Network Revealed by Diffusion Tensor Tractography. BioMed Research International, 908917. Shu, N., Liu, Y., Duan, Y., Li, K. (2015). Hemispheric Asymmetry of Human Brain Anatomical Network Revealed by Diffusion Tensor Tractography. BioMed Research International, 908917.
go back to reference Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., et al. (2006). Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. NeuroImage, 31(4), 1487–1505.PubMedCrossRef Smith, S. M., Jenkinson, M., Johansen-Berg, H., Rueckert, D., Nichols, T. E., Mackay, C. E., et al. (2006). Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data. NeuroImage, 31(4), 1487–1505.PubMedCrossRef
go back to reference Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23(Suppl 1), S208-219.PubMedCrossRef Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E., Johansen-Berg, H., et al. (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage, 23(Suppl 1), S208-219.PubMedCrossRef
go back to reference Smith, S. M., Johansen-Berg, H., Jenkinson, M., Rueckert, D., Nichols, T. E., Miller, K. L., et al. (2007). Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. Nature Protocols, 2(3), 499–503.PubMedCrossRef Smith, S. M., Johansen-Berg, H., Jenkinson, M., Rueckert, D., Nichols, T. E., Miller, K. L., et al. (2007). Acquisition and voxelwise analysis of multi-subject diffusion data with tract-based spatial statistics. Nature Protocols, 2(3), 499–503.PubMedCrossRef
go back to reference Tian, Q., Yang, G., Leuze, C., Rokem, A., Edlow, B. L., & McNab, J. A. (2019). Generalized diffusion spectrum magnetic resonance imaging (GDSI) for model-free reconstruction of the ensemble average propagator. NeuroImage, 189, 497–515.PubMedCrossRef Tian, Q., Yang, G., Leuze, C., Rokem, A., Edlow, B. L., & McNab, J. A. (2019). Generalized diffusion spectrum magnetic resonance imaging (GDSI) for model-free reconstruction of the ensemble average propagator. NeuroImage, 189, 497–515.PubMedCrossRef
go back to reference Van Der Gucht, E., Youakim, M., Arckens, L., Hof, P. R., & Baizer, J. S. (2006). Variations in the structure of the prelunate gyrus in Old World monkeys. The Anatomical Record. Part a, Discoveries in Molecular, Cellular, and Evolutionary Biology, 288(7), 753–775.PubMedCentralCrossRef Van Der Gucht, E., Youakim, M., Arckens, L., Hof, P. R., & Baizer, J. S. (2006). Variations in the structure of the prelunate gyrus in Old World monkeys. The Anatomical Record. Part a, Discoveries in Molecular, Cellular, and Evolutionary Biology, 288(7), 753–775.PubMedCentralCrossRef
go back to reference Van Essen, D. C., & Dierker, D. L. (2007). Surface-based and probabilistic atlases of primate cerebral cortex. Neuron, 56(2), 209–225.PubMedCrossRef Van Essen, D. C., & Dierker, D. L. (2007). Surface-based and probabilistic atlases of primate cerebral cortex. Neuron, 56(2), 209–225.PubMedCrossRef
go back to reference Vincent, J. L., Patel, G. H., Fox, M. D., Snyder, A. Z., Baker, J. T., Van Essen, D. C., et al. (2007). Intrinsic functional architecture in the anaesthetized monkey brain. Nature, 447(7140), 83–86.PubMedCrossRef Vincent, J. L., Patel, G. H., Fox, M. D., Snyder, A. Z., Baker, J. T., Van Essen, D. C., et al. (2007). Intrinsic functional architecture in the anaesthetized monkey brain. Nature, 447(7140), 83–86.PubMedCrossRef
go back to reference Wang, Y., Gupta, A., Liu, Z., Zhang, H., Escolar, M. L., Gilmore, J. H., et al. (2011). DTI registration in atlas based fiber analysis of infantile Krabbe disease. NeuroImage, 55(4), 1577–1586.PubMedCrossRef Wang, Y., Gupta, A., Liu, Z., Zhang, H., Escolar, M. L., Gilmore, J. H., et al. (2011). DTI registration in atlas based fiber analysis of infantile Krabbe disease. NeuroImage, 55(4), 1577–1586.PubMedCrossRef
go back to reference Wedeen, V. J., Wang, R. P., Schmahmann, J. D., Benner, T., Tseng, W. Y., Dai, G., et al. (2008). Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. NeuroImage, 41(4), 1267–1277.PubMedCrossRef Wedeen, V. J., Wang, R. P., Schmahmann, J. D., Benner, T., Tseng, W. Y., Dai, G., et al. (2008). Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. NeuroImage, 41(4), 1267–1277.PubMedCrossRef
go back to reference Wilke, M., Holland, S. K., Altaye, M., & Gaser, C. (2008). Template-O-Matic: A toolbox for creating customized pediatric templates. NeuroImage, 41(3), 903–913.PubMedCrossRef Wilke, M., Holland, S. K., Altaye, M., & Gaser, C. (2008). Template-O-Matic: A toolbox for creating customized pediatric templates. NeuroImage, 41(3), 903–913.PubMedCrossRef
go back to reference Worbe, Y., Sgambato-Faure, V., Epinat, J., Chaigneau, M., Tande, D., Francois, C., et al. (2013). Towards a primate model of Gilles de la Tourette syndrome: Anatomo-behavioural correlation of disorders induced by striatal dysfunction. Cortex, 49(4), 1126–1140.PubMedCrossRef Worbe, Y., Sgambato-Faure, V., Epinat, J., Chaigneau, M., Tande, D., Francois, C., et al. (2013). Towards a primate model of Gilles de la Tourette syndrome: Anatomo-behavioural correlation of disorders induced by striatal dysfunction. Cortex, 49(4), 1126–1140.PubMedCrossRef
go back to reference Wu, G., Jia, H., Wang, Q., & Shen, D. (2011). SharpMean: Groupwise registration guided by sharp mean image and tree-based registration. NeuroImage, 56(4), 1968–1981.PubMedCrossRef Wu, G., Jia, H., Wang, Q., & Shen, D. (2011). SharpMean: Groupwise registration guided by sharp mean image and tree-based registration. NeuroImage, 56(4), 1968–1981.PubMedCrossRef
go back to reference Zhang, H., Avants, B. B., Yushkevich, P. A., Woo, J. H., Wang, S., McCluskey, L. F., et al. (2007). High-dimensional spatial normalization of diffusion tensor images improves the detection of white matter differences: An example study using amyotrophic lateral sclerosis. IEEE Transactions on Medical Imaging, 26(11), 1585–1597.PubMedCrossRef Zhang, H., Avants, B. B., Yushkevich, P. A., Woo, J. H., Wang, S., McCluskey, L. F., et al. (2007). High-dimensional spatial normalization of diffusion tensor images improves the detection of white matter differences: An example study using amyotrophic lateral sclerosis. IEEE Transactions on Medical Imaging, 26(11), 1585–1597.PubMedCrossRef
go back to reference Zhang, S., Peng, H., Dawe, R. J., & Arfanakis, K. (2011). Enhanced ICBM diffusion tensor template of the human brain. NeuroImage, 54(2), 974–984.PubMedCrossRef Zhang, S., Peng, H., Dawe, R. J., & Arfanakis, K. (2011). Enhanced ICBM diffusion tensor template of the human brain. NeuroImage, 54(2), 974–984.PubMedCrossRef
go back to reference Zhou, Y., Sharma, J., Ke, Q., Landman, R., Yuan, J., Chen, H., et al. (2019). Atypical behaviour and connectivity in SHANK3-mutant macaques. Nature, 570(7761), 326–331.PubMedCrossRef Zhou, Y., Sharma, J., Ke, Q., Landman, R., Yuan, J., Chen, H., et al. (2019). Atypical behaviour and connectivity in SHANK3-mutant macaques. Nature, 570(7761), 326–331.PubMedCrossRef
Metadata
Title
Population-Average Brain Templates and Application to Automated Voxel-Wise Analysis Pipelines for Cynomolgus Macaque
Authors
Fubing Ouyang
Xinran Chen
Jiahui Liang
Jianle Li
Zimu Jiang
Yicong Chen
Zhicong Yan
Jinsheng Zeng
Shihui Xing
Publication date
14-09-2021
Publisher
Springer US
Published in
Neuroinformatics / Issue 3/2022
Print ISSN: 1539-2791
Electronic ISSN: 1559-0089
DOI
https://doi.org/10.1007/s12021-021-09545-4

Other articles of this Issue 3/2022

Neuroinformatics 3/2022 Go to the issue

Premium Partner