Three‐dimensional, in vivo MRI with self‐gating and image coregistration in the mouse

Motion during magnetic resonance imaging (MRI) scans routinely results in undesirable image artifact or blurring. Since high‐resolution, three‐dimensional (3D) imaging of the mouse requires long scan times for satisfactory signal‐to‐noise ratio (SNR) and image quality, motion‐related artifacts are likely over much of the body and limit applications of mouse MRI. In this investigation, we explored the use of self‐gated imaging methods and image coregistration for improving image quality in the presence of motion. Self‐gated signal results from a modified 3D gradient‐echo sequence showed detection of periodic respiratory and cardiac motion in the adult mouse—with excellent comparison to traditional measurements, sensitivity to respiration‐induced tissue changes in the brain, and even detection of embryonic cardiac motion in utero. Serial image coregistration with rapidly‐acquired, low‐SNR volumes further enabled detection and correction of bulk changes in embryo location during in utero imaging sessions and subsequent reconstruction of high‐quality images. These methods, in combination, are shown to expand the range of applications for 3D mouse MRI, enabling late‐stage embryonic heart imaging and introducing the possibility of longitudinal developmental studies from embryonic stages through adulthood. Magn Reson Med, 2009. © 2009 Wiley‐Liss, Inc.

[1]  Jeff W M Bulte,et al.  Iron oxide MR contrast agents for molecular and cellular imaging , 2004, NMR in biomedicine.

[2]  Pierre Croisille,et al.  Cardiac and respiratory double self‐gated cine MRI in the mouse at 7 T , 2006, Magnetic resonance in medicine.

[3]  Florence Franconi,et al.  In utero time-course assessment of mouse embryo development using high resolution magnetic resonance imaging , 2002, Anatomy and Embryology.

[4]  X Hu,et al.  Retrospective estimation and correction of physiological artifacts in fMRI by direct extraction of physiological activity from MR data , 1996, Magnetic resonance in medicine.

[5]  Jonathon Bishop,et al.  Magnetic resonance imaging for detection and analysis of mouse phenotypes , 2005, NMR in biomedicine.

[6]  Susumu Mori,et al.  MRI in mouse developmental biology , 2007, NMR in biomedicine.

[7]  D. Hill,et al.  Whole‐heart cine MRI using real‐time respiratory self‐gating , 2007, Magnetic resonance in medicine.

[8]  J. Felmlee,et al.  Orbital navigator echoes for motion measurements in magnetic resonance imaging , 1995, Magnetic resonance in medicine.

[9]  Mangala Srinivas,et al.  Magnetic resonance imaging of embryonic and fetal development in model systems. , 2006, Methods in molecular medicine.

[10]  Erik M. Shapiro,et al.  Cellular magnetic resonance imaging: Nanometer and micrometer size particles for noninvasive cell localization , 2007, Neurotherapeutics.

[11]  C R Meyer,et al.  Motion correction in fMRI via registration of individual slices into an anatomical volume , 1999, Magnetic resonance in medicine.

[12]  A Haase,et al.  Developmental changes of cardiac function and mass assessed with MRI in neonatal, juvenile, and adult mice. , 2000, American journal of physiology. Heart and circulatory physiology.

[13]  Mathias Hoehn,et al.  Improved Stem Cell MR Detectability in Animal Models by Modification of the Inhalation Gas , 2005, Molecular imaging.

[14]  R L Ehman,et al.  Spatial presaturation: a method for suppressing flow artifacts and improving depiction of vascular anatomy in MR imaging. , 1987, Radiology.

[15]  G. Glover,et al.  Self‐navigated spiral fMRI: Interleaved versus single‐shot , 1998, Magnetic resonance in medicine.

[16]  Clifford R. Jack,et al.  Spherical navigator echoes for full 3D rigid body motion measurement in MRI , 2001, SPIE Medical Imaging.

[17]  Luis C. Maas,et al.  Decoupled automated rotational and translational registration for functional MRI time series data: The dart registration algorithm , 1997, Magnetic resonance in medicine.

[18]  Bob S. Hu,et al.  Real‐time black‐blood MRI using spatial presaturation , 2001, Journal of magnetic resonance imaging : JMRI.

[19]  Klaas Nicolay,et al.  Comparison between prospective and retrospective triggering for mouse cardiac MRI , 2007, NMR in biomedicine.

[20]  Gabriele Lohmann,et al.  On Multivariate Spectral Analysis of fMRI Time Series , 2001, NeuroImage.

[21]  N. Richard,et al.  Cardiac and respiratory self‐gated cine MRI in the mouse: Comparison between radial and rectilinear techniques at 7T , 2007, Magnetic resonance in medicine.

[22]  J C Gore,et al.  Analysis and correction of motion artifacts in diffusion weighted imaging , 1994, Magnetic resonance in medicine.

[23]  R E Poelmann,et al.  Magnetic resonance microscopy of mouse embryos in utero , 2000, The Anatomical record.

[24]  M. F. Falangola,et al.  Quantitative MRI reveals aging‐associated T2 changes in mouse models of Alzheimer's disease , 2007, NMR in biomedicine.

[25]  Keren Ziv,et al.  MRI detection of transcriptional regulation of gene expression in transgenic mice , 2007, Nature Medicine.

[26]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[27]  Clayton E. Curtis,et al.  Coherence between fMRI time-series distinguishes two spatial working memory networks , 2005, NeuroImage.

[28]  A. Brau,et al.  Generalized self‐navigated motion detection technique: Preliminary investigation in abdominal imaging , 2006, Magnetic resonance in medicine.

[29]  J Keegan,et al.  Navigator echoes in cardiac magnetic resonance. , 2001, Journal of cardiovascular magnetic resonance : official journal of the Society for Cardiovascular Magnetic Resonance.

[30]  J. Bell,et al.  Cardiac structure and function during ageing in energetically compromised Guanidinoacetate N-methyltransferase (GAMT)-knockout mice – a one year longitudinal MRI study , 2008, Journal of cardiovascular magnetic resonance : official journal of the Society for Cardiovascular Magnetic Resonance.

[31]  Alan C. Evans,et al.  Longitudinal neuroanatomical changes determined by deformation-based morphometry in a mouse model of Alzheimer's disease , 2008, NeuroImage.

[32]  D. Louis Collins,et al.  Automatic 3‐D model‐based neuroanatomical segmentation , 1995 .

[33]  Alan C. Evans,et al.  Cortical thickness measured from MRI in the YAC128 mouse model of Huntington's disease , 2008, NeuroImage.

[34]  Todd S. Sachs,et al.  Real‐time motion detection in spiral MRI using navigators , 1994, Magnetic resonance in medicine.

[35]  V. Ferrari,et al.  Imaging the embryonic heart: how low can we go? How fast can we get? , 2003, Journal of molecular and cellular cardiology.

[36]  X. Hu,et al.  Reduction of signal fluctuation in functional MRI using navigator echoes , 1994, Magnetic resonance in medicine.

[37]  R. Henkelman,et al.  Mouse behavioral mutants have neuroimaging abnormalities , 2007, Human brain mapping.

[38]  Chris Heyn,et al.  In vivo magnetic resonance imaging of single cells in mouse brain with optical validation , 2006, Magnetic resonance in medicine.

[39]  Alan P. Koretsky,et al.  Magnetic resonance imaging of the migration of neuronal precursors generated in the adult rodent brain , 2006, NeuroImage.

[40]  Youssef Zaim Wadghiri,et al.  Mn enhancement and respiratory gating for in utero MRI of the embryonic mouse central nervous system , 2008, Magnetic resonance in medicine.

[41]  Michael Brady,et al.  Analysis of dynamic MR breast images using a model of contrast enhancement , 1997, Medical Image Anal..

[42]  Andrew C Larson,et al.  Self‐gated cardiac cine MRI , 2004, Magnetic resonance in medicine.

[43]  J. Pipe Motion correction with PROPELLER MRI: Application to head motion and free‐breathing cardiac imaging , 1999, Magnetic resonance in medicine.

[44]  G H Glover,et al.  Three‐dimensional spiral fMRI technique: A comparison with 2D spiral acquisition , 1998, Magnetic resonance in medicine.

[45]  Z H Cho,et al.  Extraction of cardiac and respiratory motion cycles by use of projection data and its applications to nmr imaging , 1990, Magnetic resonance in medicine.

[46]  Jun Dazai,et al.  Retrospective gating for mouse cardiac MRI , 2006, Magnetic resonance in medicine.