Skip to main content

T1 mapping of the mouse brain following fractionated manganese administration using MP2RAGE

Brain Structure and Function volume 222, pages 201–214 (2017)Cite this article

Abstract

With the increasing development of transgenic mouse models of neurodegenerative diseases allowing improved understanding of the underlying mechanisms of these disorders, robust quantitative mapping techniques are also needed in rodents. MP2RAGE has shown great potential for structural imaging in humans at high fields. In the present work, MP2RAGE was successfully implemented at 9.4T and 14.1T. Following fractionated injections of MnCl2, MP2RAGE images were acquired allowing simultaneous depiction and T1 mapping of structures in the mouse brain at both fields. In addition, T1 maps demonstrated significant T1 shortenings in different structures of the mouse brain (p < 0.0008 at 9.4T, p < 0.000001 at 14.1T). T1 values recovered to the levels of saline-injected animals 1 month after the last injection except in the pituitary gland. We believe that MP2RAGE represents an important prospective translational tool for further structural MRI.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Abbreviations

MP2RAGE:

Magnetization-prepared 2 rapid acquisition gradient echo sequence

MEMRI:

Manganese-enhanced MRI

FLASH:

Fast-low angle shot

SNR:

Signal-to noise-ratio

CNR:

Contrast-to-noise ratio

GRE:

Gradient echo

FASTMAP:

Fast, automatic shimming technique by mapping along projections

References

  • Allemang-Grand R, Scholz J, Ellegood J, Cahill LS, Laliberté C, Fraser PE, Josselyn SA, Sled JG, Lerch JP (2015) Altered brain development in an early-onset murine model of Alzheimer’s disease. Neurobiol Aging 36(2):638–647. doi:10.1016/j.neurobiolaging.2014.08.032

    CAS  Article  PubMed  Google Scholar 

  • Auffret M, Samim I, Lepore M, Gruetter R, Just N (2014) Quantitative activity-induced manganese-dependent MRI for characterizing cortical layers in the primary somatosensory cortex of the rat. Brain Struct Funct 221(2):695–707

    Article  PubMed  Google Scholar 

  • Bertrand A, Khan U, Hoang DM, Novikov DS, Krishnamurthy P, Rajamohamed Sait HB, Little BW, Sigurdsson EM, Wadghiri YZ (2013) Non-invasive, in vivo monitoring of neuronal transport impairment in a mouse model of tauopathy using MEMRI. Neuroimage 64:693–702. doi:10.1016/j.neuroimage.2012.08.065

    Article  PubMed  Google Scholar 

  • Bock NA, Paiva FF, Silva AC (2008) Fractionated manganese-enhanced MRI. NMR Biomed 21(5):473–478

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Botsikas D, Terraz S, Vinet L, Lamprianou S, Becker CD, Bosco D, Meda P, Montet X (2012) Pancreatic magnetic resonance imaging after manganese injection distinguishes type 2 diabetic and normoglycemic patients. Islets 4(3):243–248. doi:10.4161/isl.20857

    Article  PubMed  PubMed Central  Google Scholar 

  • Callahan JW, Abercrombie ED (2015) Age-dependent alterations in the cortical entrainment of subthalamic nucleus neurons in the YAC128 mouse model of Huntington’s disease. Neurobiol Dis 78:88–99. doi:10.1016/j.nbd.2015.03.006

    CAS  Article  PubMed  Google Scholar 

  • Canals S, Beyerlein M, Keller AL, Murayama Y, Logothetis NK (2008) Magnetic resonance imaging of cortical connectivity in vivo. Neuroimage 40(2):458–472. doi:10.1016/j.neuroimage.2007.12.007

    CAS  Article  PubMed  Google Scholar 

  • Chen MC, Ferrari L, Sacchet MD, Foland-Ross LC, Qiu MH, Gotlib IH, Fuller PM, Arrigoni E, Lu J (2015) Identification of a direct GABAergic pallidocortical pathway in rodents. Eur J Neurosci 41(6):748–759. doi:10.1111/ejn.12822

    Article  PubMed  PubMed Central  Google Scholar 

  • Cheng T, Magill AW, Comment A, Lei H (2014) Ultra-high field birdcage coils: a comparison study at 14.1T. Conf Proc IEEE Eng Med Biol Soc 2014:2360–2363. doi:10.1109/EMBC.2014.6944095

    Google Scholar 

  • Chuang KH, Koretsky A (2006) Improved neuronal tract tracing using manganese enhanced magnetic resonance imaging with fast T(1) mapping. Magn Reson Med 55(3):604–611

    CAS  Article  PubMed  Google Scholar 

  • Dolgan A, Budrewicz S, Koszewicz M, Bladowska J, Slotwinski K, Zagrajek M, Koziorowska-Gawron E, Podemski R (2015) Acute hyperkinetic syndrome due to ephedrone abuse. J Addict Med 9(3):244–245. doi:10.1097/ADM.0000000000000048

    Article  PubMed  Google Scholar 

  • Eggenschwiler F, Kober T, Magill AW, Gruetter R (2012) Marques JP.SA2RAGE: a new sequence for fast B1 + -mapping. Magn Reson Med 67(6):1609–1619. doi:10.1002/mrm.23145

    CAS  Article  PubMed  Google Scholar 

  • Gizewski ER, Maderwald S, Linn J, Dassinger B, Bochmann K, Forsting M, Ladd ME (2014) High-resolution anatomy of the human brain stem using 7-T MRI: improved detection of inner structures and nerves? Neuroradiology 56(3):177–186. doi:10.1007/s00234-013-1312-0

    Article  PubMed  Google Scholar 

  • Grünecker B, Kaltwasser SF, Zappe AC, Bedenk BT, Bicker Y, Spoormaker VI, Wotjak CT, Czisch M (2013) Regional specificity of manganese accumulation and clearance in the mouse brain: implications for manganese-enhanced MRI. NMR Biomed 26:542–556

    Article  PubMed  Google Scholar 

  • Grünecker B, Kaltwasser SF, Peterse Y, Zappe AC, Bedenk BT, Bicker Y, Spoormaker VI, Wotjak CT, Czisch M (2010) Fractionated manganese injections: effects on MRI contrast enhancement and physiological measures in C57BL/6 mice. NMR Biomed 23(8):913–921. doi:10.1002/nbm.1508

    Article  PubMed  Google Scholar 

  • Just N, Gruetter R (2011) Detection of neuronal activity and metabolism in a model of dehydration-induced anorexia in rats at 14.1 T using manganese-enhanced MRI and 1H MRS. NMR Biomed 24(10):1326–1336. doi:10.1002/nbm.1694

    CAS  Article  PubMed  Google Scholar 

  • Just N, Cudalbu C, Lei H, Gruetter R (2011) Effect of manganese chloride on the neurochemical profile of the rat hypothalamus. J Cereb Blood Flow Metab 31(12):2324–2333. doi:10.1038/jcbfm.2011.92

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Kober T, Granziera C, Ribes D, Browaeys P, Schluep M, Meuli R, Frackowiak R, Gruetter R, Krueger G (2012) MP2RAGE multiple sclerosis magnetic resonance imaging at 3 T. Invest Radiol 47(6):346–352. doi:10.1097/RLI.0b013e31824600e9

    Article  PubMed  Google Scholar 

  • Labadie C, Lee JH, Rooney WD, Jarchow S, Aubert-Frécon M, Springer CS Jr, Möller HE (2014) Myelin water mapping by spatially regularized longitudinal relaxographic imaging at high magnetic fields. Magn Reson Med 71(1):375–387. doi:10.1002/mrm.24670

    Article  PubMed  Google Scholar 

  • Lee JH, Silva AC, Merkle H, Koretsky AP (2005) Manganese-enhanced magnetic resonance imaging of mouse brain after systemic administration of MnCl2: dose-dependent and temporal evolution of T1 contrast. Magn Reson Med 53(3):640–648

    CAS  Article  PubMed  Google Scholar 

  • Liu JV, Bock NA, Silva AC (2011) Rapid high-resolution three-dimensional mapping of T1 and age-dependent variations in the non-human primate brain using magnetization-prepared rapid gradient-echo (MPRAGE) sequence. Neuroimage 56(3):1154–1163. doi:10.1016/j.neuroimage.2011.02.075

    Article  PubMed  PubMed Central  Google Scholar 

  • Maddage R, Marques J, Gruetter R (2014) Phase-based manganese-enhanced MRI, a new methodology to enhance brain cyto architectural contrast and study manganese uptake. Magn Reson Med 72:1246–1256

    Article  PubMed  Google Scholar 

  • Marques JP, Gruetter R (2013) New developments and applications of the MP2RAGE sequence–focusing the contrast and high spatial resolution R1 mapping. PLoS One 8(7):e69294. doi:10.1371/journal.pone.0069294

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Marques JP, Kober T, Krueger G, van der Zwaag W, Van de Moortele PF, Gruetter R (2010) MP2RAGE, a self bias-field corrected sequence for improved segmentation and T1-mapping at high field. Neuroimage 49(2):1271–1281. doi:10.1016/j.neuroimage.2009.10.002

    Article  PubMed  Google Scholar 

  • O’Brien KR, Kober T, Hagmann P, Maeder P, Marques J, Lazeyras F, Krueger G, Roche A (2014) Robust T1-weighted structural brain imaging and morphometry at 7T using MP2RAGE. PLoS One 9(6):e99676. doi:10.1371/journal.pone.0099676

    Article  PubMed  PubMed Central  Google Scholar 

  • Patrick PS, Rodrigues TB, Kettunen MI, Lyons SK, Neves AA, Brindle KM (2015) Development of Timd2 as a reporter gene for MRI. Magn Reson Med. doi:10.1002/mrm.25750

    PubMed Central  Google Scholar 

  • Paxinos G, Watson C (1998) The rat stereotaxic coordinates. Academic Press, San Diego

    Google Scholar 

  • Piędzia W, Jasiński K, Kalita K, Tomanek B, Węglarz WP (2014) White and gray matter contrast enhancement in MR images of the mouse brain in vivo using IR UTE with a cryo-coil at 9.4 T. J Neurosci Methods 30(232):30–35. doi:10.1016/j.jneumeth.2014.04.019

    Article  Google Scholar 

  • Rajan J, Poot D, Juntu J, Sijbers J (2010) Noise measurement from magnitude MRI using local estimates of variance and skewness. Phys Med Biol 55:N441–N449

    Article  PubMed  Google Scholar 

  • Schaefer S, Vogt T, Nowak T, Kann PH, German KIMS board (2008) Pituitary function and the somatotrophic system in patients with idiopathic Parkinson’s disease under chronic dopaminergic therapy. J Neuroendocrinol 20(1):104–109

    CAS  Article  PubMed  Google Scholar 

  • Sepúlveda MR, Dresselaers T, Vangheluwe P, Everaerts W, Himmelreich U, Mata AM, Wuytack F (2012) Evaluation of manganese uptake and toxicity in mouse brain during continuous MnCl2 administration using osmotic pumps. Contrast Media Mol Imaging 7(4):426–434. doi:10.1002/cmmi.1469

    Article  PubMed  Google Scholar 

  • Silva AC, Lee JH, Aoki I, Koretsky AP (2004) Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed 17:532–543

    CAS  Article  PubMed  Google Scholar 

  • Silva AC, Lee JH, Wu CW, Tucciarone J, Pelled G, Aoki I, Koretsky AP (2008) Detection of cortical laminar architecture using manganese-enhanced MRI. J Neurosci Methods 167(2):246–257

    CAS  Article  PubMed  Google Scholar 

  • Strotmann B, Heidemann RM, Anwander A, Weiss M, Trampel R, Villringer A, Turner R (2014) High-resolution MRI and diffusion-weighted imaging of the human habenula at 7 tesla. J Magn Reson Imaging 39(4):1018–1026. doi:10.1002/jmri.24252

    Article  PubMed  Google Scholar 

  • Thiessen JD, Zhang Y, Zhang H, Wang L, Buist R, Del Bigio MR, Kong J, Li XM, Martin M (2013) Quantitative MRI and ultrastructural examination of the cuprizone mouse model of demyelination. NMR Biomed 26(11):1562–1581. doi:10.1002/nbm.2992

    CAS  Article  PubMed  Google Scholar 

  • Tkác I, Henry PG, Andersen P, Keene CD, Low WC, Gruetter R (2004) Highly resolved in vivo 1H NMR spectroscopy of the mouse brain at 9.4 T. Magn Reson Med 52(3):478–484

    Article  PubMed  Google Scholar 

  • van de Ven RC, Hogers B, van den Maagdenberg AM, de Groot HJ, Ferrari MD, Frants RR, Poelmann RE, van der Weerd L, Kiihne SR (2007) T(1) relaxation in in vivo mouse brain at ultra-high field. Magn Reson Med 58(2):390–395

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Centre d’ Imagerie Biomédicale (CIBM) and Ecole Polytechnique Fédérale de Lausanne (EPFL). We would like to thank Professor Rolf Gruetter for contributing to the animals, materials and analysis tools, Dr Olivier Reynaud for programming the reconstruction macros and Dr José Marques for the few useful discussions and for sharing his programming tools.

Author information

Affiliations

  1. CIBM-AIT Core, Ecole Polytechnique Fédérale de Lausanne, Lausanne, Switzerland

    Luc Driencourt, Carola Jacqueline Romero, Mario Lepore, Florent Eggenschwiler, Olivier Reynaud & Nathalie Just

  2. Institut für Klinische Radiologie, Translational Research Imaging Center (TRIC), Albert-Schweitzer-Campus 1, Gebäude A16, Anfahrt: Waldeyerstr. 1, 48149, Münster, Germany

    Nathalie Just

Authors
  1. Luc Driencourt
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carola Jacqueline Romero
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mario Lepore
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Florent Eggenschwiler
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Olivier Reynaud
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Nathalie Just
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nathalie Just.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Driencourt, L., Romero, C.J., Lepore, M. et al. T1 mapping of the mouse brain following fractionated manganese administration using MP2RAGE. Brain Struct Funct 222, 201–214 (2017). https://doi.org/10.1007/s00429-016-1211-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-016-1211-3

Keywords

  • T1 relaxation
  • Mouse
  • MEMRI
  • High resolution
  • Translational